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HEART 1002 7 NOITCES Aortic valve, left coronary leaflet Fig. 57.17 A dissection opening the ventricles, viewed from the front. (With Aortic valve, permission from Waschke J, Paulsen F Left atrium non-adjacent leaflet (eds), Sobotta Atlas of Human Anatomy, 15th ed, Elsevier, Urban & Ascending aorta Fischer. Copyright 2013.) Aortic leaflet Mitral valve Aortic sinus Mural leaflet Right auricle Right coronary artery Interventricular septum, Pericardium membranous part Superolateral papillary muscle Tricuspid valve, inferior leaflet Tricuspid valve, Inferoseptal papillary muscle septal leaflet Pericardium Anterior papillary muscle Inferior papillary muscle Interventricular septum, muscular part Right coronary artery Subpulmonary infundibulum Pulmonary trunk Supraventricular crest Medial papillary muscle Aorta Septomarginal trabeculation Superior vena cava Septoparietal trabeculations Venous component Anterior pM ao pd ile lar ra yt o mr ub sa cn ld e V e Fossa ovalis stib ule Inferior papillary muscle Inferior vena cava Tricuspid valve Thebesian valve Eustachian valve Coronary sinus Sub-Thebesian recess Fig. 57.18 A ‘window dissection’ of a cadaveric heart, prepared by removing the anterosuperior wall of the right atrium and ventricle, to expose their internal features. The Eustachian valve separates the inferior vena cava from the sub-Thebesian recess. The Thebesian valve guards the entry into the coronary sinus. The smooth circumferential area of atrial wall that surrounds the orifice of the tricuspid valve is the vestibule. Note the location of the supraventricular crest and septomarginal trabeculation. The body of the septomarginal trabeculation continues as an important muscular strand, the moderator band, to the anterior papillary muscle and the parietal wall of the right ventricle. (Specimen courtesy of M Loukas MD, PhD.) anterolateral right ventricular wall. The posterolateral aspect of the crest caused by a myriad of endocardial, lined, irregular muscular ridges and provides a principal attachment for the anterosuperior leaflet of the protrusions collectively known as trabeculae carneae. These protrusions tricuspid valve. The septal limb of the crest may be continuous with, or and intervening grooves impart great variation in wall thickness; the embraced by, the septal limbs of the septomarginal trabeculation. The protrusions vary in extent from mere ridges to trabeculations, fixed at inlet and outlet regions extend apically into and from the prominent both ends but otherwise free. Other conspicuous protrusions are the coarsely trabeculated component of the ventricle. The inlet component papillary muscles, which are inserted at one end on to the ventricular itself is also trabeculated, whereas the outlet component (infundibu- wall and are continuous at the other end with collagenous cords, the lum) has predominantly smooth walls. The trabeculated appearance is chordae tendineae (tendinous cords), inserted on the free edge of the
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Heart 1003 75 RETPAHC atrioventricular valves. One protrusion in the right ventricle, the septo- leaflets. The connective tissues around the orifice of the atrioventricular marginal trabeculation or septal band, is particularly prominent, rein- valves separate the atrial and ventricular myocardial masses completely, forcing the septal surface where, at the base, it divides into limbs that except at the point of penetration of the atrioventricular bundle; they embrace the supraventricular crest. Towards the apex, it supports the vary in density and disposition around the valvular circumference. anterior papillary muscle of the tricuspid valve and, from this point, Extending from the right fibrous trigone component of the central crosses to the parietal wall of the ventricle as the moderator band (the fibrous body is a pair of curved, tapered, subendocardial tendons, or name reflects an earlier idea that septomarginal trabeculation prevented ‘prongs’ (fila coronaria), which partly encircle the circumference. The overdistension of the ventricle). The role of the moderator band as part latter is completed by more tenuous, deformable fibroblastic sulcal of the conduction system of the heart involves the right atrioventricular areolar tissue. Although the extent of fibrous tissue varies with sex and bundle, as conduction cardiomyocytes move towards the apex of the age, the tissue within the atrioventricular junction around the tricuspid ventricle before entering the anterior papillary muscle. The moderator orifice is always less robust than similar elements found at the attach- band may be short/thick, long/thick, short/thin, long/thin: it is occa- ments of the mitral valve. The topographical ‘attachment’ of the free sionally absent. A further series of prominent trabeculations, the septo- valvular leaflets in the tricuspid valve does not wholly correspond to parietal trabeculations, extend from its anterior surface and run on to the internal level of attachment of the fibrous core of the valve to the the parietal ventricular wall. The smooth-walled outflow tract, or junctional atrioventricular connective tissue. The line of attachment of infundibulum, ascends to the left, superior to the septoparietal trabecu- the leaflet is best appreciated in the heart when examined grossly, this lations and inferior to the arch of the supraventricular crest to the feature being more readily discerned clinically. pulmonary orifice (Spicer and Anderson 2013). Tricuspid valve leaflets Tricuspid valve When they are closed, it is usually possible to distinguish the three The atrioventricular valvular complex, in both ventricles, consists of the leaflets in the tricuspid valve on the basis of the zones of apposition orifice and its associated anulus, the leaflets, the supporting chordae between them: hence the name. The leaflets are located anterosuperi- tendineae of various types and the papillary muscles. Harmonious orly, septally and inferiorly, corresponding to the marginal sectors of interplay of all of these, together with the myocardial mass, depends the atrioventricular orifice named in conjunction. The inferior leaflet is on the conduction tissues and mechanical cohesion provided by the often described as being posterior, but when assessed in the attitudi- cardiac skeleton. All parts change substantially in position, shape, angu- nally correct anatomical position, the leaflet is positioned inferiorly lation and dimensions during the cardiac cycle (see Fig. 57.20). (Anderson and Loukas 2009). Each leaflet is a reduplication of endo- cardium enclosing a collagenous core, continuous marginally and on Tricuspid valvular orifice its ventricular aspect with diverging fascicles of chordae tendineae (see The tricuspid valve orifice is best seen from the atrial aspect. It measures, below) and basally confluent with the anular connective tissue. In on average, 11.4 cm in circumference in males and 10.8 cm in females. passing from the free margin to the inserted margin, all leaflets of the There is a clear line of transition from the atrial wall or septum to the atrioventricular valves display rough, clear and basal zones. The rough lines of attachment of the valvular leaflets. Its margins are not precisely zone is relatively thick, opaque and uneven on its ventricular aspect in a single plane. It is almost vertical but at 45° to the sagittal plane where most chordae tendineae are attached; its atrial aspect makes and slightly inclined to the vertical, such that it ‘faces’ (on its ventricular contact with the comparable surface of the adjacent leaflets during full aspect) anterolaterally to the left and somewhat inferiorly (Fig. 57.19). valve closure. The clear zone is smooth and translucent, receives few Roughly triangular, its margins are described as anterosuperior, inferior chordae tendineae and has a thinner, fibrous core. The basal zone, and septal, corresponding to the lines of attachment of the valvular extending 2–3 mm from the circumferential attachment of the leaflets, is thicker from increased connective tissue, vascularized and innervated. It contains the insertions of the atrial myocardium. The anterosuperior leaflet is the largest component of the tricuspid valve, attached chiefly to the atrioventricular junction on the posterolateral aspect of the supraventricular crest, and extending along its septal limb to the mem- 1 1 branous septum ending at the anteroseptal commissure. One or more notches often indent its free margin. The attachment of the septal leaflet passes from the inferoseptal commissure on the inferior ventricular wall across the muscular septum, then angling across the membranous 2 2 septum to the anteroseptal commissure. The septal leaflet defines one of the borders of the triangle of Koch, thereby aiding location of the A P atrioventricular node at the apex of this triangle, and ensuring avoid- P 3 3 ance during tricuspid valve surgery (see Figs 57.13, 57.17). The inferior leaflet is wholly mural in attachment and guards the diaphragmatic surface of the atrioventricular junction, its limits being the inferoseptal A and anteroinferior commissures. The zone of apposition between the 4 M 4 inferior and the anterosuperior leaflets is supported by the septal papil- lary muscle of the conus. T Opening of the tricuspid valve 5 5 Despite its name, the tricuspid valve acts more like a bicuspid valve T because its smallest septal leaflet is fixed between the atrial and ven- M tricular septa. The remainder of the tricuspid anulus is muscular. During diastole, the anulus dilates with right ventricular relaxation and the 6 6 large anterior and posterior leaflets move away from the plane of the anulus into the right ventricle. During systole, the anulus constricts as the right ventricle contracts and the two major leaflets move like sails about a relatively immobile septal leaflet and the septum itself 7 7 (Fig. 57.20). Chordae tendineae (tendinous cords) The chordae tendineae are fibrous collagenous structures that support Fig. 57.19 The relation of the sternocostal surface and valves of the heart the leaflets of the atrioventricular valves. Sometimes, false chordae to the thoracic cage. The right heart is blue, the arrow denoting the inflow connect the papillary muscles to each other or to the ventricular wall and outflow channels of the right ventricle; the left heart is treated or septum, or pass directly between points on the wall or septum, or similarly in red. The positions, planes and relative sizes of the cardiac valves are shown. The position of the letters A, P, T and M indicate the both. Their numbers and dimensions vary in the right ventricle; approx- aortic, pulmonary, tricuspid and mitral auscultation areas of clinical imately 40% of these false cords contain conduction cardiomyocytes. practice, respectively. Note that, for the purpose of illustration, the orifices The true chordae usually arise from small projections on the tips or of the aortic, mitral and tricuspid valves are shown with some separation margins of the apical third of papillary muscles, although they some- between them, whereas, in reality, the leaflets of the three valves are in times arise from the papillary muscle bases or directly from the ven- fibrous continuity (see Fig. 57.24). tricular walls and septum. They attach to various parts of the ventricular
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HEART 1004 7 NOITCES aspects or the free margins of the leaflets. True chordae are classified ventricular aspect) of the zones of apposition between leaflets and to into first-, second- and third-order types, according to the distance of the ends of adjacent leaflets. Rough-zone chordae arise from a single the attachment from the margins of the leaflets; the scheme has little stem that usually splits into three components that attach to the free functional or morphological merit. Fan-shaped chordae have a short margin, the ventricular aspect of the rough zone and to some intermedi- stem from which branches radiate to attach to the margins (or the ate point on the leaflet, respectively. Free-edge chordae are single, thread-like and often long, passing from either the apex or the base of 120 a papillary muscle into a marginal attachment, usually near the mid- point of a leaflet or one of its scallops. Deep chordae pass beyond the 100 margins and, branching to various extents, reach the more peripheral Aorta Pressure 80 rough zone or even the clear zone. Basal chordae are round or ribbon- (mmHg) like, long and slender, or short and muscular; they arise from the 60 in left side smooth or trabeculated ventricular wall and attach to the basal compo- of heart 40 nent of a leaflet. Left atrium 20 Left venticle Papillary muscles Pressure 0 The two major papillary muscles in the right ventricle are located in (mmHg) 20 Pulmonary artery anterior and inferior positions. A third, smaller muscle lies medially, in right side 0 Right atrium together with several smaller, variable muscles attached to the ventricu- of heart Right ventricle lar septum. The anterior papillary muscle is the largest, its base arising Atrium Ventricle from the right anterolateral ventricular wall inferior to the anteroinfe- Mechanical Left Ejection Stipple marks isometric rior commissure of the inferior leaflet, also blending with the right end activity Right Ejection contraction and relaxation of the septomarginal trabecula. The inferior, papillary muscle, often bifid or trifid, arises from the myocardium inferior to the inferoseptal Sequence of commissure. The septal (medial) papillary muscle of the conus, the valve motion muscle of Lancisi, is almost always present and is the most superior and largest of the small septal papillary muscles. It arises from the posterior Closure of 1 5 Closure of septal limb of the septomarginal trabeculation and locates the right mitral valve aortic valve bundle branch within the right ventricle. All the major papillary 6 Closure of muscles supply chordae to adjacent components of the leaflets they Closure of 2 pulmonary support (see Figs 57.17, 57.18). A feature of the right ventricle is that tricuspid valve valve the septal leaflet is tethered by individual chordae tendineae directly to the ventricular septum; such septal insertions are never seen in the left 7 Opening of ventricle. When closed, the three leaflets fit snugly together, the pattern tricuspid of the zones of apposition confirming the trifoliate arrangement of the valve Opening of 3 tricuspid valve. pulmonary valve 8 Opening of Pulmonary valve mitral valve Opening of 4 The pulmonary valve, guarding the outflow from the right ventricle, aortic valve surmounts the infundibulum and is situated at some distance from the other three cardiac valves (Figs 57.21, 57.23). Its general plane faces superiorly to the left and slightly posteriorly. It has three semilunar Phonocardiogram First heart Second heart leaflets, attached by convex edges partly to the infundibular wall of the sound sound right ventricle and partly to the origin of the pulmonary trunk. The line R Electrocardiogram P T of attachments is curved, rising at the periphery of each leaflet near their Q S zones of apposition (the commissures) and reaching the sinutubular 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 ridge of the pulmonary trunk (Fig. 57.24). Removal of the leaflets Time (seconds) reveals that the fibrous semilunar attachments enclose three crescents Fig. 57.20 A summary of some of the principal events that occur in of infundibular musculature within the pulmonary sinuses, whereas the cardiac cycle and that are mentioned at various points throughout three roughly triangular segments of arterial wall are incorporated this chapter. Systole begins at the onset of the first heart sound (see within the ventricular outflow tract beneath the apex of each commis- phonocardiogram) and ends at the onset of the second heart sound, sural attachment. Thus there is no proper circular ‘anulus’ supporting when diastole begins, and this cycle repeats itself. the leaflets of the valve, and the fibrous semilunar attachment is an Pulmonary trunk Fig. 57.21 The base of the ventricles, after removal of the atria and the pericardium, Non-adjacent Left coronary leaflet exposing the coronary arteries and cardiac veins. leaflet Contrast the planes and positions of the aortic Pulmonary valve Right adjacent Right coronary leaflet Aortic valve and pulmonary valves, and with Figure 57.23. leaflet (With permission from Waschke J, Paulsen F Left adjacent (eds), Sobotta Atlas of Human Anatomy, 15th ed, leaflet Non-adjacent leaflet Elsevier, Urban & Fischer. Copyright 2013.) Anterior interventricular branch Right coronary artery Left coronary artery Circumflex branch Right fibrous trigone Left fibrous trigone Right fibrous ring Great cardiac vein Atrioventricular bundle Left fibrous ring Valve of coronary sinus Right marginal branch Left marginal branch Middle cardiac vein Opening of coronary sinus Right coronary artery, Inferior interventricular vein inferior interventricular branch
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Heart 1005 75 RETPAHC essential requisite for snug closure of the nodules and lunules of the of the anatomical base of the heart and is approximately quadrangular, leaflets during ventricular diastole (see below). receiving the terminations of (usually) two pulmonary veins from each It is difficult to name the leaflets and corresponding sinuses of the lung, forming the anterior wall of the oblique pericardial sinus (see Fig. pulmonary valve and trunk precisely according to the coordinates of 57.3). This surface ends at the shallow vertical interatrial groove that the body because the valvular orifice is obliquely positioned. Termino- descends to the cardiac crux. logia Anatomica (2011) refers to anterior, posterior and septal leaflets on The left atrial appendage is characteristically longer, narrower and the basis of their fetal position but this changes with development, more hooked than the right, and is a finger-like extension with more becoming anterior, right and left, respectively, in the adult. Each leaflet deeply indented margins. It is constricted at its atrial junction and all is an endocardial fold with a variably developed intervening substantial its contained pectinate muscles are much smaller than their right coun- fibrous core that traverses both the free edge and the semilunar attached terparts. The left atrium lacks a crista terminalis, and the muscle bundles border. The latter is particularly thickened at its deepest central part in the appendage are arranged in a whorl-like fashion rather than being (nadir) of the base of each leaflet, and therefore never forms a simple in an array. The tip of the appendage has a variable position lying over complete fibrous ring. The free margin of each leaflet contains a central the pulmonary trunk and anterior interventricular artery, pointing pos- localized collagenous thickening, the nodule of Arantius. Perforations teriorly towards the aorta (Fig. 57.22). Its narrow morphology renders within the leaflets close to the free margin and near the commissures the left atrial appendage a potential site for deposition of thrombi. are frequently present and are of no functional significance. Each semi- The four pulmonary veins open into the superior posterolateral lunar leaflet is contained within one of the three sinuses of the pulmo- surfaces of the left atrium, two on each side (see Figs 57.3, 57.4B). This nary trunk. typical arrangement is present in 20–60% of the population. A common variation includes the presence of a short or long left common venous Opening of the pulmonary valve trunk and multiple pulmonary veins on the right (Fig. 57.25). The right During diastole, all three leaflets of the pulmonary valve are tightly pulmonary veins travel posterior to their respective venae cavae. Their apposed. The pulmonary valve is difficult to visualize at echocardio- orifices are smooth and oval, the left pair frequently opening via a graphy and usually only the posterior leaflet is visible when the valve common channel. Interpulmonary ridges are usually found between is closed; atrial systole may cause a slight posterior movement of the ipsilateral orifices; the most prominent is located between the openings valve leaflets. The pulmonary valve opens passively during ventricular of the left atrial appendage and left superior pulmonary vein. The ridges systole and then closes rapidly at the end of systole (see Fig. 57.20). are infoldings of the left atrial wall and contain adipose tissue, atrial arteries and nerve bundles. At the site of the pericardial reflection, the atrial musculature extends into the pulmonary veins, forming myocar- Left atrium dial sleeves that are thickest in the inferior wall of the superior pulmo- nary veins and the superior walls of the inferior pulmonary veins. They General, external and internal features lie external to the venous tunica media and internal to the epicardium/ Although smaller in volume than the right, the left atrium has thicker adventitia and are often the site of focal electrical activity that initiates walls (3 mm on average). It possesses a venous component that receives atrial fibrillation. Atrial myocardial bridges and crossing strands are the right and left superior and inferior pulmonary veins, a vestibule and often present, connecting the left superior and inferior pulmonary an appendage. Its cavity and walls are formed largely by the proximal veins. parts of the pulmonary veins that are incorporated into the atrium Several epicardial fat pads on the pulmonary venous component during development. Its extensive body is a remnant of the initial atrial house the superior left, posterolateral, left inferior and posteromedial component of the primary heart tube. The left atrium is roughly cuboi- ganglionated cardiac intrinsic nerve plexuses (typically four). Minimal dal, extending posterior to the right atrium and separated from it by cardiac veins (venae cordis minimae) return blood directly from the the obliquely positioned septum. The right atrium is therefore antero- myocardium to the left atrial cavity. The left atrial aspect of the septum lateral to the right part of the left atrium. The left part is concealed has a characteristically rough appearance, bounded by a crescentic, anteriorly by the initial segments of the pulmonary trunk and aorta: superiorly concave ridge that marks the site of the foramen ovale. The part of the transverse pericardial sinus lies between it and these arterial smooth circumferential area of atrial wall that surrounds the orifice of trunks. Anteroinferiorly, and to the left, it adjoins the base of the left the mitral valve is the vestibule (see Fig. 57.25A, Fig. 57.26). The mus- ventricle at the orifice of the mitral valve. Its posterior aspect forms most culature between the ostium of the inferior pulmonary vein and the Ligamentum arteriosum Fig. 57.22 The anterior or sternocostal surface of the Aortic arch heart. (With permission from Waschke J, Paulsen F (eds), Sobotta Atlas of Human Anatomy, 15th ed, Serous pericardium, parietal layer Superior vena cava Elsevier, Urban & Fischer. Copyright 2013.) Serous pericardium, Left pulmonary artery parietal layer Pulmonary trunk Right pulmonary artery Ascending aorta Left coronary artery Transverse Left atrium, left appendage pericardial sinus Great cardiac vein Right coronary artery Left coronary artery, circumflex branch Right appendage Infundibulum (conus Right atrium arteriosus) Left coronary artery, anterior interventricular branch Right ventricular veins Atrial branch Anterior interventricular vein Right marginal branch Apex of heart Notch of cardiac apex
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HEART 1006 7 NOITCES Arch of aorta Right pulmonary artery Pulmonary trunk Ascending aorta Tendon of infundibulum (conus ligament) Ostia of coronary arteries Fibrous attachment of pulmonary valve leaflets Fibrous attachment of aortic valve: Left coronary leaflet Left fibrous trigone Right coronary leaflet Non-adjacent leaflet Subaortic curtain and leaflet extension Line of aortic leaflet, Tendon of Todaro mitral valve Membranous part of septum MITRAL VALVE ANULUS Atrioventricular node Fila coronaria Line of septal leaflet, tricuspid valve Sulcal connective tissue TRICUSPID VALVE ANULUS Fila coronaria Sulcal connective tissue Mitral and aortic ‘anuli’ Right fibrous trigone Tricuspid and pulmonary ‘anuli’ (central fibrous body) Tendon of the infundibulum Fig. 57.23 Principal elements of the fibrous skeleton of the heart. For clarity, the view is from the right posterosuperior aspect. Perspective causes the pulmonary anulus to appear smaller than the aortic anulus, whereas, in fact, the reverse is the case. Consult the text for an extended discussion. (Copyright of The Royal College of Surgeons of England. Reproduced with permission.) anulus of the mitral valve is the left atrial or mitral isthmus, and is an The effect of obesity on the heart is apparent as early as the second year area where the vestibule of the left atrium directly opposes the wall of of life. Obese children aged 2 years have a greater left ventricular mass the great cardiac vein, coronary sinus and circumflex coronary artery. compared with normal weight controls (de Jonge et al 2011). Internal features Left ventricle The left ventricle has an inlet region guarded by the mitral valve (ostium venosum), an outlet region guarded by the aortic valve (ostium arterio- General and external features sum) and an apical trabecular component. The left atrioventricular The left ventricle is constructed in accordance with its role as a powerful orifice admits atrial blood during diastole, the flow being directed pump for the high-pressured systemic arterial circulation. Variously towards the cardiac apex (Fig. 57.28). After closure of the mitral leaflets described as half-ellipsoid or cone-shaped, it is longer and narrower and throughout the ejection phase of systole, blood is expelled from than the right ventricle, extending from its base in the plane of the the apex through the aortic orifice. In contrast to the orifices within the atrioventricular groove to the cardiac apex. Its long axis descends ante- right ventricle, those of the left ventricle are in close contact with riorly and to the left. In transverse section, at right angles to the axis, fibrous continuity between the leaflets of the aortic and mitral valves its cavity is oval or nearly circular, with walls three times thicker (the ‘subaortic curtain’) (Fig. 57.29); the inlet and outlet turn sharply (8–12 mm) than those of the right ventricle (Fig. 57.27). It forms part round this fibrous curtain. The anterolateral wall is the muscular ven- of the sternocostal, left and inferior (diaphragmatic) cardiac surfaces. tricular septum, the convexity of which completes the circular outline Except where obscured by the aorta and pulmonary trunk, the base of of the left ventricle (see Fig. 57.27). Towards the aortic orifice, the the ventricular cone is superficially separated from the left atrium by septum becomes the thin and collagenous interventricular component part of the atrioventricular groove with the coronary sinus within in of the membranous septum, an oval or round area below and conflu- its posterior aspect (see Fig. 57.4B,D). The anterior and posterior ent with the fibrous triangle separating the right and the non-coronary (inferior) interventricular grooves indicate the lines of mural attach- leaflets of the aortic valve. Between the inferior limits of the free ment of the ventricular septum and the limits of the ventricular territo- margins of the leaflets of the mitral valve and the ventricular apex, the ries. The sternocostal surface of the ventricle curves bluntly into its left muscular walls exhibit deeper, finer and more intricate trabeculae surface at the obtuse margin. carneae than those of the right ventricle, characteristically more devel- The shape of the left ventricle changes from elliptical in the neonatal oped nearer the apex, and becoming smoother as the superior septal period to the round adult shape later in infancy (Azancot et al 1983). surface is reached.
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Heart 1007 75 RETPAHC A Commissural ring (sinutubular junction) LAA Aortic wall within ventricle (interleaflet triangle) LUPV e V rine gn t ari ncu dl o jua nr cte tir oia nl O LLPV estibul MV V Ventricle within sinus Basal ring A B LAA Sinutubular Haemodynamic ventriculoarterial junction junction (semilunar) Commissure LUPV os LLPV Artery as part Arterial of ventricle ule wall estib MV V Ventricle Ventricle as part of aorta B GCV Anatomical ventriculoarterial junction (circular) Fig. 57.25 Sagittal sections showing the left side of the left atrium in a cadaveric heart. A, The oesophagus (O) passing behind the posterior left atrial wall and a broad left-lateral ridge (double-headed arrow). The left upper (LUPV) and left lower (LLPV) pulmonary veins enter the left atrium C Pulmonary trunk Sinutubular junction Non-adjacent leaflet via a short common stem. Other abbreviations: LAA, left atrial appendage; Right coronary Left coronary Ventriculoarterial MV, mitral valve. B, The section passes through the os of the left atrial leaflet leaflet junction appendage and the infolding of the ridge. The triangle indicates the carina or interpulmonary ridge between the upper and lower pulmonary veins. The great cardiac vein (GCV) runs underneath the left atrial wall. (With permission from Ho SY, McCarthy KP, Faletra FF. 2011. Anatomy of the left atrium for interventional echocardiography. Eur J Echocardiogr 12:11–15.) Hypertrophy of heart muscle Available with the Gray’s Anatomy e-book Mitral valve The general comments already made for the tricuspid valve also apply to the mitral valve. Thus it has an orifice with a supporting anulus, leaflets and a variety of chordae tendineae and papillary muscles. Muscular septum Mitral valve Left fibrous trigone Mitral valvular orifice Right fibrous trigone Central fibrous body Membranous septum The mitral orifice is a well-defined transitional zone between the atrial wall and the leaflet bases, being smaller than the tricuspid orifice (mean Fig. 57.24 A, The structure of the aortic root is best conceptualized in circumference is 9.0 cm in males and 7.2 cm in females). The approxi- terms of a three-pronged coronet; there are at least three rings within this mately circular orifice is almost vertical and at 45° to the sagittal plane coronet but none supports the entirety of the attachments of the valvular in diastole, but with a slight anterior tilt. Its ventricular aspect faces leaflets (compare with C). B, The leaflets have been resected at their anterolaterally to the left and a little inferiorly towards the left ventricu- attachment to the aortic wall. Note the relationship of the leaflet insertions lar apex. It is almost co-planar with the tricuspid orifice but postero- and the ventriculoarterial junction. C, The root of the aorta has been cut open and distended, in order to show the insertion of the semilunar superior to it, whereas it is posteroinferior and slightly to the left of the leaflets. Note the zone of fibrous continuity between the leaflets of the aortic orifice. The mitral, tricuspid and aortic orifices are intimately aortic and mitral valves and their relationship to the fibrous trigones, and connected at their central fibrous body. When the mitral valve leaflets the semilunar attachment of the leaflets (compare with B). (Redrawn with close, they form a single zone of coaptation, termed the commissure. permission, courtesy of Professor RH Anderson, Institute of Child Health, The anulus of the valve is not a simple fibrous ring but is made up of University College, London.) fibrocollagenous elements of varying consistency, from which the fibrous leaflet cores take origin; the variable consistency is essential to allow the major changes in anular shape and dimensions during the cardiac cycle that are needed for optimal valvular efficiency. The area of
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Heart 1007.e1 75 RETPAHC Hypertrophic cardiomyopathy is characterized by myocardial wall thickening, particularly a disproportionate thickening of the interven- tricular septum in comparison with the posterior wall. Echocardiogra- phy accurately assesses the degree of thickening and its effect on systolic function, such as dynamic left ventricular outflow obstruction, systolic anterior motion of the aortic mitral valve leaflet and mid-systolic closure of the aortic valve. There may also be a degree of diastolic dys- function. Serial short-axis gradient echo MRI allows accurate measure- ment of wall thickness and is particularly useful in assessing apically confined hypertrophy. A number of histological changes are observed, including cardiomyocytic disarray with replacement fibrosis and col- lagenous component expansion. Treatment is usually medical, except for refractory cases and those in whom the left ventricular outflow tract obstruction has a gradient of greater than 50 mmHg. Ventricular septal myotomy and myectomy are performed in such cases. Catheter alcohol septal ablation has been introduced as a non-surgical alternative. A number of patients may also require implantation of cardiac defibrilla- tors to prevent sudden cardiac death. An athlete’s heart may physiologically hypertrophy but in a uniform fashion; the left ventricle cavity is usually less than 55 mm in size, and thickness decreases on deconditioning. In contrast, hyper- trophic cardiomyopathy reveals asymmetric patterns of left ventricular hypertrophy, often with sharp segmental transitions, left atrial enlarge- ment and bizarre electrocardiographic patterns. Furthermore, there is an autosomal dominant inheritance pattern of abnormalities in genes coding for myocardial proteins associated with hypertrophic cardio- myopathy. Individuals with mutations of the β-MHC (major histo- compatibility complex) gene usually develop the classic form of hypertrophy, whereas those with cardiac troponin T gene mutations generally have only mild or clinically undetectable hypertrophy. Rare forms of hypertrophy include localized left ventricular apical hypertro- phy as a result of cardiac troponin I mutations, and isolated mid- cavity hypertrophy caused by cardiac actin and MLC (myosin light chain) gene mutations.
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HEART 1008 7 NOITCES Aorta Pulmonary trunk Superior vena cava Anterior interventricular artery Right atrium Left atrial appendage Fossa ovalis Right upper Venous mponent pulmonary vein ule Body co Right lower b Circumflex coronary artery esti pulmonary vein V Mitral valve Left atrium Fig. 57.26 The posterior wall of the left atrium close to the posterior interatrial groove in a cadaveric heart. The smooth-walled venous component of the left atrium is the most extensive component. The septal aspect of the left atrium shows the crescentic line of the free edge of the flap valve against the rim of the fossa ovalis. The orifices of the right superior and inferior pulmonary veins are adjacent to the plane of the septal aspect of the left atrium. (Specimen courtesy of M Loukas MD, PhD.) Anterior interventricular vein Serous pericardium, visceral layer (epicardium) Myocardium Left coronary artery, Endocardium anterior interventricular branch Right ventricle Anterior interventricular sulcus Septomarginal trabecula (moderator band) Superoposterior Right coronary artery, papillary muscle right marginal branch Left coronary artery, Myocardium left marginal branch Superolateral papillary muscle Trabeculae Left ventricle carneae Interventricular septum, muscular part Inferoseptal papillary muscles Tricuspid valve, septal leaflet Chordae tendineae Inferior interventricular sulcus Middle cardiac vein Right coronary artery, inferior interventricular branch Fig. 57.27 Left and right ventricles: cross-section perpendicular to the axis of the heart, superior aspect. (With permission from Waschke J, Paulsen F (eds), Sobotta Atlas of Human Anatomy, 15th ed, Elsevier, Urban & Fischer. Copyright 2013.) the anulus increases linearly with body surface area in children and commissure. These anteromedial (inferoseptal) and posterolateral young adults (Poutanen et al 2006). The anulus is strongest at the (superoposterior) extremities may be regarded as two independent internal aspects of the left and right fibrous trigones. Extending from commissures, each positionally named as indicated in brackets. these structures, the anterior and posterior coronary prongs (tapering, Although simple, the official names for these leaflets – anterior and fibrous, subendocardial tendons) partly encircle the orifice at the atrio- posterior, respectively – are somewhat misleading because of the obliq- ventricular junction (see Fig. 57.23). Between the prong tips, the atrial uity of the valve. and ventricular myocardial masses are separated by a more tenuous When the valve is laid open, the anterior leaflet (aortic, septal, sheet of deformable fibroelastic connective tissue. Spanning anteriorly ‘greater’ or anteromedial) is seen to guard one-third of the circumfer- between the trigones, the fibrous core of the central part of the aortic ence of the orifice and to be semicircular or triangular, with few or no leaflet of the mitral valve is a continuation of the fibrous subaortic marginal indentations. Its fibrous core (lamina fibrosa) is continuous curtain that descends from the adjacent halves of the left and adjacent on the outflow aspect, beyond the margins of the fibrous subaortic (non-coronary) valve leaflets (see Fig. 57.29). curtain, with the right and left fibrous trigones (see Figs 57.17, 57.21, 57.24C). Between the trigones, it is continuous with the fibrous curtain Mitral valve leaflets itself and, beyond the trigones, with the roots of the anular fibrous The mitral valvular leaflets have long been described as paired struc- prongs (see Fig. 57.23). The leaflet has a deep crescentic rough zone tures. (The name ‘bicuspid valve’ is explicit but erroneous because the that receives various chordae tendineae. The ridge limiting the outer leaflets are not cuspid, or ‘peaked’, in form). Small accessory leaflets are margin of the rough zone indicates the maximal extent of surface almost always found between the two major leaflets and so the mitral contact with the mural leaflet in full closure. A clear zone is seen valve should be described as a continuous veil that is attached around between the rough zone and the valvular anulus; it is devoid of attach- the entire circumference of the mitral orifice. Its free edge bears several ments of chordae, although its fibrous core carries extensions from indentations, of which two are sufficiently deep and regular to be chordae attached in the rough zone. The anterior leaflet has no basal nominated as the ends of a solitary and oblique zone of apposition or zone and continues into the valvular curtain. Hinging on its anular
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Heart 1009 75 RETPAHC Superior vena cava Right upper pulmonary vein Aorta comV pe on no eu ns t pulmR oig nh at r ylo vw ee inr Fossa Pulmonary trunk ovalis Body Left atrium Septal perforator A arn tete ryrior interventricular Vestibule Circumflex coronary artery Superolateral Mitral valve papillary muscle Inferoseptal papillary muscle Fig. 57.28 A dissection of the left ventricle in a cadaveric heart, exposing the papillary muscles of the ventricle. Notice the thick wall of the left ventricle and the chordae tendineae of the mitral valve attaching to the papillary muscles. (Specimen courtesy of M Loukas MD, PhD.) Left coronary leaflet Left coronary artery Aortic bulb Left coronary artery, anterior interventricular branch Non-adjacent leaflet Interventricular septum, membranous part Aortic sinus Myocardium Pulmonary trunk Chordae tendineae Posterolateral papillary muscle Left coronary leaflet Right coronary artery Nodule of left coronary leaflet Left atrioventricular orifice Right coronary leaflet Mitral valve, aortic leaflet Non-adjacent leaflet Inferoseptal papillary muscle Fig. 57.29 The aortic orifice opened from the front to show the leaflets of the aortic valves, their nodules, lunules, commissures and the triple-scalloped line of their anular attachment. Also shown are the continuity of the subaortic curtain with the mitral aortic leaflet (i.e. ‘aortic baffle’) and the coronary ostia, and the spatial relationship of the aortic orifice to the pulmonary orifice and to the left ventricle. (With permission from Waschke J, Paulsen F (eds), Sobotta Atlas of Human Anatomy, 15th ed, Elsevier, Urban & Fischer. Copyright 2013.)
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HEART 1010 7 NOITCES attachment, and continuous with the subaortic curtain, it is critically the atrial cavity, and the atrial aspects of the rough zones come into placed between the inlet and the outlet of the ventricle. During passive maximal contact. Precise papillary contraction, and increasing tension ventricular filling and atrial systole, its smooth atrial surface is impor- in the chordae, continue to prevent valvular eversion and maintain tant in directing a smooth flow of blood towards the body and apex of valvular competence. The orifices and the leaflets of both atrioventricu- the ventricle. After the onset of ventricular systole and closure of the lar valves undergo considerable changes in position, form and area mitral valve, the ventricular aspect of its clear zone merges into the during a cardiac cycle. Both valves move anteriorly and to the left during smooth surface of the subaortic curtain, which, with the remaining systole, and reverse their motion in diastole. The mitral valve reduces fibrous walls of the subvalvular aortic vestibule, forms the smooth its orificial (anular) area by as much as 40% in systole; its shape changes boundaries of the ventricular outlet. from circular to crescentic at the height of systole, the anular attachment The posterior leaflet (mural, ventricular, ‘smaller’ or posterolateral) of its aortic leaflet being the concavity of the crescent. The attachment usually has two or more minor indentations. Lack of definition of the of its mural leaflet, although remaining convex, contracts towards the major intervalvular commissures has led to disagreement and confu- anterior cardiac wall. The smooth left ventricular outflow tract (aortic sion concerning the territorial extent of this leaflet and the possible vestibule) terminates at the aortic valve leaflets. Although stronger in existence of accessory scallops. Examination of the valve in the closed construction, the aortic valve resembles the pulmonary valve (see Figs position reveals that the posterior leaflet may conveniently be regarded 57.21, 57.24, 57.29) in possessing three semilunar leaflets, supported as comprising all the valvular tissue posterior to the anterolateral within the three aortic sinuses of Valsalva. Although the aortic valve, (inferoseptal) and posteromedial (superoposterior) ends of the major like the pulmonary valve, is often described as possessing an anulus in zone of apposition with the aortic leaflet. Thus defined, it has a wider continuity with the fibrous skeleton, there is no complete collagenous attachment to the anulus than does the anterior leaflet, guarding two- ring that supports the attachments of the leaflets. As with the pulmo- thirds of the circumferential attachments. Further indentations usually nary valve, the anatomy of the aortic valve is dominated by the fibrous divide the mural leaflet into a relatively large middle scallop and semilunar leaflet attachment (see Fig. 57.24C). smaller lateral and septal commissural scallops. Each scallop has a crescentic opaque rough zone, receiving on its ventricular aspect the Mitral chordae tendineae attachments of the chordae that define the area of valvular apposition Mitral chordae tendineae resemble those supporting the tricuspid valve. in full closure. From the rough zone to within 2–3 mm of its anular False chordae are also irregularly distributed as in the right ventricle. attachment, there is a membranous clear zone devoid of chordae. They are single or multiple, thin, fibrous or fibromuscular structures The basal 2–3 mm is thick and vascular, and receives basal chordae. that traverse the cavity of the left ventricle and have no connection with The ratio of rough to clear zone in the anterior leaflet is 0.6 and in the the valvular leaflets (Fig. 57.30). They occur commonly in human left middle scallop of the posterior leaflet is 1.4. Much more of the mural ventricles and often cross the subaortic outflow. Histologically, false leaflet is in apposition with the aortic leaflet during closure of the chordae sometimes contain extensions from the ventricular conducting mitral valve. tissues; these left ventricular bands are often identified on echocardiog- raphy. It has been suggested that false chordae produce premature Opening of the mitral valve ventricular contractions and be the possible cause of functional heart At the onset of diastole, opening is passive but rapid, the leaflets parting murmurs or innocent murmurs in children and young adults. and projecting into the ventricle as left atrial pressure exceeds left ven- True mitral valve chordae may be divided into four types: inter- tricular diastolic pressure. Passive ventricular filling proceeds as atrial leaflet (commissural), rough zone (including the special strut chordae), blood pours to the apex, directed by the pendant aortic valvular leaflet. ‘cleft’ and basal chordae. Most true chordae divide into branches from The leaflets begin to float passively together, hinging on their anular a single stem soon after their origin from the apical third of a papillary attachments and partially occluding the ventricular inlet. Atrial systole muscle, or proceed as single chordae that divide into several branches now occurs, jetting blood apically and causing re-opening of the leaf- near their attachment. Basal chordae, in contrast, are solitary structures lets. As maximal filling is achieved, the leaflets again float rapidly passing from the ventricular wall to the mural leaflet. There is such together. Closure is followed by ventricular systole, which starts in the marked variation between the arrangement of the chordae that any papillary muscles and continues rapidly as a general contraction of the detailed classification loses much of its clinical significance. Suffice it walls and septum. Coordinated contraction of the papillary muscles to say that, in the majority of hearts, the chordae support the entire free increases the tension in the chordae and promotes joining of the cor- edges of the valvular leaflets, together with varying degrees of their responding points on opposing leaflets, preventing their eversion. With ventricular aspects and bases, and there is some evidence to suggest that general mural and septal excitation and contraction, left ventricular those valves with unsupported free edges become prone to prolapse in pressure increases rapidly (see Fig. 57.20). The leaflets ‘balloon’ towards later life. Fig. 57.30 The aorta has been transected at the level of the Aorta Right coronary orifice sinutubular junction in this cadaveric heart in order to Left atrium reveal the closed leaflets of the aortic valve. Note how the supporting sinuses may be Interleaflet triangle described as left coronary, right Pulmonary trunk coronary and non-adjacent, according to the origin of the Membranous septum coronary arteries. However, this Aortic-mitral Circumflex continuity terminology could be coronary artery ambiguous if the coronary arteries arise in variable locations, whereas the Anterior interventricular terminology of right, left and artery Superolateral non-facing aortic sinus, Left bundle papillary muscle respectively, is not ambiguous. branch Note the inter-leaflet triangles, membranous septum, and fibrous continuity between the aorta and mitral valve. Inferoseptal papillary muscle (Specimen courtesy of M Loukas MD, PhD.) Left ventricle Fine trabeculations
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Heart 1011 75 RETPAHC Papillary muscles except at its midpoint, where there is an aggregation of fibrous tissue, The two muscles supporting the leaflets of the mitral valve vary in length the valvular nodule of the semilunar leaflet. The fibrous core that flanks and breadth, and may be bifid. The anterolateral (superolateral) muscle each nodule is tenuous, forming the lunules of translucent and occa- arises from the sternocostal mural myocardium, and the posteromedial sionally fenestrated valvular tissue; fenestrations are of no functional (inferoseptal) from the diaphragmatic region (see Fig. 57.27). Chordae significance. The aortic surface of each leaflet is rougher than its ven- tendineae arise mostly from the tip and apical third of each muscle but tricular aspect. sometimes take origin near their base. The chordae from each papillary Confusingly, three sets of names are used to describe the aortic muscle diverge and are attached to corresponding areas of closure on leaflets. Posterior, right and left refer to their fetal positions before both valvular leaflets. full cardiac rotation has occurred (Ch. 52). Corresponding terms based on their approximate positions in maturity are anterior, left and right posterior. Widespread clinical terminology, which links both leaflets Aortic root and sinuses to the origins of the coronary arteries, has replaced anterior, left and right leaflets with right and left coronary and non-adjacent The aortic root, the anatomical bridge between the left ventricle and the (and, usually, non-coronary) leaflets, respectively; these clinical terms ascending aorta, consists of the aortic valvular leaflets (supported by are preferable in the normal heart because they are simple and the aortic sinuses of Valsalva) and the inter-leaflet triangles interposed unambiguous. between their basal attachments (see Fig. 57.24). As such, it possesses significant length, but because of the semilunar attachment of the leaf- Aortic sinuses (of Valsalva) lets, it has no discrete proximal border. It is limited distally by the The aortic sinuses are more prominent than those in the pulmonary sinutubular junction (see Fig. 57.30). The essential feature is the semi- trunk. The upper limit of each sinus reaches considerably beyond the lunar attachments of the valve leaflets; their hinge lines cross the ana- level of the free border of the leaflet and forms a well-defined circum- tomical ventriculoarterial junction, marking a transition from the ferential sinutubular ridge on the aortic inner surface, just above the myocardium of the left ventricle to the fibroelastic tissue of the valve aortic valvular leaflets (see Fig. 57.24C). Coronary arteries usually open sinuses (Fig. 57.31). The muscular portion of the aortic root is roughly near this ridge within the upper part of the sinus but are markedly vari- two-thirds of its widest circumference. Descriptions of the aortic root able in their origin. The walls of the sinuses are largely collagenous near over the years have been bedevilled by accounts of a valve anulus. the attachment of the leaflets but the amount of lamellated elastic tissue Although echocardiographers used to describe this proximal border in increases with distance from the zone of attachment. At the midlevel terms of an ‘anulus’, examination of cross-sections of the left ventricular of each sinus, its wall is about half the thickness of the supravalvular outflow tract has never found any circular anatomical boundary or a aortic wall and less than one-quarter of the thickness of the sinutubular distinct boundary of any kind (Loukas et al 2014a). There are at least ridge. At this level, the mean luminal diameter at the commencement two rings within the root; neither serves to support the valve leaflets, of the aortic root is much larger than that of the ascending aorta; these which are attached in semilunar fashion from the sinutubular junction details are functionally significant in the mechanism of valvular motion. to a basal ventricular attachment. Two leaflets are supported by muscle, A linear relationship between the diameter of the aortic sinus and the and the third has an exclusively fibrous attachment. The root acts as a square root of body surface area has been described in children (Kaiser bridging structure not only anatomically, separating the myocardial and et al 2008). arterial components of the left ventricular pathway, but also function- ally because its proximal and distal components can withstand consid- Opening of the aortic valve erable changes in ventricular and arterial pressures. During diastole, the closed aortic valve supports an aortic column of blood at high but slowly diminishing pressure (see Fig. 57.20). Each Aortic valve leaflets sinus and its leaflet form a hemispherical chamber. The three nodules The aortic valve leaflets are attached in part to the aortic wall and in are apposed and the margins and lunular parts of adjacent leaflets are part to the supporting ventricular structures. The situation is more tightly apposed on their ventricular aspects. From the aortic aspect, the complicated than in the pulmonary valve because parts of the leaflets closed valve is triradiate, three pairs of closely compressed lunules also take origin from the fibrous subaortic curtain, and are continuous radiating from their nodules to their peripheral commissural attach- with the aortic leaflet of the mitral valve (see Fig. 57.29). This area of ments at the sinutubular junction (see Fig. 57.21). As ventricular systolic continuity is thickened at its two ends to form the right and left fibrous pressure increases, it exceeds aortic pressure and the valve is passively trigones (see Fig. 57.21). As with the pulmonary valve, the semilunar opened. attachments incorporate segments of ventricular tissue within the bases The fibrous wall of the sinuses nearest the aortic vestibule is almost of two of the aortic sinuses. The sinuses and leaflets are conveniently inextensible but, more superiorly, the wall is fibroelastic. Under left named as right, left and non-coronary, according to the origins of the ventricular ejection pressure, the radius here increases 16% in systole, coronary arteries (see Fig. 57.24C). However, the so-called non-coronary as the commissures move apart to form a fully open triangular orifice. leaflet is better termed the non-adjacent leaflet because it rarely gives The free margins of the leaflets then become almost straight lines rise to a coronary artery. between peripheral attachments. However, they do not flatten against The semilunar attachments incorporate three triangular areas (trigo- the sinus walls, even at maximal systolic pressure, which is probably an nes) of aortic wall within the apex of the left ventricular outflow tract. important factor in their subsequent closure. During ejection, most They are interposed between the bulbous aortic sinuses and separate blood enters the ascending aorta but some enters the sinuses, forming the cavity of the left ventricle from the pericardial space. Removal of the vortices that help to maintain the triangular ‘mid position’ of the leaflet trigones in an otherwise intact heart is instructive in demonstrating the during ventricular systole and also probably initiate their approxima- relationships of the aortic valve, which, justifiably, may be considered tion at the end of systole. Tight and full closure ensues with the rapid as the keystone of the heart. The first triangle, between the non-coronary decrease in ventricular pressure in diastole. Commissures narrow, and left coronary leaflets, has a base continuous inferiorly with the nodules aggregate and the valve reassumes its triradiate form. Experi- fibrous aortic–mitral curtain. The second triangle, between right and ments indicate that 4% of ejected blood regurgitates through a valve non-coronary leaflets, has the membranous components of the inter- with normal sinuses, whereas 23% regurgitates through a valve without ventricular septum as its base and thus ‘faces’ the right ventricle, whereas them. The normal structure of the aortic sinuses also promotes non- its apex ‘points’ towards the transverse pericardial space behind the turbulent flow into the coronary arteries. origin of the right coronary artery. The third triangle, between the two coronary leaflets, has its base on the muscular interventricular septum Echocardiography and its apex ‘points’ to the plane of space found between the aortic wall and the free-standing sleeve of right ventricular infundibular muscula- ture that supports the leaflets of the pulmonary valve. Although the Echocardiography allows a detailed assessment of the functional basal attachments of each aortic valvular leaflet are thickened and col- anatomy of the heart. The gross anatomy of the heart can be evaluated lagenous at their ventricular origins, the leaflets lack a continuous col- by two-dimensional echocardiography in the parasternal, apical, lagenous circular skeletal support; valvular function depends primarily suprasternal and subcostal positions (Fig. 57.32). The standardized upon the semilunar attachments of the leaflets. planes used are long-axis, short-axis and four-chamber. The long-axis The leaflets are endocardial folds with a central fibrous core. With view is obtained by placing the ultrasound transducer in the left apico- the valve half-open, each equals slightly more than a quarter of a sphere, sternal position and provides detailed images of the left ventricle, aorta, an approximate hemisphere being completed by the corresponding left atrium, and mitral and aortic valves (Fig. 57.32C). Angling the sinus. Each leaflet has a thick basal border, deeply concave on its aortic beam towards the right also allows assessment of the right atrium, right aspect, and a horizontal free margin that is only slightly thickened, ventricle and tricuspid valves. Rotating the transducer by 90° in the
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Heart 1011.e1 75 RETPAHC Sinus wall Ventriculo- arterial junction Leaflet Transitional zone Hinge Ventricular myocardium Fig. 57.31 A histological section through one of the coronary aortic sinuses to demonstrate the way in which ventricular muscle supports the transition from the fibroelastic wall of the sinus to the tissues of the leaflet. The transitional area is anchored to the ventricular muscle. The hinge of the leaflet is well below the level of the ventriculoarterial junction. Importantly, there is no ring-like structure in the form of an ‘anulus’ supporting the hinge of the leaflet within the ventricle. The muscular tissue of the ventricle is stained pink; fibrous tissue, which would show up as a characteristic light colour with this stain, is absent. Haematoxylin and eosin stain. (Courtesy of Diane E Spicer.)
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HEART 1012 7 NOITCES RV RV PV R LV TV AV RV NA LV L RA MV LA LA RA LA A B C RV RV RV AV RA LV PV RA AV LV LA LA MV LA D E F Fig. 57.32 Cardiac anatomy shown by transthoracic echocardiography and CT. A, Four-chamber view. B, Short-axis view at aortic valve level. Note three aortic leaflets – right, left and non-adjacent – and the central position of the aorta. C, Parasternal long-axis view. D–F, Corresponding images by CT. Note the different orientation compared with transthoracic echocardiography (looked at from below, foot to head). Abbreviations: A, anterior; AV, aortic valve; F, foot; H, head; L, left; LA, left atrium; LV, left ventricle; MV; mitral valve; NC, non-adjacent; P, posterior; PV, pulmonary valve; R, right; RA, right atrium; RV, right ventricle; TV, tricuspid valve. (Images courtesy of Dr Konstantinos Dimopoulos, Royal Brompton and Chelsea and Westminster Hospitals, London.) clockwise direction produces the short-axis view, which allows assess- connective tissue matrix itself is interconnected laterally to form ment of the left ventricle, papillary muscles, chordae tendineae and bundles, strands or sheets of macroscopic proportions showing a mitral valves (Fig. 57.32B). The four-chamber view demonstrates the complex geometric pattern. Surrounding and attaching to larger myo- ventricles, atria, and mitral and tricuspid valves (Fig. 57.32A). Rotation cardial bundles are stronger perimysial condensations. The overall of the transducer allows two-chamber views of the heart and more pattern is described in terms of struts and weaves. Despite its impor- detailed assessment of the aorta and aortic valves. Cardiac MRI and CT tance, the myocardial matrix cannot be grossly dissected. provide similar information on cardiac structure and function (see Figs Running at the ventricular base is a complex framework of dense 57.2, 57.35A,B), together with complementary information on great collagen with membranous, tendinous and fibroareolar extensions, vessels (Fig. 57.32D–F) and other extracardiac intrathoracic structures. intimately related to atrioventricular valves and the aortic orifice. The whole is sufficiently distinct to be termed the fibrous skeleton of the heart, but although it is often stated that all four valves are contained CONNECTIVE TISSUE AND FIBROUS SKELETON OF within this skeleton, this is not the case. The leaflets of the pulmonary THE HEART valve are supported on a free-standing sleeve of right ventricular infundibulum that can easily be removed from the heart without dis- From epicardium to endocardium and from the orifices of the great turbing either the fibrous skeleton or the left ventricle. Another point veins to the roots of the arterial trunks, the intercellular spaces between of confusion is the idea that the ‘skeleton’ provides the support for the contractile and conduction elements are permeated by connective cardiac valves. In reality, it is the overall structure of the atrioventricular tissue; the amount, arrangement and texture vary greatly with location. junctions that supports the mitral and tricuspid valves, whereas the Over much of the heart, a fine layer of areolar tissue is found beneath arterial valves are hinged within the valvular sinuses. The fibrous skel- the mesothelium of the serous (visceral) epicardium that accumulates eton is strongest at the junction of the aortic, mitral and tricuspid valves, subepicardial fat, concentrated along the acute margin, the atrioven- the so-called central fibrous body (see below) (see Figs 57.21, 57.23). tricular and interventricular grooves, and their side channels. The coro- Two pairs of curved, tapering, collagenous prongs, fila coronaria, extend nary vessels and their main branches are embedded in this fat; the from the central fibrous body. They are stronger on the left, where they amount increases with age. The endocardium also lies on a fine areolar pass partially around the mitral and tricuspid orifices. These orifices are tissue rich in elastic fibres. Fibrocellular components of these subepi- almost co-planar and incline to face the cardiac apex. In contrast, the cardial and subendocardial layers blend on their mural aspects with the aortic valve faces superiorly, lying anterosuperior and to the right of the endomysial and perimysial connective tissue on the myocardium. Each mitral orifice. Two of the leaflets of the aortic valve are in fibrous con- cardiac myocyte is invested by a delicate endomysium composed of fine tinuity with the aortic leaflet of the mitral valve; this subaortic curtain reticular, collagen and elastin fibres embedded in ground substance. is also an integral part of the fibrous skeleton (see Figs 57.21, 57.24C). This matrix is lacking only at desmosomal and gap junctional contacts The two ends of the curtain are strengthened as the right and left fibrous of intercalated discs. Similar arrangements apply to ventricular conduc- trigones, which are the strongest parts of the skeleton. The right trigone, tion myocytes and their extensive working myocardial contacts. The together with the membranous septum, constitutes the central fibrous
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Heart 1013 75 RETPAHC body, which is penetrated by the atrioventricular bundle of His (see below). The membranous septum is crossed on its right aspect by the attachment of the tricuspid valve, dividing the septum into atrioven- tricular and interventricular components. The aortic root is central within the fibrous skeleton and is often described in terms of an ‘anulus’ integrated within the fibrous skeleton (Anderson et al 2013b). However, as with the pulmonary valve, the structure of the aortic root corresponds to the triple fibrous semilunar attachments of its leaflets. Within this complex circumferential zone are three crucially important triangular areas that separate, on the ven- tricular aspect, the aortic bulbous sinuses that house the valvular leaf- lets. As a whole, three triangles, known as the subaortic spans, can be conceptualized in terms of a three-pointed coronet; their triangular apices correspond to the tips of the valvular commissures and their walls, significantly thinner than those of the sinuses, consist variously of collagen or admixed muscle strands and fibroelastic tissue. They form the subvalvular extensions of the aortic vestibule. The first span is the interval between the non-coronary and left coronary sinuses that is filled with the deformable subaortic curtain. The second span between the non-coronary and right coronary sinuses is continuous with the anterior surface of the membranous septum. The third span, between the two coronary aortic sinuses, is filled with loose fibroelastic tissue and separates the extension of the subaortic root from the wall of the free-standing subpulmonary infundibulum. Previously, this was Fig. 57.33 A reconstruction of a porcine heart made following diffusion thought to be the location of the tendon of the infundibulum (conal tensor MRI of an autopsied heart. The tracks are created from the first (conus) ligament) (Loukas et al 2007); research using mouse hearts eigenvectors and represent the alignment of the aggregated myocytes. has shown that the ligament is found at the level of the sinutubular This technique enables the identification of reproducible tracks, or junctions at the site of initial fusion of the distal outflow cushions. The pathways, through the myocardium that connect remote end and line of proximal fusion is the longitudinal raphe sometimes seen in epicardial regions by means of simultaneous changes in helical and the muscular subpulmonary infundibulum. intrusion angles. (With permission from Anderson R, Smerup M, Sanchez- Similar fibrous triangles are found separating the sinuses of the Quintana D, Loukas M, Lunkenheimer P. 2009. The three-dimensional pulmonary trunk but these are significantly less robust. Use of the terms arrangement of the myocytes in the ventricular walls. Clin Anat 22:64–76.) mitral and tricuspid ‘anuli’ implies that the atrioventricular valves are supported by discrete circular fibrous rings, when, in reality, they are D-shaped structures integrally attached to the fibrous cardiac skeleton. estimated at 8 per 1000 live births but they are found in up to 2% of It is therefore inaccurate to consider these valvular orifices as circular. stillbirths. Only a small proportion of the anomalies are directly attrib- Rather, the straight edge of the ‘D’-shaped mitral valve represents a utable to genetic or environmental factors and the majority are the fibrous continuity between the anterior leaflet and the aortic root, and result of multifactorial events. the remainder supports the mural leaflet. The straight edge of the tri- cuspid valve represents the attachment of the septal leaflet, marking Abnormalities of cardiac position the inferior border of the triangle of Koch, and the remainder supports the anterosuperior and inferior leaflets. The valvular attachments of the Available with the Gray’s Anatomy e-book atrioventricular valves are not simple, rigid collagenous structures but dynamic, deformable lines that vary greatly at different peripheral points and change considerably with each phase of the cardiac cycle Acyanotic cardiac defects and with increasing age. The tricuspid attachments are even less robust than those of the mitral valve. At several sites, only fibroareolar tissue Available with the Gray’s Anatomy e-book separates the atrial and ventricular muscular masses. The fibrous skeleton ensures electrophysiological discontinuity Cyanotic cardiac defects between the atrial and ventricular myocardial masses (except at the site of penetration of the conduction tissue). It also provides direct attach- ment for the myocardium and for fibrous tissue throughout the Available with the Gray’s Anatomy e-book heart as a support matrix for a three-dimensional meshwork of cardiomyocytes. CONDUCTION TISSUES Arrangement of cardiomyocytes The microstructure of cardiac muscle is described in detail in Chapter 6. Ventricular myocytes form a The cells of cardiac muscle differ from those of skeletal muscle in having three-dimensional mesh in a supporting fibrous matrix. One popula- the inherent ability to contract and relax spontaneously. This myogenic tion is aligned so that the long axis of the aggregated cells is tangential rhythm is shown by small pieces of cardiac tissue, and even isolated to the epicardial and endocardial borders, albeit with marked variation myocytes. Ventricular cells contract and relax at a lower frequency than in the angulation relative to the ventricular equator. Correlation with atrial cells, but in the intact heart, both are synchronized to a more measurements taken using force probes shows that these myocytes rapid rhythm, generated by pacemaker tissue in the sinus and atrioven- produce the major unloading of the blood during ventricular systole. A tricular nodes and conveyed by a system of specialist conduction fibres second population is aligned at angles of up to 40° from the epicar- in the atrioventricular conduction axis and the ventricular conducting dium towards the endocardium and produces auxotonic forces during pathways (Purkinje cells). For an account of excitation–contraction the cardiac cycle. The three-dimensional arrangement of the mesh as coupling in cardiac muscle, see page 138. demonstrated in MRI of the porcine heart also mediates the realign- The anatomical arrangement of these tissues is described in the ment of cardiomyocytes that must take place during ventricular con- context of the heart. Here, consideration is restricted to the cells that traction and accounts for the extent of systolic mural thickening make up the impulse-generating and conduction system. All are modi- (Fig. 57.33). fied cardiac cells. Three types within a continuum of morphology may The finding that the number of cardiomyocytes in the left ventricle be distinguished from normal working cells, namely: nodal cells, tran- increases between the first and the twentieth year of life suggests that sitional cells and Purkinje cardiomyocytes. children may be able to regenerate myocardium (Mollova et al 2013). Overview of the conduction system CONGENITAL CARDIAC MALFORMATIONS Of all the cells in the heart, those of the sinu-atrial node generate the Congenital malformations of the heart are common and amount to most rapid rhythm, and therefore function as the cardiac pacemaker. about one-quarter of all developmental anomalies. Their incidence is The impulse, believed to be generated in the nodal cells, is transmitted
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Heart 1013.e1 75 RETPAHC The most severe abnormality of position is an extrathoracic heart Most congenital heart abnormalities can be detected during antena- (ectopia cordis), where the heart usually projects to the surface through tal ultrasound screening (Fig. 57.34). Neonates with severe congenital the lower thoracic and upper abdominal wall, remaining covered, in heart disease may present with tachypnoea, difficulty in feeding, cyano- most instances, by the fibrous pericardium, and usually accompanied sis and/or cardiovascular collapse, and there may be audible murmurs by herniation of the abdominal contents. A mirror image, i.e. reversal on auscultation. The vast majority of abnormalities may be detected by in cardiac shape and position, occurs predominantly in the right postnatal echocardiography; in a very few cases, cardiac catheterization hemithorax (dextroposition). The apex of the heart may be directed to and direct measurements of pressure, oxygen saturations and angiogra- the right instead of the left (dextrocardia). This arrangement may phy may be required. be part of ‘situs inversus totalis’, where the heart, great vessels and abdominal organs all occupy mirror-imaged positions. The heart may Acyanotic cardiac defects are the result of either left-to-right cardiac also be right-sided in Kartagener’s syndrome (a subgroup of ciliary shunting through heart defects (intra- or extracardiac) or of obstruction. dyskinesias). Left-to-right shunting leads to an increased workload and stress on the More usually, an abnormal location of the heart occurs in cases of heart and the lungs as a consequence of increased pulmonary blood isomerism, in which both sides of the thorax, including the main flow and increased pulmonary venous return. Depending on the loca- bronchi and the atrial appendages, retain features of either morphologi- tion of the shunt and the magnitude of left-to-right shunting, patients cal right- or left-sidedness. Isomerism is also commonly associated with are at risk of developing pulmonary arterial hypertension unless the anomalous arrangement of the abdominal organs: right isomerism timely heart surgery is undertaken. Examples of defects leading to left- with absence of the spleen (asplenia) and left isomerism with multiple to-right shunting are simple septal defects such as atrial or ventricular spleens (polysplenia). Intracardiac anatomy in cases of isomerism is septal defects or patent ductus arteriosus, or more complex atrioven- almost universally abnormal, and there is a range of heart defects tricular septal defects, and/or a combination of any of these defects with (usually more simple in left and more complex in right isomerism). abnormal atrioventricular or ventriculoarterial connections (e.g. a These intrathoracic abnormal arrangements, with or without abdom- double-outlet right ventricle, where more than 50% of both the aorta inal abnormalities, often first manifest themselves incidentally follow- and the pulmonary artery originate from the right ventricle) (Ch. 52). ing chest radiography. Reversal of normal anatomy has obvious clinical Obstructive lesions may involve the atrioventricular or arterial valves implications, a typical example being a patient with mirror-image (mitral, aortic or pulmonary valve stenosis), or narrow vessels (e.g. arrangements and appendicitis, who presents with an acute left lower coarctation of the aorta or interrupted aortic arch). Depending on the quadrant pain. level and severity of the obstruction, patients may have a range of RV LV MV VSD RA LA LV RV LV RV TV RA A B C VSD RV LV RV RV Ao Ao PA RA LV D E F Fig. 57.34 A, Tricuspid atresia at 21 weeks’ gestation. A four-chamber view showing a large left ventricle and a hypoplastic right ventricle. The mitral valve is seen; no tricuspid valve is identified. There is an associated ventricular septal defect. B, An atrioventricular septal defect at 20 weeks’ gestation. A common atrioventricular valve (arrow) is associated with a defect in the atrioventricular septum. C, Hypoplastic left heart syndrome at 32 weeks’ gestation. This four-chamber view shows a large right atrium, right ventricle and tricuspid valve. There is a hypoplastic left ventricle; no mitral valve is identified. D, Hypoplastic left heart syndrome at 32 weeks’ gestation. This four-chamber view shows colour flow from right atrium to right ventricle across the tricuspid valve; no mitral valve is identified and there is no flow in the left side of the heart. E, Tetralogy of Fallot at 33 weeks’ gestation. The aorta arises astride a ventricular septal defect. F, Transposition of the great arteries at 21 weeks’ gestation. The aorta and pulmonary artery arise in parallel orientation. The aorta arises from the right ventricle and the pulmonary artery from the left ventricle. Abbreviations: Ao, aorta; LA, left atrium; LV, left ventricle; MV, mitral valve; PA, pulmonary artery; RA, right atrium; RV, right ventricle; TV, tricuspid valve; VSD, ventricular septal defect. (Courtesy of Gurleen Sharland, Evelina London Children’s Hospital.)
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HEART 1013.e2 7 NOITCES A B Fig. 57.35 A, Cardiac magnetic resonance angiography in a patient with a normal heart. Note the criss-cross relationship of the great arteries; the aorta arises from the left ventricle and runs to the right and posteriorly to the pulmonary trunk (at its origin) and towards the head. The pulmonary artery arises from the right and anterior right ventricle, crosses over and then runs to the left of the aorta and towards the back (where it bifurcates into the right and left pulmonary arteries at the underside of the aortic arch). B, A cardiac magnetic resonance angiogram from a patient with transposition of the great arteries. Note the parallel or side-by-side relationship of the great vessels and loss of their normal criss-cross relationship. The aorta runs anteriorly and comes off the right ventricle. The hypertrophied right ventricle supports the systemic circulation, and the ventricular septum bows from right to left. Abbreviations: Ao, aorta; LV, left ventricle; PT, pulmonary trunk; RV, right ventricle. (Courtesy of Dr Philip Kilner, Royal Brompton Hospital, London.) clinical presentations from an asymptomatic heart murmur (common) position of the great arteries (Fig. 57.35; p. 924) and tricuspid and to cardiovascular collapse (uncommon). Treatment in all cases is pulmonary atresia (often in the setting of hypoplastic right ventricle directed towards normalizing heart workload, systemic and pulmonary and functionally univentricular physiology). Neonates with severe cyan- blood flow, and cardiac output, and may be surgical and/or catheter- otic congenital heart defects may be dependent on the patency of the based. ductus arteriosus; early diagnosis, treatment with intravenous prosta- glandin infusion and timely transfer to a tertiary centre for more defini- Cyanotic cardiac defects may be attributable to a right-to-left intra- or tive therapy is key to survival and good long-term outcomes. extracardiac shunt or to a severe reduction in pulmonary blood flow. Major advances in the diagnosis and management of infants with They may be caused by simple lesions such as severe pulmonary steno- congenital cardiac malformations in recent years have resulted in an sis with an atrial septal defect and right-to-left shunting; moderate increased number of adolescents and adults with palliated or repaired, lesions, including Fallot’s tetralogy, in which there is a ventricular septal but not cured, congenital heart disease. This is an area that poses mul- defect, right ventricular outflow obstruction, right ventricular hypertro- tiple challenges to both cardiovascular and other medical disciplines. phy and an overriding aorta; or more complex lesions, including trans-
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HEART 1014 7 NOITCES over preferentially conducting pathways to right and left atria, and to parts of the right atrium (see Figs 57.13A, 57.37). In hearts over 65 years the atrioventricular node. At the atrioventricular node, the impulse is of age, a layer of connective or fatty tissue between the subendocardium delayed by 40 ms, allowing the atria to eject their contents fully before and the body of the node may sometimes render it visible to the naked commencement of ventricular contraction, and also placing an upper eye. Extending on the right from the crest of the right appendage, the limit on the frequency of signals that can be transmitted to the ventri- node typically courses posteroinferiorly into the upper part of the ter- cles. The transitional cells interpose between the atrial cardiomyocytes minal groove; in about 1 in 10 hearts it extends in horseshoe fashion and the nodal cells. There is no transition in humans between the across the crest of the appendage. Nodal tissue does not occupy the full node and the penetrating bundle, and the cells are virtually identical. thickness of the right atrial wall from epicardium to endocardium but Here, they become continuous with the more distinctively appearing sits as a wedge of specialized subepicardial tissue within the terminal Purkinje cells. Conduction of the impulse is rapid in the bundle and groove. Its location is consistently marked by a large central artery, its branches (2–3 m/sec, as opposed to 0.6 m/sec in normal myocar- which originates from either the proximal part of the right coronary or dium). The cardiac impulse therefore arrives at the apex of the heart circumflex arteries in equal proportion. Nodal cells are grouped circum- before spreading through the ventricular walls, producing a properly ferentially around the sinu-atrial nodal artery, packed within a dense coordinated ventricular ejection. The human heart beats ceaselessly at matrix of connective tissue as interlacing strands of myocytes. They are 70 cycles every minute for many decades, maintaining perfusion of smaller, paler and more empty-looking than working atrial myocardial pulmonary and systemic tissues. The rate and stroke volume fluctuate fibres, being 5–10 µm in their greatest diameter, with a large central in response to prevailing physiological demands. The principal events nucleus. Their pale appearance is attributable to the sparsity of in a cardiac cycle are summarized in Figure 57.20, including the elec- organelles; myofibrils are few and irregularly arranged, and there is no trical events recorded in the electrocardiogram; the mechanical proper sarcotubular system with little glycogen. sequences of diastole, atrial systole, volumetric contraction, ejection The sinu-atrial node is described as having a head, body and tail, and isovolumetric relaxation in ventricular systole; the acoustic phe- from which 5–8 short digitations of nodal tissue radiate towards the nomena recorded in the phonocardiogram; the pressure profiles of superior vena cava, subepicardium and crista terminalis, penetrating the right and left hearts and arterial trunks; and the sequences of valvular working atrial myocardium (Figs 57.38–57.39). At the nodal periphery, events. nodal cells intermingle with slender, fusiform, transitional ‘linking’ Cardiac efficiency depends on precise timing of the operation in cells that are part of a heterogeneous cellular group intermediate in interdependent structures. Passive diastolic filling of the atria and ven- appearance between nodal cells and normal working atrial myocytes. tricles is followed by atrial systole, stimulated by discharge from the (For further reading on the use of molecular markers to map the extent sinu-atrial node, which completes ventricular filling. Excitation and of nodal tissue, see Monfredi et al (2010).) There are no autonomic contraction of the atria must be synchronous and finish before ventricu- ganglion cells within the node, although many border it anteriorly and lar contraction; this is effected by a delay in the conduction of excitation posteriorly. Nerve fibres are present but do not appear to contact the from atria to ventricles. Thereafter, ventricular contraction proceeds in nodal myocytes. a precise manner. The atrioventricular valves are closed by ventricular Paranodal area systole, which must occur prior to closure; ventricular activation must therefore precede valvular closure, which spreads from the ventricular A paranodal area within the terminal crest, between the cells of the apices towards the outflow tracts and orifices. sinu-atrial node and the working atrial cardiomyocytes, and possessing Cardiac contraction originates unequivocally in specialized cardio- properties of both nodal and atrial tissues, has been identified (Molenaar myocytes, but neural influences are important in adapting the intrinsic et al 2011). Its precise function remains to be determined, but computer cardiac rhythm to functional demands from the entire body. All cardio- simulations suggest that it is an integral part of normal atrial activation myocytes are excitable. They display autonomous rhythmic depolariza- and may play a role in pacemaking. tion and repolarization of their cell membranes, conduction of waves Internodal atrial myocardium of excitation via gap junctions to adjacent cardiomyocytes, and excitation–contraction coupling to their actomyosin complexes. These Specialized pathways have been alleged to connect the sinus and atrio- properties are developed to different degrees in different sites and in ventricular nodes, but there is no evidence that tracts insulated from different types of cardiomyocyte (Ch. 6). The rate of depolarization and the working myocardium, as occurs in the ventricular conduction path- repolarization is slowest in the ventricular myocardium, intermediate ways, exist within the atrial walls. The impulse generated by the sinu- in the atrial muscle, and fastest in the myocytes of the sinu-atrial node. atrial node is conducted more rapidly via the long axis of the atrial The latter override those generating slower rhythms and, in the normal muscle bundles than it is transversely. The main pathways for conduc- heart, are the locus for the rhythmic initiation of cardiac cycles. Con- tion towards the atrioventricular node are the terminal crest and the versely, conduction velocity is slow in nodal myocytes, intermediate in margins of the oval fossa. Conduction to the left atrium is preferentially general ‘working’ cardiac myocytes, and fastest in the myocytes of the through Bachmann’s bundle; additional pathways occur through the ventricular conduction system. margins of the oval fossa and through the muscular connections The nodes and networks of the so-called specialized myocardial cells between the walls of the coronary sinus and left atrium. During devel- constitute the cardiac conduction system (Figs 57.36–57.37). The com- opment, the walls of the systemic venous sinus are exclusively com- ponents of this system are the sinus and atrioventricular nodes, the posed of primary myocardium. Although pathways within these walls atrioventricular bundle with its left and right bundle branches, and the may be identified in prenatal stages, primary myocardium is slowly subendocardial plexus of ventricular conduction cells (Purkinje cells). conducting, which means that these pathways do not represent areas of The main pacemaker rhythm of the heart (sinus rhythm) is generated preferentially rapid conduction. within the system but is influenced by nerves. It is transmitted specifi- Atrioventricular node cally from atria to ventricles via the atrioventricular node and bundle. The spread of excitation is very rapid but not instantaneous. Different The atrioventricular node is an oblique, half-oval atrial structure, located parts of the ventricles are excited at slightly different times, with impor- within the atrial component of the muscular atrioventricular septum tant functional consequences. Failure of the conduction system will not and separated from the ventricular musculature by the insulating tissues block cardiac contraction but the system will become poorly coordi- of the atrioventricular groove (see Fig. 57.37). Its anatomical landmarks nated. The rhythm will be slower because it originates from a spontane- are the boundaries of the triangle of Koch, i.e. the attachment of the ous (myogenic) activity in the working cardiac myocytes or in a septal leaflet of the tricuspid valve inferiorly, the ostium of the coronary subsidiary pacemaker in a more distal part of the diseased or disrupted sinus basally and the tendon of Todaro superiorly (see Fig. 57.13). The conduction system. There are no specialized internodal and interatrial atrial aspect of the node is convex and overlain by atrial myocardium. conduction pathways; the excitation emanating from the sinu-atrial Its left margin is concave and abuts on to the superior aspect of the node spreads to the atrial musculature and to the atrioventricular node central fibrous body. The basal end projects into the atrial muscle and through ordinary atrial working myocardium. The geometric arrange- the anteroinferior end enters the central fibrous body to become the ment of fibres along well-organized atrial muscle bundles, e.g. the ter- penetrating atrioventricular bundle. minal crest, the rims of the fossa ovalis and Bachmann’s bundle, ensures The node consists of two zones, compact and transitional, pervaded that conduction is marginally more rapid than elsewhere within the by an irregular collagenous reticulum that enmeshes the myocytes (Fig. atrium. 57.40). The compact zone consists of frequently stratified, interlocking nodal cells. Cells from the right and left atrial walls and the atrial Sinu-atrial node septum feed directly into the compact zone. The transitional zone In the majority of hearts, the sinu-atrial node is a crescent-shaped struc- envelops the compact portion of the node and consists of elongated ture, between 8 and 25 mm long, located at the embryonic junction ‘transitional cells’, intermediate in morphology and function between between the venous part (sinus venosus) and the atrium proper derived compact nodal cells and working atrial cardiomyocytes.
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Heart 1014.e1 75 RETPAHC Sinu-atrial node artery Terminal crest Endocardium A F Width Terminal crest A B C G D E F Detail of panel B 5 mm Fig. 57.38 Measurements of the width and height of the sinu-atrial node and the distances of nodal tissue to epicardium (a) and endocardium (b), measured in cadaveric tissue. (Top) A gross cadaveric specimen together with an example of a histological section and a diagram to indicate where measurements were made on each histological section. (Bottom) Histological sections (Masson trichrome stain) taken through levels A–F as indicated on the gross specimen. (G) The red dotted line delineates the nodal boundaries. Note the irregular contour of the node and the extensions towards the neighbouring myocardium (arrows). Abbreviations: SVC, superior vena cava. (With permission from Sánchez-Quintana D, Cabrera JA, Farré J, Climent V, Anderson RH, Ho SY. 2005. Sinu-atrial node revisited in the era of electroanatomical mapping and catheter ablation. 2005 91:189–94.) muidracipE Terminal groove SVC Height b a Histological sections Head Body Body Body Tail Tail f f f f f A B C Fig. 57.39 Histological sections of the nodal body. A, Fibro-fatty tissue (f) between the caudal aspect of the nodal body and the subendocardium. B–C, Fragmentation of the nodal tail into clusters. Masson trichrome stain. (With permission from Sánchez-Quintana D, Cabrera JA, Farré J, Climent V, Anderson RH, Ho SY. 2005. Sinu-atrial node revisited in the era of electroanatomical mapping and catheter ablation. 2005 91:189–94.)
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HEART 1014.e2 7 NOITCES Atrial Transitional Compact Atrial Penetrating Fig. 57.40 Histological sections showing the overlay cells cells AV node myocardium AV bundle features of (A) the atrioventricular (AV) node and (B) the penetrating atrioventricular bundle. Trichrome method, fibrous tissue stained green. (With permission from Anderson RH, Boyett MR, Dobrzynski H, Moorman AF. 2013. The anatomy of the conduction system: implications for the clinical cardiologist. J Cardiovasc Transl Res. 6:187–196.) A B Atrial Insulating Ventricular Insulating Ventricular septum tissues septum tissues myocardium
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Heart 1015 75 RETPAHC A Aorta Right pulmonary artery Right appendage Pulmonary valve Superior vena cava Sinu-atrial node Aortic mound Fossa ovalis Membranous part of interventricular septum Tendon of Todaro Radiation of left branch Valve of inferior vena cava Right bundle branch Coronary sinus Septal leaflet of tricuspid valve Inferior vena cava Atrioventricular node Septomarginal trabecula (moderator band) Papillary muscles B Aorta Left appendage Left pulmonary artery Cut chordae tendineae of mitral valve Right pulmonary veins Superoposterior papillary muscle Aortic valve Radiation of left branch Inferior vena cava Fig. 57.36 The conduction tissue of the heart. A, Right aspect. B, Left aspect. The elements of the conduction system are shown in purple. Conduction tissue accompanies fine trabeculae carneae and false chordae. In reality, the radiation of the left bundle branch is directly related to the leaflets of the aortic valve. Extensions of nodal cardiomyocytes run in the direction of the coro- Atrioventricular bundle nary sinus along the tricuspid anulus (the putative ‘slow pathway’); in the anterior portion of the triangle of Koch near the compact portion of The atrioventricular bundle (of His) is the direct continuation of the the atrioventricular node (the putative ‘fast pathway’); and in the direc- atrioventricular node. It becomes oval, quadrangular or triangular in tion of the mitral anulus (the left atrial extension) (Mani and Pavri transverse sectional profile as it enters the central fibrous body. It 2014). In both sinus and atrioventricular nodes, the intercellular con- traverses the fibrous body and branches on the crest of the muscular tacts between nodal cells, and between nodal and transitional cells, are interventricular septum; the branching tract is sandwiched between the much less specialized than the intercalated discs between normal cardiac muscular and the membranous components of the septum. cells (p. 137). A sparsity of gap junctions is consistent with the absence The right branch of the bundle (crus dextrum) is a narrow, discrete, from these areas of connexin-43 (a major protein component of mam- rounded group of fascicles that courses at first within the myocardium malian gap junctions), and probably accounts for the observed difficulty and then subendocardially towards the ventricular apex, entering the in exciting these cells from adjacent cells. The atrioventricular delay may septomarginal trabecula to reach the anterior papillary muscle. Its owe much to this relative non-excitability, which appears to disturb the branches to the ventricular walls are few in its septal course. At the spread of potential, delaying propagation; the narrow diameter of the origin of the anterior papillary muscle, it divides profusely into fine transitional cells may also contribute to conduction delay. subendocardial fascicles that diverge, first embracing the papillary The arterial supply to the atrioventricular node is from a character- muscle, then recurving subendocardially for distribution to the remain- istic vessel that originates from the dominant coronary artery at the ing ventricular walls. cardiac crux. Autonomic ganglia are present between the node and the The left branch (crus sinistrum) arises as numerous fine, intermin- coronary sinus. gling fascicles that leave the left margin of the branching bundle through
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HEART 1016 7 NOITCES oblique inverted crown within the atrioventricular groove. They also R form a variable and often insignificant anastomosis (in the non- pathological state) via marginal and interventricular (descending) loops that intersect at the cardiac apex. The main arteries and major P Q S T branches are usually subepicardial, but those in the atrioventricular and interventricular grooves are often deeply sited, and occasionally hidden by overlapping myocardium or embedded in it (myocardial bridging). The term ‘dominant’ is used to refer to the coronary artery giving off the posterior interventricular (posterior descending or inferior interven- Fibro-fatty atrioventricular groove (separation of atrial tricular) branch, which supplies the posterior (inferior) part of the SVC and ventricular myocardium) ventricular septum and often part of the posterolateral (inferolateral) wall of the left ventricle. The right artery is the dominant artery in 60% LA of hearts. Anastomoses between right and left coronary arteries are Sinu-atrial node (pacemaker) abundant in the fetus but are much reduced by the end of the first year RA of life. Anastomoses providing collateral circulation may become prom- Atrioventricular inent in conditions of chronic hypoxia and in coronary artery disease. node (delay) An additional collateral circulation is provided by small branches from Atrioventricular mediastinal, pericardial and bronchial vessels. bundle and branches (insulated) Coronary arterial original calibre, based on arterial casts or angio- gram measurements, ranges between 1.5 and 5.5 mm. The calibre of the left origin exceeds the right in 60% of hearts, the right being larger in 17%, and both vessels being of approximately equal calibre in 23%. The external diameter of the left coronary artery increases from 2.1 mm at the age of 1 year to 3.3 mm at the age of 15 years (Pesonen et al 1991) Purkinje fibres and the diameters of the coronary arteries may increase up to the 30th (activation) year. A significant association has been found between the diameters of the right and left coronary arteries at birth and at 1 and 6 months of Fig. 57.37 The basic structure of the conduction system and its age and birth weight, height and body surface area (Karagol et al 2012). relationship with the electrocardiogram. Note the foramen ovale allowing for communication between the right atrium (RA) and the left atrium (LA). Right coronary artery Other abbreviations: SCV, superior vena cava. (Redrawn by courtesy of Professor RH Anderson, Institute of Child Health, University College, The right coronary artery arises from the anterior (‘right coronary’) London.) aortic sinus; its ostium is usually below the sinutubular junction. The artery is usually single but as many as four right ostia have been observed, reflecting the independent origins of the conal, sinu-atrial node and ventricular arteries (Figs 57.42–57.43). The right coronary most of its course along the crest of the muscular ventricular septum artery passes at first anteriorly and slightly to the right between the right (see Fig. 57.36). These fascicles form a flattened sheet down the smooth atrial appendage and pulmonary trunk, where the sinus usually bulges. left ventricular septal surface that diverges apically and subendocar- On reaching the atrioventricular groove, it descends almost vertically to dially across the left aspect of the ventricular septum, trifurcating into the right (acute) cardiac border, curving around it into the posterior anterior, septal and posterior divisions. Fine branches leave the sheets, (inferior) part of the groove, where the latter approaches its junction forming subendocardial networks, which first surround the papillary with both interatrial and interventricular grooves, the appropriately muscles and then curve back subendocardially to be distributed to all termed cardiac crux. The artery ends a little to the left of the crux, often parts of the ventricle. The principal branches of the bundle are insulated by anastomosing with the circumflex branch of the left coronary artery. from the surrounding myocardium by sheaths of connective tissue. The right coronary artery may end near the right cardiac border, between Functional contacts between ventricular conduction and working this and the crux, or more often it reaches the left border, replacing the myocytes become numerous only in the subendocardial terminal rami- more distal part of the circumflex artery. Its branches supply the right fications. Hence, papillary muscles contract first, followed by a wave of and variable parts of the left chambers and atrioventricular septum. excitation and ensuing contraction that travels from the apex of the Usually, the first branch is the right conal artery (conus artery, artery of ventricle to the arterial outflow tract. Because the Purkinje network is the conus, arteria coni arteriosi; Loukas et al 2014b). (This vessel arises subendocardial, muscular excitation proceeds from endocardium to independently from the anterior aortic sinus in approximately one- epicardium. third of hearts and is therefore sometimes termed the ‘third coronary In the developing heart, the bundle responsible for atrioventricular artery’; a similarly named vessel arises from the left coronary circulation conduction is a much more extensive structure. Immunohistochemical and so this title is inappropriate.) The right conal artery ramifies antero- analysis has revealed that the precursor of the system is a ring of cells inferiorly over the pulmonary conus and over the superior aspect of the that surrounds the inlet and outlet components of the developing ven- right ventricle, sometimes anastomosing with a similar branch from the tricular loop (Ch. 52). left interventricular (anterior descending) artery to form the anulus of Vieussens, a tenuous anastomosis around the right ventricular outflow Cardiac pacing tract (Figs 57.44–57.45) (Loukas et al 2009). The first segment of the right coronary artery (between its origin and Available with the Gray’s Anatomy e-book the right cardiac margin) gives off anterior atrial and ventricular branches that diverge widely, approaching a right angle in the case of Cardiac conduction studies the ventricular arteries, an arrangement that is in marked contrast to the more acute origins of the left coronary ventricular branches. The Available with the Gray’s Anatomy e-book anterior ventricular branches, usually two or three, ramify towards the cardiac apex, which they rarely reach (unless the right marginal artery Congenital conduction abnormalities is included within this group of branches, as it is by some authors). The right marginal artery is greater in calibre than the other anterior ven- tricular arteries and long enough to reach the apex in most hearts. When Available with the Gray’s Anatomy e-book it is very large, there may be only one other remaining anterior ven- tricular branch, or even no other branches. Up to three small posterior (inferior) ventricular branches, most often two, arise from the second VASCULAR SUPPLY AND LYMPHATIC DRAINAGE segment of the right coronary artery between the right border and crux to supply the right ventricular diaphragmatic aspect. Their size is Coronary arteries inversely proportional to that of the right marginal artery, which usually extends to the cardiac diaphragmatic surface. On approaching the crux, The right coronary artery arises from the anterior (‘right coronary’) sinus the right coronary artery normally produces up to three posterior (infe- and the left coronary artery from the left posterior (‘left coronary’) sinus rior) interventricular branches (occasionally none). The posterior (infe- of the ascending aorta (see Figs 57.21–57.22; Fig. 57.41); ostia levels rior) interventricular artery itself, lying within the interventricular vary. The two arteries, as indicated by their generic name, form an groove, may therefore be flanked, either to the right or to the left, or on
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Heart 1016.e1 75 RETPAHC This ring is in continuity with the atrioventricular bundle, itself part of an interventricular ring of specialized cardiomyocytes. The segment of the interventricular ring that encircles the developing left ventricular outflow tract subsequently breaks down. The segment that persists within the ventricles extends along the septum beyond the branching atrioventricular bundle and forms a dead-end tract. The dorsal compo- nent of the interventricular ring is part of the definitive atrioventricular node, continuous with the atrioventricular bundle. The rightward com- ponent of the atrioventricular ring system, emerging inferiorly from the atrioventricular node, is part of the slow nodal pathway. The cardio- myocytes that formed the ring initially possessed a primary phenotype, i.e. they would have conducted slowly. Wolff–Parkinson–White syndrome is caused by abnormal small strands of otherwise unremarkable ventricular myocardium that run through the fibroareolar tissue of the atrioventricular groove, connect- ing the atrial and ventricular myocardial masses at some point around the atrioventricular junctions. Temporary pacing wires are usually inserted by cannulation of either the internal jugular or subclavian veins; the latter approach carries a slightly greater risk of a pneumothorax because of the proximity of the pleural cavity. Other potential risks are brachial plexus injury if the entry Conal artery Right coronary artery site is too posterior, and thoracic duct injury if the left subclavian vein Fig. 57.43 The right coronary sinus, revealing a coronary orifice for the is cannulated. The most common location for permanent pacemaker right coronary artery and a coronary orifice for the conal artery. (With devices is subcutaneously on the anterior chest wall. Access to the permission from Loukas M, Sharma A, Blaak C, Sorenson E, Mian A. chambers and endocardium of the right heart is gained via the cephalic 2013. The clinical anatomy of the coronary arteries. J Cardiovasc Transl vein within the deltopectoral groove. Res. 6:197–207.) Intracardiac electrocardiography and electrophysiology are used to assess cardiac conduction and rhythm abnormalities. A catheter is inserted via the femoral, subclavian or internal jugular veins using a guidewire technique. Fluoroscopy, echocardiography and, more recently, cardiac magnetic resonance are used to guide accurate place- Aorta ment of the catheters to the appropriate position. The sites of study are Right the high right atrium (for assessing the atrioventricular bundle and right coronary bundle branch) and the coronary sinus (for evaluating atrioventricular artery junctional arrhythmias and accessory pathways). The multipolar elec- Conal artery trodes provide detailed electro-anatomical mapping of the sequence of excitation from the atria, atrioventricular junction and ventricles. The * origin of supraventricular arrhythmias, ventricular tachycardias, acces- sory conduction pathways and re-entrant pathways can be identified Anterior and used to guide radiofrequency ablation. interventricular artery In the past, there was an anatomical basis for the majority of presenting congenital conduction abnormalities: they were the product of either Ventricular accessory pathways or conduction tissue dysgenesis at any point from branches the atrioventricular node to the atrioventricular bundle. Today, conduc- tion abnormalities are increasingly likely to relate to long-standing haemodynamic problems and/or the effects of previous surgery for ** patients with congenital heart defects. This reflects the fact that, although surgery for most of these defects has been available for the past four decades, surgery itself has not been curative; more often than not, patients develop conduction abnormalities and arrhythmia from surgi- *** cal scars that cause haemodynamic problems such as chamber dilation and/or hypertrophy. Occasionally, conduction abnormalities are caused by tumours such as multifocal Purkinje cell tumours, or benign con- genital polycystic tumours of the atrioventricular node. Congenital abnormalities of the coronary arteries are found rarely in children. The two most common abnormalities are coronary arterio- venous fistula and anomalous left coronary artery arising from the Fig. 57.44 A variation of the anulus of Vieussens (*). This corrosion cast pulmonary artery (Uysal et al 2014). Other congenital abnormalities specimen shows the right conal artery, a branch of the right coronary include ectopic origin of left circumflex artery from right coronary artery, anastomosing with a proximal ventricular branch of the anterior artery, single coronary artery arising from right sinus of Valsalva, and interventricular artery. A second anastomosis (**) occurs between the ectopic right coronary artery arising from the left sinus of Valsalva ventricular branches of the right coronary and anterior interventricular (Clemente et al 2010). arteries. Close to the apex, a third anastomosis (***) appears between the distal part of the anterior interventricular artery and branches of the acute marginal artery. (With permission from Loukas M, Bilinsky S, Bilinsky E, Matusz P, Anderson RH. 2009. The clinical anatomy of the coronary collateral circulation. Clin Anat. 22:146–160.)
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Heart 1017 75 RETPAHC A B Arch of aorta Pulmonary trunk Left coronary artery (main stem) Superior vena cava Anterior interventricular (descending) artery Sinu-atrial nodal artery Circumflex artery Left atrial auricle Right coronary artery Left atrial rami Outlines of: Left conal artery Anterior aortic sinus Circumflex artery Sinu-atrial artery Right posterior aortic sinus Left (obtuse) Left posterior aortic sinus marginal artery C Right conal artery Diagonal artery Right anterior ventricular arteries Atrioventricular Interventricular nodal artery anterior septal branches Inferior interventricular (descending) arteries Right (acute) marginal artery D E Ascending aorta Right posterior Pulmonary trunk Superior vena cava atrial arteries Left pulmonary veins Stem of posterior Right pulmonary veins atrial arteries Circumflex artery Region of crux of heart Inferior vena cava Right coronary artery Anterior interventricular (descending) artery (termination) Inferior interventricular (descending) arteries Fig. 57.41 Anterior views of the coronary arterial system, with the principal variations. The right coronary arterial tree is shown in purple, the left in red. In both cases, posterior distribution is shown in a paler shade. A, The most common arrangement. B, A common variation in the origin of the sinu-atrial nodal artery. C, An example of left ‘dominance’ by the left coronary artery, also showing an uncommon origin of the sinu-atrial nodal artery. Posteroinferior views of the coronary arterial system. The right coronary arterial tree is shown in purple, the left in red. D, An example of the more normal distribution in right ‘dominance’. E, A less common form of left ‘dominance’. In these ‘posterior’ views, the diaphragmatic (inferior) surface of the ventricular part of the heart has been artificially displaced and foreshortening ignored, to clarify the details of the so-called posterior (inferior) distribution of the coronary arteries.
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HEART 1018 7 NOITCES Aorta Fig. 57.42 A dissection of a cadaveric heart in which both coronary arteries have been exposed to reveal their branches to the right and left ventricles, respectively. Notice how the great cardiac vein is intertwined around the Left atrium anterior interventricular artery. Left coronary (Specimen courtesy of M Loukas MD, Arterial branch artery PhD.) Right coronary Sinu-atrial nodal artery artery Acute marginal Circumflex artery coronary artery Coronary sinus Diagonal arteries Ventricular branches Anterior Infundibular branch interventricular artery Great cardiac vein Conal artery Anterior lateral branches – occasionally double, and very rarely triple – mainly interventricular artery supply the right atrium. The posterior branch is usually single and sup- plies both atria. The artery of the sinu-atrial node is an atrial branch, distributed largely to right atrial myocardium. Its origin is variable: most commonly, it arises from the anterior atrial branch of the right coronary artery, less * often from its right lateral part, and least often from its posterior atriov- entricular part. This ‘nodal’ artery thus usually passes posteriorly in the groove between the right atrial appendage and aorta. It may originate from the circumflex branch of the left coronary artery. Whatever its ** origin, it usually branches around the base of the superior vena cava, typically as an arterial loop from which small branches supply the right atrium. A large branch, the ramus cristae terminalis, traverses the sinu- atrial node; it would seem more appropriate to name this branch the ‘nodal artery’, on the grounds that the vessel that currently bears this name actually supplies the atria and serves as the ‘main atrial branch’. Septal perforating branches of the right coronary artery are relatively *** short, and leave the posterior (inferior) interventricular branch to supply the posterior interventricular septum. They are numerous but do not usually reach the septal apex. The largest posterior septal perfo- rating artery, usually the first, commonly arises from the inverted loop Right coronary Ventricular artery branches said to characterize the right coronary artery at the crux; it almost always supplies the atrioventricular node. Small, recurrent atrioventricular Fig. 57.45 A coronary angiogram demonstrating three collateral arterial branches originate from the ventricular branches of the right coronary anastomoses. At the area of the subpulmonary infundibulum, the right artery as they cross the atrioventricular groove, and supply adjacent conal artery, a branch of the right coronary artery, anastomoses with the atrial myocardium. left conal artery, a branch of the anterior interventricular artery, to form the anulus (arterial circle or vascular ring) of Vieussens (*). Ventricular Left coronary artery branches of the right coronary artery anastomose with the proximal (**) and distal portions (***) of the anterior interventricular artery, forming two The left coronary artery is usually larger in calibre than the right. It collateral pathways. As a result, there is contrast medium in the anterior supplies a greater volume of myocardium, including almost all of the interventricular artery. (With permission from Loukas M, Bilinsky S, left ventricle and atrium, and most of the interventricular septum (see Bilinsky E, Matusz P, Anderson RH. 2009. The clinical anatomy of the Fig. 57.42; Figs 57.49–57.51). In hearts with ‘right dominance’, the coronary collateral circulation. Clin Anat. 22:146–160.) right coronary artery supplies a variable posterior region of the left ventricle (see Fig. 57.41A–C). The left coronary artery arises from the left posterior (left coronary) aortic sinus; the ostium sometimes lies inferior to the margin of the both sides, by these parallel branches. When these flanking vessels exist, leaflets and may be double, leading into major initial branches, usually branches of the posterior (inferior) interventricular artery are small and the circumflex and anterior interventricular (descending) arteries. Its sparse. The posterior (inferior) interventricular artery is occasionally initial portion, between its ostium and its first branches, varies in length replaced by a left coronary branch. Although the atrial branches of the from a few millimetres to a few centimetres. The artery lies between the right coronary artery are sometimes described as part of anterior, lateral pulmonary trunk and the left atrial appendage, emerging into the atrio- (right or marginal) and posterior groups, they are usually small single ventricular groove, where it turns left. This part is loosely embedded in vessels, 1 mm in diameter (Figs 57.46–57.48). The right anterior and subepicardial fat and usually has no branches, but may give off a small
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Heart 1018.e1 75 RETPAHC A PA Fig. 57.47 Normal ECG-gated multidetector row CT anatomy of the right coronary artery and its branches. This lateral oblique volume-rendered image shows the caudal course of the proximal right coronary artery (long Fig. 57.46 Normal ECG-gated CT anatomy of the right coronary artery arrow), which gives off an acute marginal branch (short arrows) to the and its branches. This oblique volume-rendered image of the superior right ventricle. (With permission from Kim SY, Seo JB, Do KH, et al. 2006. aspect of the heart shows the right coronary artery (arrow) arising from Coronary artery anomalies: classification and ECG-gated multi-detector the right sinus of Valsalva and coursing in the right atrioventricular groove row CT findings with angiographic correlation. Radiographics. 26:317–33.) towards the posterior interventricular septum. Abbreviations: A, aorta; PA, pulmonary artery. The conal artery and the sinu-atrial nodal artery were too small to be seen in this case. (With permission from Kim SY, Seo JB, Do KH, et al 2006. Coronary artery anomalies: classification and ECG-gated multi-detector row CT findings with angiographic correlation. Radiographics. 26:317–33.) PA A Fig. 57.49 Normal ECG-gated multidetector row CT anatomy of the left coronary artery and its branches. This oblique volume-rendered image of Fig. 57.48 Normal ECG-gated multidetector row CT anatomy of the right the top of the heart shows the left coronary artery (long white arrow) coronary artery and its branches. This posterior oblique volume-rendered arising from the left sinus of Valsalva and trifurcating into the left anterior image shows that the distal right coronary artery divides into the posterior interventricular artery (thick black arrow), the left circumflex artery (thin (inferior) interventricular artery (long black arrow) and posterior left black arrow), and the ramus intermedius (short white arrow), which takes ventricular branches (short black arrows). The posterior (inferior) a course similar to that of the usual first diagonal branch. The left anterior interventricular artery courses in the posterior (inferior) interventricular interventricular artery then gives rise to diagonal branches (short black groove, parallel to the middle cardiac vein (white arrow). (With permission arrows) to the anterior free wall of the left ventricle. Abbreviations: A, from Kim SY, Seo JB, Do KH, et al. 2006. Coronary artery anomalies: aorta; PA, pulmonary artery. (With permission from Kim SY, Seo JB, Do classification and ECG-gated multi-detector row CT findings with KH, et al. 2006. Coronary artery anomalies: classification and ECG-gated angiographic correlation. Radiographics. 26:317–33.) multi-detector row CT findings with angiographic correlation. Radiographics. 26:317–33.)
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HEART 1018.e2 7 NOITCES A PA Fig. 57.50 An anterior oblique volume-rendered image showing the left anterior ventricular artery (thin black arrows) coursing along the anterior interventricular groove, and the left circumflex artery (thick black arrow) coursing in the left atrioventricular groove. Obtuse marginal branches (short white arrow) and diagonal branches (short black arrows) are also Fig. 57.51 A posterior oblique volume-rendered image showing the left shown. Abbreviations: A, aorta; PA, pulmonary artery. (With permission anterior ventricular artery (long white arrows) coursing along the anterior from Kim SY, Seo JB, Do KH, et al. 2006. Coronary artery anomalies: interventricular groove, and the left circumflex artery (thick black arrow) classification and ECG-gated multi-detector row CT findings with coursing in the left atrioventricular groove. Obtuse marginal branches angiographic correlation. Radiographics. 26:317–33.) (short white arrows) and a diagonal branch (short black arrow) are also shown. (With permission from Kim SY, Seo JB, Do KH, et al 2006. Coronary artery anomalies: classification and ECG-gated multi-detector row CT findings with angiographic correlation. Radiographics. 26:317–33.)
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Heart 1019 75 RETPAHC Fig. 57.52 A dissection of a cadaveric heart revealing the course of the left Aorta coronary artery and its branches. (With Superior vena cava permission from Loukas M, Sharma A, Blaak C, Sorenson E, Mian A. 2013. The clinical anatomy of the coronary arteries. J Cardiovasc Transl Res. 6:197–207.) Conal artery Left atrium Circumflex Right atrium artery Diagonal artery Right coronary artery Anterior interventricular artery Acute marginal artery atrial ramus and, rarely, the sinu-atrial nodal artery. Reaching the atrio- posterior branches of the circumflex artery also supply the left ventricle. ventricular groove, the left coronary artery divides into its main branches: Anterior ventricular branches (from one to five, commonly two or namely, the circumflex and anterior interventricular arteries. three) course parallel to the diagonal artery when it is present, and The anterior interventricular artery is commonly described as the replace it when it is absent. Posterior ventricular branches are smaller continuation of the left coronary artery. It descends obliquely forwards and fewer because the left ventricle is partly supplied by the posterior and to the left in the interventricular groove (Fig. 57.52), sometimes (inferior) interventricular artery. When this artery is small or absent, it deeply embedded in or crossed by bridges of myocardial tissue (myo- is accompanied or replaced by often doubled or tripled interventricular cardial bridges), and by the great cardiac vein and its tributaries. continuations of the circumflex artery. Almost invariably, the anterior interventricular artery reaches the The artery to the sinu-atrial node is often derived from the anterior apex, where it terminates in one-third of hearts. More frequently, it circumflex segment (less often from the circum-marginal segment). It turns round the apex into the posterior interventricular groove and passes over and supplies the left atrium, encircles the superior vena cava passes one-third to one-half of the way along its length, meeting the (like a right coronary nodal branch) and sends a large branch through terminal twigs of the posterior (inferior) interventricular branches of the node; despite its name, it is predominantly atrial in distribution. the right coronary artery (see above). The artery to the atrioventricular node, sometimes the terminal branch The anterior interventricular artery gives off right and left anterior of the circumflex artery (20%), arises near the crux. When this occurs, ventricular and anterior septal branches, and a variable number of cor- the circumflex artery usually gives off the posterior interventricular responding posterior branches. Anterior right ventricular branches are artery, an example of so-called ‘left dominance’. small and rarely number more than one or two; the right ventricle is Coronary arterial distribution supplied almost entirely by the right coronary artery. Up to nine large left anterior ventricular arteries branch at acute angles from the anterior Details of coronary arterial distribution require integration into a interventricular artery, crossing the anterior aspect of the left ventricle concept of total cardiac supply. Most commonly, the right coronary diagonally, with the largest reaching the rounded (obtuse) left cardiac artery supplies all of the right ventricle (except a small region to the border. One often dominates, sometimes arising separately from the right of the anterior interventricular groove); a variable part of the dia- left coronary trunk, which then ends by trifurcation. This left diagonal phragmatic aspect of the left ventricle; the posteroinferior third of the artery, reported to exist in at least 33–50% of hearts, may be doubled interventricular septum; the right atrium and part of the left atrium; and (20%). A small left conal artery frequently leaves the anterior interven- the conduction system as far as the proximal parts of the right and left tricular artery near its origin, and anastomoses on the conus with its crura. Left coronary distribution is reciprocal and includes most of the counterpart from the right coronary artery and with the vasa vasorum left ventricle; a narrow strip of right ventricle; the anterior two-thirds of of the pulmonary artery and aorta. The anterior septal perforating the interventricular septum; and most of the left atrium. As noted previ- branches leave the anterior interventricular artery almost perpendicu- ously (see Fig. 57.41), variations in the coronary arterial system mainly larly, and pass posteroinferiorly within the septum, usually supplying affect the diaphragmatic aspect of the ventricles and reflect the relative its ventral two-thirds. The first septal perforator artery usually supplies ‘dominance’ of coronary arterial supply. The term is misleading because the atrioventricular bundle at the point of its division. Small posterior the left artery almost always supplies a greater volume of tissue than septal branches from the same source supply the posterior third of the the right. In ‘right dominance’, the posterior (inferior) interventricular septum for a variable distance from the cardiac apex (Loukas et al artery is derived from the right coronary artery; in ‘left dominance’, it 2009). is derived from the left coronary artery. In the so-called ‘balanced’ The circumflex artery, comparable to the anterior interventricular pattern, branches of both arteries run in or near the posterior (inferior) artery in calibre, curves left in the atrioventricular groove, and continues interventricular groove. round the left cardiac border into the posterior part of the groove, ter- Less is known about variations in atrial supply because the small minating left of the crux in most hearts, although sometimes continu- vessels involved are not easily preserved in the corrosion casts that are ing as the posterior (inferior) interventricular artery. Proximally, the left used for analysis. In more than 50% of individuals, the right atrium is atrial appendage usually overlaps it. A large ventricular branch, the left supplied only by the right coronary artery, and in the remainder the marginal artery, normally arises perpendicularly from the circumflex supply is dual. More than 62% of left atria are supplied mainly by the artery and ramifies over the rounded ‘obtuse’ margin, supplying much left coronary artery, 27% by the right coronary artery (in each group a of the adjacent left ventricle, typically to its apex. Smaller anterior and small accessory supply from the other coronary artery exists), and 11%
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Heart 1019.e1 75 RETPAHC Aorta Pulmonary vein Pulmonary Left auricle trunk Conal artery Circumflex artery Right coronary Diagonal artery artery Myocardial bridge Anterior interventricular artery Fig. 57.53 A dissection of a cadaveric heart in which a large part of the anterior interventricular artery is covered by a myocardial bridge. Myocardial bridges are reported to have a frequency varying from 0.5 to 40% when identified clinically and from 15 to 85% when found at autopsy (Fig. 57.53). The wide variation in frequency indicates that many bridges may be asymptomatic during life. The major clinical conditions produced by a myocardial bridge are cardiac ischaemia, atherosclerosis and sudden cardiac death. The incidence of atheroscle- rosis is increased when the right coronary artery is bridged. Although a relationship between myocardial bridges and sudden cardiac death has not been established, autopsy series have shown histological evidence of otherwise unexplained ischaemia in individuals with myocardial bridges; many died during exercise and had no other risk factors for coronary arterial disease.
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HEART 1020 7 NOITCES are supplied almost equally by both arteries. Arterial supply to the sinu- develop later in life. Congenital fistulae are more common and account atrial and atrioventricular nodes also varies: the sinu-atrial node is for 50% of paediatric coronary vascular aberrations; they are believed supplied more often by the right coronary artery; fewer than 10% of to be derived from Thebesian vessels. Acquired coronary artery fistulae sinu-atrial nodes receive a bilateral supply. The atrioventricular node is are most commonly iatrogenic in aetiology but may also occur after usually supplied by the right coronary artery. traumatic injury; these most commonly are of the coronary cameral type, from the right coronary artery into the right side of the heart. Coronary anastomoses The cardiac collateral circulation represents a native system for coronary Cardiac veins arterial bypass. The first few centimetres of the arterial main stems are devoid of anastomotic branches, but further distally, collateral channels The cardiac venous system is divided into two major parts. The greater are abundant, exhibit variable calibres and occupy numerous locations, system consists of large vessels that lie within the subepicardial myo- allowing for bidirectional flow between most native arteries. Approxi- cardium and drain most of the outer myocardium. These veins extend mately 30 different sites of collateral extramural vessels have been over the myocardial surface and do not adhere to topographical borders, described, the most frequent being at the apex; the anterior aspect of although the larger collecting vessels lie within the interventricular the right ventricle; the posterior aspect of the left ventricle; the crux; grooves before draining into the coronary sinus. The intercommunicat- the interatrial and interventricular grooves; and between the sinu-atrial ing parts of this system are the coronary sinus and its tributaries, the nodal and other atrial vessels (see Figs 57.44, 57.45). Anastomoses anterior cardiac venous system, and the ventricular septal and atrial between branches of the coronary arteries, both subepicardial and myo- veins. The coronary sinus and its tributaries return blood to the right cardial, and between these arteries and extracardiac vessels, are of prime atrium from the entire heart (including its septa), except for the anterior medical importance. Clinical studies suggest that anastomoses cannot region of the right ventricle and small, variable parts of both atria and rapidly provide collateral routes sufficient to circumvent sudden coro- the left ventricle. The anterior cardiac veins drain an anterior region of nary obstruction (see Figs 57.44, 57.45, 57.54). Nevertheless, it has long the right ventricle, expanding to include a region around the right been established that anastomoses do occur, particularly between fine cardiac border when the right marginal vein joins this group. subepicardial branches, and they may increase during individual life by The smaller system functions primarily to return venous blood from mechanisms of angiogenesis and arteriogenesis. The anulus of Vieus- the inner myocardial walls into the right atrium and ventricle and, to sens is a collateral vessel that crosses the subpulmonary infundibulum, a lesser extent, into the left atrium and sometimes the left ventricle. It providing an anastomosis between the conal branch of the right coro- contains the smallest cardiac veins (Thebesian veins) that drain the nary artery and the anterior interventricular artery. The artery to the subendocardial myocardium either directly, via connecting intramural sinu-atrial node commonly provides a communication between the arteries and veins, or indirectly, via subendocardial sinusoidal spaces. proximal parts of the coronary arteries. The apical collateral artery joins the interventricular arteries. The frequent enlargement of the first septal Variation in cardiac veins Attempts to categorize variations in branch of the anterior inter ventricular artery, Kugel’s anastomotic artery cardiac venous circulation into ‘types’ have not produced any accepted (arteria anastomotica auricularis magna), has been described as running pattern. The coronary sinus may receive all the cardiac veins other than between the proximal parts of the coronary arteries along the antero- the Thebesian veins, including the anterior cardiac veins, which may be superior margin of the oval fossa to anastomose with the distal part of reduced by diversion into the small cardiac vein and then to the coro- the right coronary artery. nary sinus. Extracardiac anastomoses Coronary sinus Extracardiac anastomoses connect various coronary branches with other Most cardiac veins drain into the wide coronary sinus, 2 or 3 cm long, thoracic vessels, most commonly involving the bronchial and internal lying in the posterior atrioventricular groove between the left atrium thoracic arteries (Fig. 57.54). To a much lesser degree, anastomoses and ventricle (see Fig. 57.4B; Fig. 57.59). The sinus opens into the right between coronary arteries and pericardiacophrenic branches of the atrium between the opening of the inferior vena cava and the right internal thoracic, anterior mediastinal, intercostal and oesophageal atrioventricular orifice. The opening may be guarded by an endocardial arteries also exist. The posterior pericardium also receives a direct fold (semilunar valve of the coronary sinus, Thebesian valve; see Fig. supply from the bronchial arteries; extracardiac coronary anastomoses 57.13A); the fold may be absent or may cover the ostium of the sinus involving bronchial arteries are typically found at the pericardial reflec- completely. The tributaries of the coronary sinus are the great, small tions, such as the points of entry of the venae cavae. The most common and middle cardiac veins, the posterior vein of the left ventricle and the anastomoses are with the circumflex branch of the left coronary artery oblique vein (of Marshall) of the left atrium; all except the oblique vein via the posterior pericardial reflections and reflect the close proximity have orificial valves. Isolated absence of the coronary sinus has been of the bronchial arteries within the pulmonary hila. In pathological reported, with coronary venous drainage into the pulmonary trunk conditions, notably those resulting in pericardial adhesions, it is (Ogawa et al 2013). also possible for extracardiac anastomoses to develop through trans- pericardial vascularization. Extracardiac communications also exist with coronary atrial branches, especially the sinu-atrial nodal artery. The effectiveness of any of these connections as collateral routes in coronary occlusion is not Aorta well quantified. Coronary arteriovenous anastomoses and numerous connections between the coronary circulation and cardiac cavities, pro- Pulmonary trunk ducing so-called ‘myocardial sinusoids’ and ‘arterioluminal vessels’, Superior vena cava have been reported, but their importance in coronary disease remains uncertain. Left pulmonary veins Coronary angiography Right pulmonary Oblique vein of veins left atrium Available with the Gray’s Anatomy e-book Great cardiac vein Coronary revascularization Right atrium Left marginal vein Available with the Gray’s Anatomy e-book Inferior vein of Coronary sinus left ventricle Coronary artery fistula Inferior vena A coronary artery fistula is an abnormal connection that directly links cava one or more coronary arteries to a heart chamber or to major thoracic vessels without an interposed capillary bed. Small cardiac vein Middle Coronary artery fistulae are rare (Fig. 57.58); those that arise from cardiac vein Right marginal vein a coronary artery and then terminate in a chamber of the heart are known as coronary cameral fistulae, while those terminating into a vein are coronary arteriovenous fistulae. Fistulae may be congenital or may Fig. 57.59 The principal veins of the heart.
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Heart 1020.e1 75 RETPAHC Table 57.1 Patterns of cardiac collateral arteries Anterior interventricular artery Grade Description 0 Total absence of any collateral arteries 1 Poorly developed collateral arteries with no prominent distal channel visualized by angiography 2 Presence of moderate collateral arteries providing faint but delayed opacification of a prominent distal channel 3 Good collateral arteries giving clear opacification of a prominent distal channel 4 Excellent collateralization giving full and brisk opacification of prominent distal vessels Clinical imaging (catheter angiography and colour Doppler ultra- sound) has led to the development of a grading system to describe the overall pattern of cardiac collateral arteries (Table 57.1). Coronary angiography may be performed by introducing a catheter through the femoral, radial or brachial arteries. The femoral artery is punctured with a needle 3 cm below the inguinal ligament while the leg is held adducted and slightly externally rotated. The exact position is guided by palpation of the femoral arterial pulse, and the needle is inserted at an angle of 45°. After arterial puncture, a fine guidewire is inserted through the needle and fed into the artery. The catheter is then Circumflex coronary artery Lower lobe of left lung inserted over the guidewire and manipulated via the iliac artery into the Fig. 57.54 A left coronary angiogram in left lateral projection, showing a aorta, up the aortic arch and into the ascending aorta. The brachial or large, tortuous vessel (arrow) arising from the proximal circumflex branch radial artery may be used for percutaneous access to the circulation. of the left coronary artery and anastomosing with the bronchial artery, Once the catheter is located in the ascending aorta, a variety of which goes on to supply the lower lobe of the left lung. (With permission guidewires may be used to enter the coronary vessels for selective arte- from Stefas L, Assayag P, Aubry P, et al, Coronary to bronchial artery riography and interventions. Angiography is performed with standard anastomosis with bronchial steal syndrome demonstrated by thallium-201 high-osmolality contrast medium with cineangiography. In selected myocardial tomoscintigraphy. Eur Heart J, 1990, 11, 275–279.) patients, new-generation, low-osmolality contrast medium may also be used. All the coronary arteries are catheterized and evaluated in a variety of views to obtain a full evaluation of their anatomy and to determine Cn the location and degree of any stenoses (Figs 57.55–57.56). The ostium of the left coronary artery arises from the left aortic sinus and is best viewed in the direct frontal and left anterior oblique projections. The SA right anterior oblique view is useful in demonstrating the diagonal branches and anterior interventricular (descending) coronary artery. The right coronary artery originates from the right sinus of Valsalva and is usually visualized in the right anterior oblique view. Pressure and Rv oxygen saturations can be measured via the catheter; changes in pres- sure across valves allow the degree of stenosis to be measured. Coronary blood flow and relative flow reserve can also be calculated. Significant Rm stenosis may be treated initially by balloon angioplasty followed by stent insertion. The balloon exerts pressure against the plaque in the arterial wall, fracturing and splitting the plaque. The splinting effect of the plaque and elastic recoil are reduced, resulting in an increase in the PIA arterial lumen. Stent insertion reduces the re-stenosis rate. Fig. 57.55 A right coronary angiogram showing several branches of the right coronary artery. Abbreviations: Cn, conal artery; PIA, posterior (inferior) interventricular artery; Rm, right marginal artery; Rv, right ventricular branches; SA, artery to the sinu-atrial node. (Courtesy of M Loukas MD, PhD.) LCA Sp AIA Latr LCx ObM PIA Fig. 57.56 A left coronary angiogram showing several branches of the left coronary artery (LCA). Other abbreviations: AIA, anterior interventricular artery; Latr, left atrial branch; LCx, left circumflex artery; ObM, obtuse marginal; PIA, posterior (inferior) interventricular artery; Sp, septal perforator. (Courtesy of M Loukas MD, PhD.)
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HEART 1020.e2 7 NOITCES Fig. 57.57 A, A left coronary angiogram showing a stent placement within the anterior interventricular artery. B, After stent placement (and once the contrast medium has filled the coronary arterial tree), the anterior interventricular artery shows no evidence of stenosis. Abbreviations: AIA, anterior interventricular artery; Stent Dg, diagonal branch; LCx, left circumflex artery. (Courtesy of M Loukas MD, PhD.) AIA LCx Dg A B Atherosclerosis causing more than 60% stenosis of the terminal diam- eter of the coronary arteries is likely to cause significant reduction in myocardial perfusion. Patients with high-grade lesions, left main stem coronary artery or triple-vessel disease with impaired left ventricular function are usually considered for coronary artery bypass grafting. The common grafts that are used are the internal thoracic (mammary) and radial arteries. The left internal thoracic artery and radial artery grafts have a greater patency rate than saphenous vein grafts. Approximately 15% of saphenous vein grafts occlude in 1 year and, from then on, at an annual rate of 1–2% in the first 6 years and 4% thereafter; between 40% and 50% of saphenous vein grafts have occluded by 10 years, whereas only about 10% of left internal thoracic or radial artery grafts have occluded over this time. The common surgical approach is via a midline sternotomy. If the internal thoracic artery is used as a donor graft, it is divided distally (maintaining its proximal origin from the subclavian artery) and anastomosed to the coronary artery distal to the A stenosis. If radial artery grafts are used, they must be anastomosed both proximal and distal to the coronary artery, to bridge the site of the stenosis. In selected cases, minimally invasive direct coronary artery bypass grafting is performed, but the approach is dependent on the vessel being grafted. The anterior approach is via mini-thoracotomy over the fourth intercostal space underneath the nipple for grafting the mid-left anterior interventricular (descending) and diagonal branches. The anterolateral approach is via an incision in the third intercostal space from the mid-clavicular to anterior axillary lines and is used for grafting early marginal branches of the circumflex system. The lateral approach allows grafting of the circumflex vessels via a lateral thora- cotomy measuring only 10 cm in size through the fifth or sixth inter- costal spaces. Extrathoracic approaches that are occasionally used include the subxiphoid approach for the distal right coronary artery and posterior interventricular (descending) artery. Port access surgery allows for full revascularization with cardiopulmonary bypass but obviates the need for midline sternotomy. However, the vast majority of patients are B treated with stent placement (Fig. 57.57). Fig. 57.58 A coronary artery fistula in a 54-year-old woman with palpitations. A, A CT image showing a tortuous left circumflex artery (white arrows) that is dilated in comparison with the anterior interventricular artery (black arrow). B, A volume-rendered CT image shows the markedly tortuous left circumflex artery (arrows). (With permission from Shriki JE, Shinbane JS, Rashid MA, Hindoyan A, Withey JG, DeFrance A, Cunningham M, Oliveira GR, Warren BH, Wilcox A. 2012. Identifying, characterizing, and classifying congenital anomalies of the coronary arteries. Radiographics 32:453–468.)
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Heart 1021 75 RETPAHC Great cardiac vein The great cardiac vein begins at the cardiac apex, veritable venous plexus. Not only are adjacent veins often connected, and ascends in the anterior interventricular groove to the atrioventricu- but connections also exist between tributaries of the coronary sinus and lar groove, which it follows, passing to the left and posteriorly to enter those of the anterior cardiac veins. Abundant anastomoses occur at the the coronary sinus at its origin (see Fig. 57.59). It receives tributaries apex and its anterior and posterior aspects. Like the coronary arteries, from the left atrium and both ventricles, including the large left mar- cardiac veins connect with extracardiac vessels, particularly the vasa ginal vein that ascends the left aspect (obtuse border) of the heart. It vasorum of the large vessels that are continuous with the heart. usually courses superior to the arterial branches. The valve of Vieussens normally guards the orifice of the great cardiac vein at its junction with Lymphatic drainage of the heart the oblique vein; smaller diminutive valves may occur. Cardiac lymphatic vessels form subendocardial, myocardial and sub- Small cardiac vein The small cardiac vein lies in the posterior atrio- epicardial plexuses. Efferents from the subepicardial plexuses form the ventricular groove between the right atrium and ventricle, receiving left and right cardiac collecting trunks; two or three left-sided trunks blood from their posterior parts and opening into the atrial end of the ascend the anterior interventricular groove, receiving vessels from both coronary sinus (see Fig. 57.59). The right marginal vein passes right, ventricles. On reaching the atrioventricular groove, they are joined by a along the inferior cardiac margin (acute border), and sometimes joins large vessel from the diaphragmatic surface of the left ventricle, which the small cardiac vein in the atrioventricular groove, typically opening first ascends in the posterior interventricular groove and then turns left directly into the right atrium. along the atrioventricular groove. The vessel formed by this union ascends between the pulmonary artery and the left atrium, and usually Middle cardiac vein The middle cardiac vein begins at the cardiac ends in an inferior tracheobronchial node. The right trunk receives apex and runs posteriorly in the inferior interventricular groove to end afferents from the right atrium and the right border and diaphragmatic in the coronary sinus near its atrial end (see Fig. 57.59). The vein is also surface of the right ventricle. It ascends in the atrioventricular groove, described as meeting the great cardiac vein at the apex, so forming, near the right coronary artery, and then anterior to the ascending aorta, together with the coronary sinus, a full venous circle. and ends in a brachiocephalic node, usually on the left (Fig. 57.60). (For further reading, see Loukas et al (2011).) Inferior vein of the left ventricle The inferior vein of the left ventricle (previously named as the posterior vein of the left ventricle) lies on the diaphragmatic surface of the left ventricle, a little to the left INNERVATION of the middle cardiac vein, and usually opens into the middle of the coronary sinus, sometimes into the great cardiac vein (see Fig. 57.59). Initiation of the cardiac cycle is myogenic, originating in the sinu-atrial Rarely, the inferior vein of the left ventricle is absent, in which case the node. It is harmonized in rate, force and output by autonomic nerves left marginal vein drains most of the left ventricular wall. that operate on the nodal tissues and their prolongations, on coronary vessels and on the working atrial and ventricular musculature. All the Oblique vein of the left atrium The diminutive oblique vein of cardiac branches of the vagus (parasympathetic) and all the sympathetic the left atrium descends obliquely on the posterior aspect of the left branches (other than the cardiac branch of the superior cervical sym- atrium to join the coronary sinus (see Fig. 57.59). It is continuous above pathetic ganglion) contain both afferent and efferent fibres; the cardiac with the ligament of the left vena cava; both structures are remnants of branch of the superior cervical sympathetic ganglion is entirely efferent. the left common cardinal vein. Sympathetic fibres accelerate the heart and dilate the coronary arteries Left marginal vein when stimulated, whereas vagal fibres slow the heart and cause coro- The left (obtuse) marginal vein courses over the left oblique marginal nary arterial constriction. surface of the heart, draining much of the left ventricular myocardium. Preganglionic cardiac sympathetic axons arise from neurones in the It runs superficial to the marginal branch of the left coronary artery and intermediolateral column of the upper four or five thoracic spinal seg- usually drains into the great cardiac vein, although may sometimes ments. Some synapse in the corresponding upper thoracic sympathetic drain directly into the coronary sinus. ganglia, while others ascend to synapse in the cervical ganglia; postgan- glionic fibres from these ganglia form the sympathetic cardiac nerves. Anterior cardiac veins Preganglionic cardiac parasympathetic axons arise from neurones either The anterior cardiac veins drain the anterior part of the right ventricle. in the dorsal vagal nucleus or near the nucleus ambiguus, and run in Usually two or three, sometimes even five, they ascend in subepicardial vagal cardiac branches to synapse in the cardiac plexuses and atrial tissue to cross the right part of the atrioventricular groove, passing deep walls. In humans (like most mammals), intrinsic cardiac neurones are or superficial to the right coronary artery. They end in the right atrium, limited to the atria and interatrial septum, and are most numerous in near the atrioventricular groove, separately or in variable combinations. the subepicardial connective tissue near the sinus and atrioventricular A subendocardial collecting channel, into which all may open, has been nodes. The intrinsic ganglia are thought not to be simple nicotinic described. relays, but may act as sites for the integration of extrinsic nervous inputs and form complex circuits for the local neuronal control of the heart, Right marginal vein and perhaps even local reflexes. The right marginal vein courses along the inferior (acute) cardiac margin, draining adjacent parts of the right ventricle, and usually opens Cardiac plexus separately into the right atrium, although it may join the anterior cardiac veins or, less often, the coronary sinus. It is often grouped with Nearing the heart, the autonomic nerves form a mixed cardiac plexus, the small cardiac veins but it is larger in calibre, comparable to the usually described in terms of a superficial component inferior to the anterior cardiac veins or even wider. aortic arch, lying between it and the pulmonary trunk, and a deep part Small cardiac veins between the aortic arch and tracheal bifurcation. The cardiac plexus is The existence of small cardiac (venae cordis minimae; Thebesian) veins, also described by regional names for its coronary, pulmonary, atrial and opening into all cardiac cavities, has been confirmed but they are dif- aortic extensions (Fig. 57.61). Ganglion cells are largely confined to the ficult to demonstrate. Their numbers and size are highly variable: vessels atrial tissues, with a preponderance adjacent to the sinu-atrial node, but up to 2 mm in diameter open into the right atrium and ones as small some may also be found within the heart along the branches of the as 0.5 mm in diameter open into the right ventricle, all with valveless plexuses. Their axons are considered to be largely, if not exclusively, orifices. Numerous small cardiac veins have been identified in the right postganglionic parasympathetic. Cholinergic and adrenergic fibres, atrium and ventricle but they are rarely found in the left side. Four types arising in or passing through the cardiac plexus, are distributed most of Thebesian veins have been described: venoluminal veins drain profusely to the sinus and atrioventricular nodes; the supply to the atrial directly into the cardiac chambers; venosinusoidal veins drain into and ventricular myocardium is much less dense. Adrenergic fibres subendocardial sinusoids (which, in turn, drain into the cardiac cham- supply the coronary arteries and cardiac veins. Rich plexuses of nerves bers); arterioluminal veins connect small arteries and arterioles directly containing cholinesterase, adrenergic transmitters and other peptides, with the cardiac chambers; and arteriosinusoidal veins connect thin e.g. neuropeptide Y, are found in the subendocardial regions of all arteries or arterioles with subendocardial sinusoidal spaces. chambers and within the valvular leaflets. Cardiac venous anastomoses Superficial (ventral) part of the cardiac plexus The superficial Widespread anastomoses occur at all levels of the cardiac venous circu- (ventral) part of the cardiac plexus lies inferior to the aortic arch and lation, on a scale exceeding that of the arteries and amounting to a anterior to the right pulmonary artery. It is formed by the cardiac branch
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HEART 1022 7 NOITCES Right internal jugular vein Paratracheal lymph nodes Fig. 57.60 The cardiac lymphatic system. (With permission from Loukas, M, Shah, S, Bhusnurmath S, et al; A general outline Left internal jugular vein Right lymphatic duct of the cardiac lymphatic system. In: The Cardiac Lymphatic System, Thoracic duct Karunamuni, G (ed). Springer. 2013.) Right subclavian vein Left brachiocephalic vein Right brachiocephalic vein Posterior mediastinal lymph nodes Posterior mediastinal lymph nodes Tracheobronchial lymph nodes Anterior mediastinal Anterior mediastinal lymph nodes lymph nodes Thoracic duct Right sympathetic trunk Left sympathetic trunk Fig. 57.61 The cardiac plexus: its source from the cervical parts of the vagus nerves and sympathetic Left vagus nerve trunks and its extensions, the Right vagus nerve pulmonary, atrial and coronary plexuses. Note the numerous junctions between sympathetic and Left recurrent laryngeal nerve Right recurrent parasympathetic (vagal) branches laryngeal nerve that form the plexus. Left common carotid artery Trachea Oesophagus Left subclavian artery Right recurrent laryngeal nerve Third thoracic sympathetic ganglion Thoracic cardiac branch of vagus nerve Thoracic (sympathetic) Brachiocephalic trunk cardiac branches Thoracic cardiac branch Thoracic (sympathetic) of vagus nerve cardiac branches Arch of aorta Deep cardiac plexus Superficial cardiac plexus Left recurrent laryngeal nerve Ligamentum arteriosum Left pulmonary artery Superior vena cava
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Heart 1023 75 RETPAHC of the left superior cervical sympathetic ganglion and the lower of the onwards to form part of the right coronary plexus. Fibres passing pos- two cervical cardiac branches of the left vagus. A small cardiac ganglion terior to the pulmonary artery supply a few filaments to the right atrium is usually present in this plexus immediately below the aortic arch, to and then continue into the left coronary plexus. The left half of the deep the right of the ligamentum arteriosum. This part of the cardiac plexus part of the cardiac plexus is connected to the superficial part; it supplies connects with the deep part, the right coronary plexus and the left filaments to the left atrium and left anterior pulmonary plexus, and anterior pulmonary plexus. forms much of the left coronary plexus. Deep (dorsal) part of the cardiac plexus The deep (dorsal) part Left coronary plexus The left coronary plexus is larger than the of the cardiac plexus lies anterior to the tracheal bifurcation, superior right and is formed mainly by the prolongation of the left half of the to the point of division of the pulmonary trunk and posterior to the deep part of the cardiac plexus and a few fibres from the right half. It aortic arch. It is formed by the cardiac branches of the cervical and accompanies the left coronary artery to supply the left atrium and upper thoracic sympathetic ganglia, the vagus and recurrent laryngeal ventricle. nerves. The only cardiac nerves that do not join it are those that join the superficial part of the plexus. The deep plexus consists of right and Right coronary plexus The right coronary plexus is formed from left halves; the right typically surrounds the brachiocephalic trunk, and both superficial and deep parts of the cardiac plexus. It accompanies the left surrounds the aortic arch. The more dorsal (deep) aspect is the right coronary artery to supply the right atrium and ventricle. larger than its more ventral (superficial) aspect on both sides. Branches from the right half of the deep part of the cardiac plexus pass both Atrial plexuses The atrial plexuses are derivatives of the right and anterior and posterior to the right pulmonary artery. Fibres passing left continuations of the cardiac plexus along the coronary arteries. anterior to the pulmonary artery are more numerous; they supply a few Their fibres are distributed to the corresponding atria, overlapping those filaments to the right anterior pulmonary plexus before continuing from the coronary plexuses. Bonus e-book images and table Fig. 57.5 Acute cardiac tamponade due to F, Transposition of the great arteries at 21 ventricular artery coursing along the anterior ruptured aortic dissection. weeks’ gestation. interventricular groove, and the left circumflex artery coursing in the left Fig. 57.6 A, The subxiphoid approach in Fig. 57.35 A, Cardiac magnetic resonance atrioventricular groove. pericardiocentesis. B, A mid-sagittal section angiography in a patient with a normal of a cadaver. C, A cross-section of the heart. B, A cardiac magnetic resonance Fig. 57.51 A posterior oblique volume- lower part of the thorax to show the angiogram from a patient with transposition rendered image showing the left anterior relationships of the pericardial cavity with of the great arteries. ventricular artery coursing along the anterior adjacent structures. D, Bedside cardiac interventricular groove, and the left ultrasound performed in a 62-year-old male, Fig. 57.38 Measurements of the width and circumflex artery coursing in the left demonstrating a large pericardial effusion height of the sinu-atrial node and the atrioventricular groove. consistent with cardiac tamponade. distances of nodal tissue to epicardium and endocardium, measured in cadaveric tissue. Fig. 57.53 A dissection of a cadaveric Fig. 57.7 The typical appearance of a heart in which a large part of the anterior pericardial cyst. Fig. 57.39 Histological sections of the nodal interventricular artery is covered by a body. myocardial bridge. Fig. 57.8 Congenital absence of the pericardium. Fig. 57.40 Histological sections showing the Fig. 57.54 A left coronary angiogram in left features of (A) the atrioventricular (AV) node lateral projection, showing a large, tortuous Fig. 57.11 The fundamental differences and (B) the penetrating atrioventricular vessel arising from the proximal circumflex between describing the heart according to bundle. branch of the left coronary artery and the conventional (A) or the attitudinally anastomosing with the bronchial artery, correct (B) orientation. Fig. 57.43 The right coronary sinus, which goes on to supply the lower lobe of revealing a coronary orifice for the right the left lung. Fig. 57.15 An inferior view of a cadaveric coronary artery and a coronary orifice for heart, demonstrating an exaggerated the conal artery. Fig. 57.55 A right coronary angiogram Eustachian valve occupying a significant showing several branches of the right portion of the lumen of the inferior vena Fig. 57.44 A variation of the anulus of coronary artery. cava. Vieussens. Fig. 57.56 A left coronary angiogram Fig.57.16 Chiari’s network. Fig. 57.46 Normal ECG-gated CT anatomy showing several branches of the left of the right coronary artery and its branches. coronary artery. Fig. 57.31 A histological section through one of the coronary aortic sinuses to Fig. 57.47 Normal ECG-gated multidetector Fig. 57.57 A, A left coronary angiogram demonstrate the way in which ventricular row CT anatomy of the right coronary artery showing a stent placement within the muscle supports the transition from the and its branches. anterior interventricular artery. B, After stent fibroelastic wall of the sinus to the tissues of placement (and once the contrast medium the leaflet. Fig. 57.48 Normal ECG-gated multidetector has filled the coronary arterial tree), the row CT anatomy of the right coronary artery anterior interventricular artery shows no Fig. 57.34 A, Tricuspid atresia at 21 weeks’ and its branches. evidence of stenosis. gestation. B, An atrioventricular septal defect at 20 weeks’ gestation. C, Fig. 57.49 Normal ECG-gated multidetector Fig. 57.58 A coronary artery fistula in a Hypoplastic left heart syndrome at 32 row CT anatomy of the left coronary artery 54-year-old woman with palpitations. weeks’ gestation. D, Hypoplastic left heart and its branches. syndrome at 32 weeks’ gestation. E, Table 57.1 Patterns of cardiac collateral Tetralogy of Fallot at 33 weeks’ gestation. Fig. 57.50 An anterior oblique volume- arteries. rendered image showing the left anterior
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Heart 1023.e1 75 RETPAHC REFERENCES Anderson R, Smerup M, Sanchez-Quintana D et al 2009a The three- Loukas M, Patel S, Cesmebasi A et al 2014b The clinical anatomy of the dimensional arrangement of the myocytes in the ventricular walls. Clin conal artery. Clin Anat. doi: 10.1002/ca.22469 (ePub ahead of print). Anat 22:64–76. Loukas M, Tubbs RS, Bright JL et al 2007 The anatomy of the tendon of the Anderson RH, Boyett MR, Dobrzynski H et al 2013a The anatomy of the infundibulum revisited. Folia Morphol (Warsz) 66:33–8. conduction system: implications for the clinical cardiologist. J Cardio- Mani BC, Pavri BB 2014 Dual atrioventricular nodal pathways physiology: vasc Transl Res 6:187–96. a review of relevant anatomy, electrophysiology, and electrocardio- Anderson RH, Loukas M 2009 The importance of attitudinally appropriate graphic manifestations. Indian Pacing Electrophysiol J 14:12–25. description of cardiac anatomy. Clin Anat 22:47–51. Molenaar P, Anderson R, Sharma V et al 2011 Computer three-dimensional Anderson RH, Spicer DE, Hlavacek AM et al 2013b Wilcox’s Surgical anatomical reconstruction of the human sinus node and a novel para- Anatomy of the Heart, 4th ed. Cambridge: Cambridge University nodal area. Anat Rec (Hoboken) 294:970–9. Press. Mollova M, Bersell K, Walsh S et al 2013 Cardiomyocyte proliferation Azancot A, Caudell TP, Allen HD et al 1983 Analysis of ventricular shape by contributes to heart growth in young humans. Proc Nat Acad Sci U S A echocardiography in normal fetuses, newborns, and infants. Circulation 110:1446–51. 68:1201–11. Monfredi O, Dobrzynski H, Mondal T et al 2010 The anatomy and physiol- Clemente A, Del Borrello M, Greco P et al 2010 Anomalous origin of the ogy of the sinoatrial node – a contemporary review. Pacing Clin Elec- coronary arteries in children: diagnostic role of three-dimensional coro- trophysiol 33:1392–406. nary MR angiography. Clin Imaging 34:337–43. Nidorf SM, Picard MH, Triulzi MO et al 1992 New perspectives in the assess- de Jonge LL, van Osch-Gevers L, Willemsen SP et al 2011 Growth, obesity, ment of cardiac chamber dimensions during development and adult- and cardiac structures in early childhood: the Generation R study. hood. J Am Coll Cardiol 19:983–8. Hypertension 57:934–40. Ogawa K, Hishitani T, Hoshino K 2013 Absence of the coronary sinus with Ho SY, McCarthy KP, Faletra FF 2011 Anatomy of the left atrium for inter- coronary venous drainage into the main pulmonary artery. Cardiol ventional echocardiography. Eur J Echocardiogr 12:11–15. Young 23:759–62. Hutchison SJ 2009 Pericardial Diseases: Clinical Diagnostic Imaging Atlas. Ozdemir O, Hizli S, Abaci A et al 2010 Echocardiographic measurement of Philadelphia: Saunders; pp. 8–15. epicardial adipose tissue in obese children. Pediatr Cardiol 31: Kaiser T, Kellenberger CJ, Albisetti M et al 2008 Normal values for aortic 853–60. diameters in children and adolescents – assessment in vivo by contrast- Pesonen E, Hirvonen J, Karkola K et al 1991 Dimensions of the coronary enhanced CMR-angiography. J Cardiovasc Magn Reson 10:56. arteries in children. Ann Med 23:85–8. Karagol BS, Orun UA, Zenciroglu A et al 2012 The diameter of coronary Poutanen T, Tikanoja T, Sairanen H et al 2006 Normal mitral and aortic arteries in healthy newborns at birth, 1 and 6 months of ages. J Matern valve areas assessed by three- and two-dimensional echocardiography Fetal Neonatal Med 25:2729–34. in 168 children and young adults. Pediatr Cardiol 27:217–25. Kortelainen ML 1997 Adiposity, cardiac size and precursors of coronary Sánchez-Quintana D, Pizarro G, López-Mínguez JR et al 2013 Standardized atherosclerosis in 5 to 15-year-old children: a retrospective study of 210 review of atrial anatomy for cardiac electrophysiologists. J Cardiovasc violent deaths. Int J Obes Relat Metab Disord 21:691–7. Transl Res 6:124–44. Loukas M, Abel N, Tubbs RS et al 2011 The cardiac lymphatic system. Clin Spicer DE, Anderson RH 2013 Methodological review of ventricular Anat 24:684–91. anatomy – the basis for understanding congenital cardiac malforma- Loukas M, Bilinsky E, Bilinsky S et al 2014a The anatomy of the aortic root. tions. J Cardiovasc Transl Res 6:145–54. Clin Anat 27:748–56. Uysal F, Bostan OM, Semizel E et al 2014 Congenital anomalies of coronary Loukas M, Groat C, Khangura R et al 2009 The normal and abnormal arteries in children: the evaluation of 22 patients. Pediat Cardiol anatomy of the coronary arteries. Clin Anat 22:114–28. 35:778–84.
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CHAPTER 58 Great vessels pulmonary trunk atretic, small or even normal in size, making diagnosis MAJOR BLOOD VESSELS challenging. A diminished pulmonary flow is supplied through a patent ductus arteriosus (Smith and McKay 2004), and a concomitant ven- The major blood vessels are the pulmonary trunk, the thoracic aorta tricular septal defect may permit outflow from the right ventricle. Surgi- and its branches, and the superior and inferior venae cavae and their cal repair is necessary to allow adequate oxygenation throughout the tributaries. body. In truncus arteriosus, a single arterial trunk exits the heart and sub- sequently divides into the pulmonary trunk and the aorta. Early neo- ARTERIES natal life is possible because there is usually a coexisting ventricular septal defect; expedited surgical repair is necessary to avoid congestive Pulmonary trunk heart failure, failure to thrive and death. Right and left pulmonary arteries The pulmonary trunk, or pulmonary artery, conveys deoxygenated blood from the right ventricle to the lungs. About 5 cm in length and The pulmonary arteries are described on page 959. 3 cm in diameter, it is the most anterior of the cardiac vessels and arises from the pulmonary anulus surrounding the subpulmonary infundibu- Thoracic aorta lum at the base of the right ventricle, superior and to the left of the supraventricular crest. It slopes posterosuperiorly, at first anterior to the Ascending aorta ascending aorta and then to its left; at the level of the fifth thoracic vertebra, inferior to the aortic arch at the left of the midline, it divides The ascending aorta is typically 5 cm long. It originates at the base of into right and left pulmonary arteries, of almost equal size. The bifurca- the left ventricle, level with the inferior border of the third left costal tion of the pulmonary trunk lies anteroinferior and to the left of the cartilage, and ascends obliquely, curving anteriorly and to the right, and tracheal bifurcation and its associated inferior tracheobronchial lymph passing from posterior to the left half of the sternum to the level of the nodes and deep cardiac plexus. In the fetus, at the level of the bifurca- superior border of the second left costal cartilage. In children, the diam- tion, the pulmonary artery is connected to the aortic arch by the ductus eter of the thoracic aorta correlates most closely with body surface area arteriosus. (Kervancioglu et al 2006, Kaiser et al 2008). Relations The pulmonary artery is entirely within the pericardium, Relations The ascending aorta lies within the fibrous pericardium, enclosed with the ascending aorta in a common tube of visceral peri- enclosed in a tube of serous pericardium together with the pulmonary cardium. The fibrous pericardium gradually disappears within the trunk (see Figs 57.3, 57.4A–C). The infundibulum, initial segment of adventitia of the pulmonary arteries. Anteriorly, it is separated from the the pulmonary trunk and right appendage are anterior to its lower sternal end of the left second intercostal space by the pleura, left lung part. Superiorly, it is separated from the sternum by the pericardium, and pericardium. Posterior relations are the ascending aorta and left right pleura, anterior margin of the right lung, loose areolar tissue and coronary artery initially, then the left atrium. The ascending aorta ulti- the thymus or its remnants. The left atrium, right pulmonary artery and mately lies on its right. The appendage and coronary artery lie on each principal bronchus are posterior. The superior vena cava and right side of its origin. The superficial cardiac plexus lies between the pulmo- atrium, the former partly posterior, are to the right. The left atrium and, nary bifurcation and the aortic arch. The tracheal bifurcation, lymph more superiorly, the pulmonary trunk are to the left. At least two aort- nodes and nerves are superior, bilateral and to the right. icopulmonary bodies lie between the ascending aorta and the pulmo- nary trunk. The inferior aorticopulmonary body is near the heart and Variations and congenital conditions The pulmonary trunk is anterior to the aorta, and the middle aorticopulmonary body is near a relatively constant structure and there are minimal variations in the right side of the ascending aorta. healthy individuals. Congenital anomalies include pulmonary atresia The aortopulmonary window is a space between the pulmonary and truncus arteriosus. artery and aortic arch, bordered by the ascending aorta anteriorly, the The coronary arteries usually originate from within the aortic sinuses, descending aorta posteriorly, the mediastinal pleura laterally and the but occasionally may arise from ectopic locations. Most commonly, an left principal bronchus medially (Deutsch and Savides 2005) (Fig. ectopic left coronary artery arises from the pulmonary trunk or one of 58.3). It contains lymph nodes, fatty tissue, the ligamentum arteriosum its branches (Bland–White–Garland syndrome). This potentially fatal and the left recurrent laryngeal nerve. condition requires urgent surgical correction because the myocardium Aortic arch is supplied with pulmonary blood instead of systemic blood (Loukas et al 2009). Infantile symptoms include pallor, fatigue, irritability, weak The aortic arch continues from the ascending aorta (see Figs 57.3, cry, cough, dyspnoea, and signs of ischaemia and cardiac failure pre- 57.4A–C). Its origin, slightly to the right, is level with the superior cipitated by feeding, bowel movements or crying. The electrocardio- border of the right second sternocostal joint. The arch first ascends gram may reveal deep narrow Q waves, left ventricular hypertrophy and diagonally and posteriorly to the left over the anterior surface of the left axis deviation. Radiologically, cardiomegaly is present with left trachea, then posteriorly across its left side, finally descending to the ventricular and left atrial enlargement. Colour flow imaging can identify left of the fourth thoracic vertebral body, continuing as the descending the anomalous origin of the left coronary artery. The pulmonary trunk thoracic aorta. It terminates level with the sternal end of the left second may also give rise to the right coronary artery, the left interventricular costal cartilage and so lies wholly within the superior mediastinum. It (anterior descending) coronary artery, or even both coronary arteries. curves around the hilum of the left lung, and extends superiorly to the Typically, there is a large development of collateral vessels in the heart midlevel of the manubrium of the sternum. (Figs 58.1–58.2). The shadow of the arch is easily identified in frontal chest radio- Pulmonary atresia is caused by a complete obstruction of pulmonary graphs; its left profile is sometimes called the aortic ‘knuckle’ or ‘knob’ outflow and may be due to an absence or defect of the pulmonary (see Fig. 56.16). There may also be an ‘aortic nipple’ (the shadow of valvular leaflets. It is associated with a blind-ending pulmonary trunk the adjacent left superior intercostal vein crossing posteroanteriorly to 1024 that causes right ventricular hypoplasia. Reduced flow may render the its left). The aortic arch is best visualized in left anterior oblique views
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Great vessels 1024.e1 85 RETPAHC Pulmonary valve Left coronary artery orifice Anterior interventricular artery Tricuspid valve Fig. 58.1 A case of a left anterior interventricular artery arising from the pulmonary trunk. (Courtesy of Professor Loukas. With permission from Loukas M, Groat C, Khangura R, Owens DG, Anderson R. The normal and abnormal anatomy of the coronary arteries. Clinical Anatomy. 2009; 22: 114–128.)
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GREAT vEssEls 1024.e2 7 NOITCEs A A PA PA A B A PPAA A PA * C D A PA Fig. 58.2 Bland–White–Garland syndrome in a 29-year-old woman. A, A preoperative anterior oblique volume-rendered (VR) image shows a dilated right coronary artery (arrow) and the anterior interventricular artery with multiple collateral vessels at the right ventricular wall (arrowheads). B–C, Preoperative VR images (cardiac chambers removed with manual editing) clearly demonstrate the anomalous origin of the left coronary artery (long arrow) from the pulmonary trunk, along with multiple collateral vessels within the interventricular septum (short arrows in B) and the dilated right coronary artery (short arrow in C). D–E, Postoperative VR images, obtained after ligation of the original os of the left coronary artery from the pulmonary trunk and creation of an anastomosis between the left internal thoracic artery (short white arrows) and the left coronary artery * (long white arrow), demonstrate a decrease in the size of the right coronary artery (black arrow) and markedly diminished collateral vessels in the interventricular septum and right ventricular wall (*). Abbreviations: A, aorta; PA, pulmonary artery. (With permission from Kim SY, Seo JB, Do KH, et al 2006 Coronary artery anomalies: classification and ECG-gated multi E detector row CT findings with angiographic correlation. Radiographics 26:317–33; discussion 333–4.)
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Major blood vessels 1025 85 RETPAHC AP window Pneumomediastinum and aortic nipple Available with the Gray’s Anatomy e-book Variations of the arch The summit of the arch is usually about 2.5 cm inferior to the sternal notch but may diverge from this. In the infant, it is closer to the superior border of the sternum; the same is often the case in senescence as a result of vascular ectasia/unfolding. In a right-sided aortic arch, the aorta curves over the right pulmonary hilum and descends to the right of the vertebral column; this is usually associated with transposition of the thoraco-abdominal viscera. Less often, after arching over the right hilum, the aorta may pass posterior to the oesophagus to gain its position (this is not accompanied by visceral transposition). The presence of a right-sided arch is of relevance to the paediatric surgeon who is planning repair of oesophageal atresia in neonates. The aorta may divide into ascending and descending trunks, the former dividing into three branches to supply the head and upper limbs. It may divide near its origin, producing a double aortic arch; the two branches soon reunite and the oesophagus and trachea usually pass through the interval between them. If the aorta, ductus arteriosus or descending aorta entraps the oesophagus and/or trachea, this is referred A to as a vascular ring. AP window Branches and variations Three branches arise from the convex aspect of the arch: the brachiocephalic trunk, left common carotid and left subclavian arteries (see Figs 57.3–57.4). They may branch from the beginning of the arch or the superior part of the ascending aorta. The distance between these origins varies, the most frequent being approxi- mation of the left common carotid artery to the brachiocephalic trunk. Other branches may arise from the aortic arch, including the inferior thyroid, thyroidea ima, thymic, left coronary and bronchial arteries (Bergman et al 1988). Coarctation of the aorta The aortic lumen is occasionally partly or completely obliterated, either above (preductal or infantile type), opposite or just beyond (postductal or adult type), the entry of the ductus arteriosus. In the preductal type, the length of coarctation is variable, aortic arch hypoplasia is common, and the left subclavian and even the brachiocephalic trunk may be involved. Severe forms of infan- tile coarctation and its extreme form (aortic interruption) may be patent B ductus arteriosus-dependent, as there is no time for effective collateral circulation to develop. Prostaglandin infusion prior to transfer, and surgery at a tertiary centre often provide a very good mid- to long-term Fig. 58.3 The aortopulmonary (AP) window. A, A posteroanterior (PA) outlook for such infants. chest radiograph. B, A coronal computed tomography (CT) scan The postductal type of coarctation has been attributed to abnormal reconstruction. extension of the ductal tissue into the aortic wall, stenosing both vessels as the duct contracts after birth. This form may permit years of on angiography and with equivalent computed tomography (CT) normal life, allowing the development of an extensive collateral circu- reconstruction planes; the pulmonary trunk and its left branch may be lation to the aorta distal to the stenosis (Figs 58.6–58.7). High vascu- discerned nestling inferiorly in its concavity. The diameter of the arch larity of the thoracic wall is important and clinically characteristic; initially matches that of the ascending aorta but is significantly reduced many arteries arising indirectly from the aorta proximal to the coarcta- distal to the origin of the great vascular branches. The aortic isthmus, a tion segment anastomose with vessels connected with it distal to the small stricture at the border with the descending thoracic aorta, may block, and all of these vessels become greatly enlarged. Thus, in the be followed by a dilation; in the fetus, the isthmus lies between the anterior thoracic wall, the thoraco-acromial, lateral thoracic and sub- origin of the left subclavian artery and the opening of the ductus scapular arteries (from the axillary artery), the suprascapular artery arteriosus. (from the subclavian artery) and the first and second posterior inter- costal arteries (from the costocervical trunk) anastomose with other Relations The left mediastinal pleura is anterior and to the left of the posterior intercostal arteries, and the internal thoracic artery and its arch. Deep to the pleura, the arch is crossed, in anteroposterior order, terminal branches anastomose with the lower posterior intercostal and by the left phrenic nerve, left lower cervical cardiac branch of the vagus inferior epigastric arteries. nerve, left superior cervical cardiac branch of the sympathetic trunk and Posterior intercostal arteries are always involved, and enlargement the left vagus nerve (see Figs 57.3, 57.61). As the left vagus nerve crosses of their dorsal branches may eventually groove (‘notch’) the inferior the arch, its recurrent laryngeal branch hooks below the vessel, to the margins of the ribs. The radiographic shadow of the enlarged left sub- left and behind the ligamentum arteriosum, then ascends on the right clavian artery is also increased. Enlargement of the scapular vessels and of the arch. The left superior intercostal vein ascends obliquely anteri- anastomoses may lead to widespread interscapular pulsation (easily orly on the arch, superficial to the left vagus nerve, deep to the left appreciated with the palm of the hand, and sometimes heard on phrenic nerve. The left lung and pleura separate all these from the auscultation). thoracic wall. Posterior and to the right are the trachea and the deep cardiac plexus, the left recurrent laryngeal nerve, oesophagus, thoracic Aortic aneurysm formation Degeneration of the aortic tunica duct and vertebral column. Superiorly, the brachiocephalic trunk, left media and intimal dissection play a major role in the pathogenesis of common carotid and subclavian arteries arise from its convexity, and aneurysms affecting the ascending aorta and arch. Smooth muscle cells are crossed anteriorly near their origins by the left brachiocephalic vein. are lost and elastic fibres degenerate, producing cystic spaces in the The pulmonary bifurcation, left principal bronchus, ligamentum arte- media, which then fill with mucoid material. The loss of these structural riosum, superficial cardiac plexus and the left recurrent laryngeal nerve cells leads to weakening of the wall with progressive dilation. Ageing are all inferior. The concavity of the aortic arch, best viewed from the and hypertension are major predisposing factors to cystic medial degen- left, is the upper curved limit through which structures gain access to, eration and there is a strong link with cigarette smoking. Thoracic aortic or leave, the hilum of the left lung. aneurysms are categorized by their location. A particular pattern of
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Great vessels 1025.e1 85 RETPAHC Pneumomediastinum is an encompassing term that describes the pres- Aortic arch Superior intercostal vein/aortic nipple ence of air in the mediastinum. It may arise from a wide range of pathological conditions or physiological states, e.g. penetrating trauma, ruptured major airways or oesophagus, hyperventilation or distressed ventilation such as acute asthma, periparturition or diabetic ketoacido- sis. The ‘aortic nipple’ is the radiographic term used to describe a lateral nipple-like projection from the aortic knuckle seen in a small number of individuals that corresponds to the end-on appearance of the left superior intercostal vein coursing anteriorly. It may be mistaken radio- logically for lymphadenopathy or an intrapulmonary nodule/neoplasm. Despite their relative independence, the aortic nipple is defined by new contours in cases of pneumomediastinum, taking on an ‘inverted aortic nipple’ appearance (Fig. 58.4). In this position, the inverted aortic nipple may facilitate radiographic discrimination of pneumomediasti- num from similar conditions. An aortic nipple has been shown to precede pathological conditions such as venous obstruction in the supe- rior and inferior vena cavae or left brachiocephalic vein, and has been identified in conditions where venous flow through the left superior intercostal vein is increased (e.g. portal hypertension and certain con- genital venous anomalies). There are several variants of this arrangement, of which the most common are as follows: a right-sided aortic arch and upper portion of the descending aorta pass anterior to the oesophagus and trachea, and the ductus arteriosus passes posterior to the oesophagus into an aortic diverticulum; a right-sided aortic arch and the upper portion of the descending aorta pass anteriorly, and the ductus arteriosus is inserted Pneumomediastinum Pleura into the left subclavian artery, which arises as a fourth branch from the aortic arch; a left-sided descending aorta is attached to a left-sided Fig. 58.4 A PA chest radiograph, anteroposterior view, showing the ductus arteriosus anterior to the oesophagus, and a right-sided arch classic ‘aortic nipple’ in a patient with pneumomediastinum. A label is added on the left to delineate the nipple-like appearance of the left passes posteriorly; the right superior portion of the descending aorta superior intercostal vein more clearly. (Courtesy of Professor Loukas. With wraps around the oesophagus and the ductus arteriosus is right-sided; permission from Walters A, Cassidy L, Muhleman M, Peterson A, Blaak C, or the right upper portion of the aorta wraps around the oesophagus Loukas M. Pneumomediastinum and the aortic nipple: the clinical and the ductus arteriosus is left-sided (Bergman et al 1988). relevance of the left superior intercostal vein. Clinical Anatomy 2013; The right common carotid and subclavian arteries may arise sepa- 27:757–63.) rately, in which case the latter often branches from the left end of the arch distal to the left subclavian artery, and usually passes posterior to the oesophagus as an aberrant right subclavian artery. When this artery arises from a dilated portion of the descending aorta, the diverticulum Right common carotid artery Trachea RtRSA Oesophagus of Kommerell, it is known as the lusoria artery (Fig. 58.5). It may become aneurysmal and cause fatal haemorrhage during endoscopy. It may form a vascular ring around the oesophagus and trachea, present- ing in the neonate as a feeding disorder with failure to thrive. The left vertebral artery may arise between the left common carotid and the subclavian arteries. A rare avian form has been reported in which the right common carotid and subclavian arteries arise from the aortic arch, and the left common carotid and subclavian arteries arise from the descending aorta (Bergman et al 1988). Another rare avian form with two brachio- cephalic trunks, the right trunk originating both common carotid arter- ies, and the left trunk originating both subclavian arteries, has been reported. Another rare order of the aortic branches is (in order from right to left): the right subclavian artery, left subclavian artery, followed by the right common carotid, and left common carotid arteries close together – almost forming a common carotid trunk. The aortic arch may also curve behind the oesophagus and trachea, instead of in front, with variations in the aortic branches as well. Another rare avian form reported is with both carotid arteries originat- ing from the same stem, and a left subclavian artery originating from the arch, while the right subclavian artery arises from the descending aorta. One or more of the ductus arteriosi may remain patent. Very rarely, external and internal carotid arteries arise separately, the Left common Right and left Left subclavian common carotid artery being absent on one or both sides, or both carotid artery vertebral arteries artery carotid arteries and one or both vertebral arteries may be separate Fig. 58.5 A dissection showing a left aortic arch that gives rise to a branches. When a ‘right aorta’ occurs, the arrangement of its three common vertebral trunk and a retrotracheal right subclavian artery branches is reversed and the common carotid arteries may have a single (RtRSA), also known as a lusoria artery. (Courtesy of Professor Loukas trunk. Other arteries may branch from it: most commonly, one or both with permission from Loukas M, Louis RG Jr, Gaspard J, Fudalej M, bronchial arteries and the thyroidea ima artery. Tubbs RS, Merbs W. A retrotracheal right subclavian artery in association Associations also exist between thoracic aortic aneurysm and other with a vertebral artery and thyroidea ima. Folia Morphol (Warsz). 2006 connective tissue diseases such as homocysteinuria and Ehlers–Danlos Aug;65(3):236–41.) syndrome. A genetic relation is seen in familial thoracic aortic aneurysm syndrome (Baliga et al 2007). Rarely, aneurysms may occur as a result of Takayasu’s arteritis, or infections within the aortic wall.
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GREAT vEssEls 1025.e2 7 NOITCEs Fig. 58.6 A cardiac magnetic resonance (MR) angiograph showing three-dimensional reconstruction of a native aortic coarctation (arrow) in an adult with extensive collateral flow. Note the marked dilation of the left subclavian artery, supplying most of the collateral vessels, and mild aortic arch hypoplasia. (Courtesy of Dr Raad Mohiaddin, Royal Brompton Hospital, London.) Fig. 58.7 The collateral circulation at MR angiography and phase-contrast velocity-encoded cine MRI. The MR angiogram shows the intercostal (short arrows) and internal thoracic (medium arrow) arteries, obtained in a patient with a haemodynamically significant aortic coarctation (long arrow). Note that the arteries appear enlarged. (With permission from Hom JJ, Ordovas K, Reddy GP. Velocity-encoded cine MR imaging in aortic coarctation: functional assessment of hemodynamic events. Radiographics 2008 Mar–Apr;28(2):407–16.)
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GREAT vEssEls 1026 7 NOITCEs aortic root involvement is seen in those with Marfan’s syndrome, diaphragm. The vertebral column and hemiazygos veins are posterior. known as anulo-aortic ectasia (Baliga et al 2007). Descending aortic Posterior to the right are the azygos vein and thoracic duct, and inferi- aneurysms are generally caused by atherosclerosis (90%); the remainder orly, the right pleura and lung; the pleura and lung are to the left. The result from mycotic disease or trauma. oesophagus with its plexus of nerves is located laterally and to the right Some aortic aneurysms are incidental findings on chest films or CT in the upper thorax, anteriorly in the lower thorax and descends to a studies. Symptomatic cases present with breathlessness, unbearable left anterolateral position when it reaches the diaphragm. To a limited chest and back pain, hoarse voice, cough and haemoptysis. Early diasto- degree, the descending aorta and oesophagus are mutually spiralized. lic murmurs caused by aortic regurgitation may be audible. Repair is Occasionally, the aorta enters the diaphragm to the left and behind the carried out in patients with symptoms or fusiform dilation measuring oesophagus (Berdjas and Turina 2011). more than 5 cm in diameter. Aneurysms may also occur in an aberrant right subclavian artery and Surface anatomy The descending thoracic aorta may be projected may or may not involve the diverticulum of Kommerell, leading to as a 2.5 cm broad band from the sternal end of the second left costal dysphagia and even tracheal compression. Inadvertent rupture may cartilage to a median position 2 cm above the transpyloric plane at the occur during endoscopy because of its retro-oesophageal position. first lumbar vertebra. Aortic dissection Branches The thoracic aorta provides visceral branches to the pericardium, Available with the Gray’s Anatomy e-book lungs, bronchi and oesophagus, and parietal branches to the thoracic wall. Aortopulmonary paraganglia Pericardial branches A few small vessels are distributed to the posterior aspect of the pericardium. Aortopulmonary paraganglia (aortic bodies) belong to the branchio- meric category of paraganglia. They are chemoreceptors and respond to Bronchial arteries Bronchial arteries vary in number, size and changes in arterial gas concentrations such as lowered pO, increased origin. There is usually only one right bronchial artery; it arises from 2 pCO and increased hydrogen ion concentration. These microscopic either the third posterior intercostal or the upper left bronchial artery, 2 structures occur in several locations within the thorax: coronary para- and runs posteriorly on the right principal bronchus. Its branches ganglia lie between the ascending aorta and pulmonary trunk, either supply these structures, the pulmonary areolar tissue and the broncho- anteriorly or posteriorly, adjacent to the aortic root; pulmonary para- pulmonary lymph nodes, pericardium and oesophagus. The left bron- ganglia lie in the groove between the ductus arteriosus and the pulmo- chial arteries, usually two, arise from the thoracic aorta – the upper near nary artery; and subclavian–supra-aortic paraganglia lie between either the fifth thoracic vertebra, the lower below the left principal bronchus the right subclavian and right common carotid arteries or the left sub- – and run posterior to the left main bronchus; their branches are dis- clavian and left common carotid arteries, or caudal to the left subclavian tributed as on the right. artery, adjacent to the aortic arch. Oesophageal branches Two or three bronchial arteries supply the Brachiocephalic trunk (artery) thoracic portion of the oesophagus. In addition, two or three oesopha- geal arteries that arise either anteriorly or from the right side of the aorta supply the distal oesophagus (Norton et al 2008). The brachiocephalic (innominate) artery (trunk), the largest branch of the aortic arch, is 4–5 cm in length (see Fig. 57.4A,B). It arises from the Mediastinal branches Numerous small vessels supply lymph convexity of the arch posterior to the centre of the manubrium of the nodes and areolar tissue in the posterior mediastinum. sternum, and ascends posterolaterally to the right, at first anterior to the trachea, then on its right. The brachiocephalic and left common Phrenic branches Superior phrenic arteries arise from the lower carotid arteries often share a common origin (Osborn 1998). It divides thoracic aorta and are distributed posteriorly to the superior diaphrag- into the right common carotid and subclavian arteries level with the matic surface, anastomosing with the musculophrenic and pericardi- upper border of the right sternoclavicular joint. acophrenic arteries. Relations Sternohyoid and sternothyroid, thymic remnants, left Posterior intercostal arteries The posterior intercostal arteries brachiocephalic and right inferior thyroid veins, crossing its root, and their branches are described on page 943. and sometimes the right cardiac branches of the vagus nerve, all sepa- rate the brachiocephalic trunk from the manubrium. Posterior are the Subcostal arteries Subcostal arteries are the last paired branches of trachea (superiorly) and the right pleura (inferiorly). The right vagus the thoracic aorta, in series with the posterior intercostal arteries and nerve is posterolateral before passing lateral to the trachea. On its right inferior to the twelfth ribs. Each runs laterally anterior to the twelfth side are the right brachiocephalic vein and the upper part of the supe- thoracic vertebral body and posterior to the splanchnic nerves, sympa- rior vena cava and pleura, and on its left side are thymic remains, the thetic trunk, pleura and diaphragm. The right subcostal artery is also origin of the left common carotid artery, the inferior thyroid veins and posterior to the thoracic duct and azygos vein, while the left is posterior the trachea. to the accessory hemiazygos vein. Each artery enters the abdomen at the lower border of the twelfth rib, accompanied by the twelfth thoracic Branches The brachiocephalic trunk usually has only terminal (subcostal) nerve, lying posterior to the lateral arcuate ligament and branches, the right common carotid and subclavian arteries. Occasion- kidney, and anterior to quadratus lumborum. The right artery courses ally, a thymic or bronchial branch, or a thyroidea ima artery arise from posterior to the ascending colon, and the left courses posterior to the it. The thyroidea ima artery is a small and inconstant artery that may descending colon. Piercing the aponeurosis of transversus abdominis, arise from the aorta, right common carotid, subclavian or internal each subcostal artery proceeds between this and internal oblique, and thoracic arteries; it ascends on the trachea to the thyroid isthmus, where anastomoses with the superior epigastric, lower posterior intercostal it terminates. and lumbar arteries. Each has a dorsal branch, distributed like those of the posterior intercostal arteries. Descending thoracic aorta Aberrant artery A small artery sometimes leaves the descending The descending aorta is the segment of the thoracic aorta that is con- thoracic aorta on its right near the right bronchial artery origin. It fined to the posterior mediastinum (see Figs 56.1–56.2, 56.6–56.7B, ascends to the right behind the trachea and oesophagus, and may anas- 56.13–56.14A, 56.19D,E). It begins level with the lower border of the tomose with the right superior intercostal artery. It is a vestige of the fourth thoracic vertebra, continuous with the aortic arch, and ends right dorsal aorta and, occasionally, it is enlarged as the first part of a anterior to the lower border of the twelfth thoracic vertebra in the aortic right subclavian artery. hiatus. At its origin, it is left of the vertebral column; as it descends, it reaches and terminates in the midline. Aortic rupture in trauma Rupture of the ascending aorta is usually associated with a high immediate mortality (Baliga et al 2007). Blunt Relations Anterior to the descending thoracic aorta, from superior to aortic rupture commonly occurs in road traffic accidents and has a 20% inferior, are the left pulmonary hilum, the pericardium separating it survival rate. There is usually a transverse tear involving the tunica from the left atrium, oesophagus and the vertebral portion of the intima and tunica media of the aortic wall; systemic circulatory pressure
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Great vessels 1026.e1 85 RETPAHC Aortic dissection occurs as a result of degeneration of the tunica media Aortic dissections are classified as types I, II, IIIa and IIIb (De Bakey of the aortic wall and is associated with senescence, persistent hyperten- classification), or types A and B (Stanford classification). Dissections sion or collagen vascular diseases such as Marfan’s syndrome. Many that are proximal to the left subclavian artery, with or without distal patients with aortic dissection have a pre-existing aneurysm. Other extension, are classified as type I, II or A. Type I may involve the entire associations include aortic coarctation, Turner’s syndrome, cocaine aorta, whereas type II involves the ascending aorta only. Dissections abuse (<1%) and trauma during surgical procedures. There is a higher that are distal to the left subclavian artery are classified as type IIIa prevalence in men than women; after the age of 75, however, there is (involve the distal aorta up to the diaphragm), IIIb (extend below the no sex difference (Baliga et al 2007). In a classic aortic dissection, an diaphragm) or B. These cases present acutely with severe retrosternal, intimal tear may occur, producing a split into the tunica media that neck or interscapular chest pain. Depending on the extent of the dis- creates a false lumen (Fig. 58.8). If another tear occurs, connection can section, they may be associated with neurological signs, diarrhoea or be made once again with the true lumen (the double-barrel aorta). leg weakness. Extension into the pericardium causes cardiac tamponade Additional aetiopathologies include penetrating atherosclerotic ulcera- and circulatory collapse. Diagnosis is established by echocardiography tion, where an atherosclerotic plaque ruptures into the aortic tunica and on contrast-enhanced CT or magnetic resonance imaging (MRI). media, and aortic intramural haematoma, where the vasa vasorum Medical management is possible for descending aortic dissections, haemorrhage into the wall of the aorta (Baliga et al 2007). while surgical repair is essential for ascending aortic or aortic arch dissection. A B C D E Fig. 58.8 A Stanford type A aortic dissection. A–B, Axial images taken through the thorax. A, Dissection flap involvement of the aortic root and descending aorta. B, The dissection flap in the aortic arch. C–E, A type A aortic dissection in a different patient. C–D, Sagittal reformatted images through the thorax and upper abdomen obtained at different levels from 64-slice multi-detector CT demonstrating intimal flap involvement of the ascending thoracic aorta. Note the extension of the dissection flap into aortic branch vessels (arrow). E, A sagittal maximum-intensity projection image showing dissection flap involvement of both the ascending and descending aorta. (With permission from McMahon MA, Squirrell CA. Multidetector CT of Aortic Dissection: A Pictorial Review. Radiographics. 2010 Mar;30(2):445–60.)
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Major blood vessels 1027 85 RETPAHC may cause the formation of a false aneurysm. Rupture of the isthmus VEINS region of the descending aorta is more common probably because it marks the junction between the mobile and fixed portions of the aorta. Brachiocephalic veins Other sites include the ascending aorta proximal to the origin of the brachiocephalic trunk, the aortic arch and the abdominal aorta. Rupture The right and left brachiocephalic veins join to form the superior is likely to be the result of a number of factors, including torsion, shear vena cava. and stretching forces, possibly compounded by hydrostatic pressure. Right brachiocephalic vein Aortic atherosclerosis or calcification Echocardiography, par- The right brachiocephalic vein is about 2.5 cm long. It arises posterior ticularly trans-oesophageal, allows very detailed assessment of proximal to the sternal end of the right clavicle and descends almost vertically to aortic atherosclerosis implicated in systemic embolic events and strokes. join the left brachiocephalic vein, forming the superior vena cava pos- The extent of turbulent flow may be documented. MRI may also allow terior to the inferior border of the first right costal cartilage, near the an accurate assessment of the composition and size of atherosclerotic right sternal border. It is anterolateral to the brachiocephalic trunk and plaques and flow dynamics, permitting assessment of the risk of plaque right vagus nerve; the right pleura, phrenic nerve and internal thoracic rupture and thrombus formation. artery are initially posterosuperior, becoming lateral inferiorly (see Fig. 29.14). Its tributaries are the right vertebral, internal thoracic and infe- Subclavian arteries rior thyroid veins, and sometimes the first right posterior intercostal veins. Right subclavian artery Left brachiocephalic vein The right subclavian artery arises from the brachiocephalic trunk, origi- nating posterior to the upper border of the right sternoclavicular joint The left brachiocephalic vein is about 6 cm long, over twice the length (see Fig. 51.2). It ascends superomedial to the clavicle and posterior to of the right. It arises posterior to the sternal end of the left clavicle, scalenus anterior, then descends laterally to the outer border of the first anterior to the cervical pleura, and descends obliquely to the right, rib, where it becomes the axillary artery. posterior to the superior half of the manubrium sterni, reaching the sternal end of the first right costal cartilage where it joins the right Left subclavian artery brachiocephalic vein to form the superior vena cava (see Fig. 29.14). It is separated from the left sternoclavicular joint and manubrium by In the majority of individuals, the left subclavian artery originates inde- sternohyoid and sternothyroid, the thymus or its remnants, and areolar pendently from the aortic arch after the origins of the brachiocephalic tissue; terminally, it is overlapped by the right pleura. It crosses anterior and left common carotid arteries (see Fig. 57.4). It rises into the neck to the left internal thoracic, subclavian, brachiocephalic and common lateral to the medial border of scalenus anterior, crosses posterior to carotid arteries, left phrenic and vagus nerves, and the trachea. The this muscle and then descends towards the outer border of the first rib, aortic arch is inferior to it. Its tributaries are the left vertebral, internal where it becomes the left axillary artery. A common origin occasionally thoracic, inferior thyroid and superior intercostal veins, and sometimes exists between the left subclavian and vertebral arteries. Rarely, there are the first left posterior intercostal, thymic and pericardial veins. bilateral brachiocephalic trunks, which subsequently divide on both In children, the length and diameter of the left brachiocephalic vein sides into common carotid and subclavian arteries. are closely related to height; the diameter reaches adult dimensions at Relations In the thorax, the left subclavian artery is related anteri- the age of 10 years (Figs 58.9–58.10) (Sanjeev and Karpawich 2006). orly to the left common carotid artery and left brachiocephalic vein, Superior vena cava from which it is separated by the left vagus, cardiac and phrenic nerves. More superficially, the anterior pulmonary margin, pleura, sternothyroid and sternohyoid lie between the vessel and the upper The superior vena cava returns blood to the heart from the tissues above left area of the manubrium of the sternum. On the left side of the the diaphragm. It is approximately 7 cm in length, and is formed by the oesophagus, the thoracic duct and longus colli are posterior. The left junction of the brachiocephalic veins posterior to the lower border of subclavian artery is in contact posterolaterally with the left lung and the first right costal cartilage. It descends vertically, posterior to the first pleura. The trachea, left recurrent laryngeal nerve, oesophagus and and second intercostal spaces, and drains into the upper right atrium thoracic duct are medial. Laterally, the artery grooves the mediastinal posterior to the third right costal cartilage. Its inferior half is within the surface of the left lung and pleura, which also encroach on its anterior fibrous pericardium, which it pierces level with the second costal carti- and posterior aspects. lage. Covered anterolaterally by serous pericardium (from which a ret- rocaval recess projects), it is slightly convex to the right (see Figs 57.3, 57.4A,B, 57.12, 29.14). The superior vena cava is valveless. In children, Common carotid arteries the length and diameter of the superior vena cava are also closely related to height; the diameter reaches adult dimensions at the age of 10 years The right and left common carotid arteries differ in their length and (see Figs 58.9–58.10) (Sanjeev and Karpawich 2006). origin. The right is exclusively cervical and arises from the brachio- cephalic trunk posterior to the right sternoclavicular joint. The left Relations The anterior margins of the right lung and pleura are ante- originates directly from the aortic arch immediately posterolateral to rior and the pericardium intervenes below; these structures separate the the brachiocephalic trunk and therefore has both thoracic and cervical superior vena cava from the right internal thoracic artery, first and parts. second intercostal spaces, and second and third costal cartilages. The trachea and right vagus nerve are posteromedial, the right lung and Right common carotid artery pleura are posterolateral, and the right pulmonary hilum is posterior. The right common carotid artery and its relations are described in The right phrenic nerve and pleura are immediate right lateral relations Chapter 29. and the brachiocephalic trunk and ascending aorta lie to the left, the aorta overlapping the superior vena cava (see Fig. 55.7). Left common carotid artery The left common carotid artery (see Figs 57.4, 29.7) ascends until level Tributaries Tributaries of the superior vena cava are the azygos vein with the left sternoclavicular joint, where it enters the neck. Its thoracic and small veins from the pericardium and other mediastinal structures portion is 20–25 mm long and it lies first anterior to the trachea, then (see Fig. 56.7A). inclines to the left. The further course of the artery is described in Chapter 29. Superior vena cava obstruction Superior vena cava obstruction is characterized by headaches, facial and neck venous congestion, and Relations Sternohyoid and sternothyroid, the anterior parts of the left oedema, reflecting impaired venous drainage of the head, neck and pleura and lung, the left brachiocephalic vein and the thymic remnants arms, and of the collateral circulation, resulting in chest wall telangiecta- are anterior and separate the left common carotid artery from the sia. Several of the symptoms may subside with recumbency, or may be manubrium. The trachea, left subclavian artery, left border of the aggravated by standing up. The obstruction may be either partial or oesophagus, left recurrent laryngeal nerve and thoracic duct are poste- complete, and may occur suddenly or gradually. It is usually caused by rior. To the right are the brachiocephalic trunk (inferior) and the mediastinally invasive right upper lobe primary bronchogenic carci- trachea, inferior thyroid veins and thymic remains (superior). To the noma or by metastatic involvement of the right paratracheal lymph left are the left vagus and phrenic nerves, left pleura and lung. nodes.
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Great vessels 1027.e1 85 RETPAHC A B C D Fig. 58.9 Sites of measurement of the left brachiocephalic (innominate) vein and superior vena cava at angiography. Key: A, distal brachiocephalic vein; B, mid-brachiocephalic vein; C, brachiocephalic– superior vena cava junction; D, mid-superior vena cava. (Redrawn with permission from Sanjeev S, Karpawich PP. Superior vena cava and innominate vein dimensions in growing children: an aid for interventional devices and transvenous leads. Pediatr Cardiol. 2006 Jul–Aug;27(4):414–9.) 18 16 14 12 10 Fig. 58.10 Diameters of the distal brachiocephalic (innominate) vein (dis-INN), mid-brachiocephalic vein (mid-INN), brachiocephalic–superior vena cava junction (INN-SVC) and mid-superior vena cava (mid-SVC) in children of varying ages. (Redrawn with permission from Sanjeev S, Karpawich PP. Superior vena cava and innominate vein dimensions in growing children: an aid for interventional devices and transvenous leads. Pediatr Cardiol. 2006 Jul–Aug;27(4):414–9.) )mm( sretemaiD <2 yr 3–4 yr 5–8 yr 8 8–9 yr 6 10–12 yr 4 2 0 Dis-INN Mid-INN INN-SVC Mid-SVC
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GREAT vEssEls 1028 7 NOITCEs Haemorrhagic intrathoracic goitre, mediastinitis (either benign, malig- and central area of the central tendon of the diaphragm at the level of nant or fibrous), mediastinal haematoma, constrictive pericarditis, the eighth and ninth thoracic vertebrae, and drains into the inferopos- mediastinal cyst, thrombosis of the superior vena cava and sarcoidosis terior part of the right atrium (see Fig. 55.1, 57.4B). The thoracic part are less common aetiologies. Radiographic findings might include wid- is very short, and is partly inside and partly outside the pericardial sac. ening of the upper mediastinum on the frontal film or obliteration of The extrapericardial part is separated from the right pleura and lung by the retrosternal space on the lateral film. Other correlative findings may the right phrenic nerve, and the intrapericardial part is covered, except include pulmonary or mediastinal masses, lymphadenopathy, enlarged posteriorly, by inflected serous pericardium. The abdominal course of or obliterated azygos venous system, pleural effusion or rib notching. the inferior vena cava is described in Chapter 62. This is usually considered to be an oncological emergency and symp- toms are often completely and promptly relieved by insertion of a Collateral venous channels In obstruction of the upper inferior vascular stent via the common femoral vein or by radiotherapy to the vena cava, the azygos and hemiazygos veins and vertebral venous plex- affected region after a tissue diagnosis is established. uses are the main collateral channels that maintain venous circulation. They connect the superior and inferior venae cavae and communicate Variations of the brachiocephalic veins and superior with the common iliac vein by the ascending lumbar veins and with vena cava many tributaries of the inferior vena cava. Available with the Gray’s Anatomy e-book Variations Broadly speaking, the inferior vena cava may be congeni- tally interrupted, duplicated, left-sided or even absent. Inferior vena cava The inferior vena cava returns blood to the heart from infradiaphrag- matic tissues. It passes through the diaphragm between the right leaf Bonus e-book images Fig. 58.1 A case of a left anterior trunk and a retrotracheal right subclavian Fig. 58.9 Sites of measurement of the left interventricular artery arising from the artery, also known as a lusoria artery. brachiocephalic (innominate) vein and pulmonary trunk. superior vena cava at angiography. Fig. 58.6 A cardiac magnetic resonance Fig. 58.2 Bland–White–Garland syndrome in angiograph showing three-dimensional Fig. 58.10 Diameters of the distal a 29-year-old woman. reconstruction of a native aortic coarctation brachiocephalic (innominate) vein mid- in an adult with extensive collateral flow. brachiocephalic vein, brachiocephalic– Fig. 58.4 A PA chest radiograph, superior vena cava junction and anteroposterior view, showing the classic Fig. 58.7 The collateral circulation at MR mid-superior vena cava in children of ‘aortic nipple’ in a patient with angiography and phase-contrast velocity- varying ages. pneumomediastinum. encoded cine MR imaging. Fig. 58.5 A dissection showing a left aortic Fig. 58.8 A Stanford type A aortic arch that gives rise to a common vertebral dissection.
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Great vessels 1028.e1 85 RETPAHC The brachiocephalic veins may enter the right atrium separately, the Embryologically, if the right subcardinal vein fails to anastomose right vein descending like a normal superior vena cava. During embryo- with the hepatic sinusoids, the hepatic segment of the inferior vena cava logical development, if the cardinal vein does not become obliterated, fails to develop. When this occurs, the hemiazygos or azygos veins, it will persist as a left-sided superior vena cava. A left superior vena cava which both originate from the cranial supracardinal veins, return blood may have a slender connection with the right and then cross the left to the heart. Azygos continuation of the inferior vena cava, character- side of the aortic arch to pass anterior to the left pulmonary hilum ized by a prominent azygos vein, is an entity of which the paediatric before turning to enter the right atrium. It replaces the oblique vein of surgeon should be aware when undertaking repair of oesophageal the left atrium and coronary sinus, and receives all the tributaries of atresia and tracheo-oesophageal atresia in neonates. The azygos vein, the coronary sinus. The left brachiocephalic vein sometimes projects which is commonly ligated and divided during this procedure, should above the manubrium (more frequently in childhood), and crosses the be spared because ligation of this vessel in neonates with azygos con- suprasternal fossa in front of the trachea. A left-sided superior vena cava tinuation of the inferior vena cava leads to intraoperative circulatory may cause difficulties when placing a cardiac catheter, pacing or defibril- collapse and death. Double inferior vena cava (right side usually domi- lating electrodes because the angle between the left superior vena cava nant) is a result of the persistence of all or any segments of the subcar- and the left subclavian vein is much more acute than that between the dinal veins. One of the most common variations is a left-sided inferior subclavian and a normal left brachiocephalic vein. Its calibre may also vena cava, which is formed if the right supracardinal vein regresses and be smaller than that of the right. Even if insertion of a catheter into a the left supracardinal vein persists. There may also be a duplication of left superior vena cava is possible, the angle at which the catheter enters the inferior vena cava, which typically occurs below the renal veins, and the right atrium causes difficulty when attempting to place it into the is the result of persistence of the left lumbar and thoracic supracardinal right ventricle and pulmonary trunk; this generally leaves the catheter veins and left suprasubcardinal anastomosis as well as malformation of tip against the coronary sinus, making it difficult to obtain blood right subcardinal–hepatic anastomosis. Abnormalities associated with samples. In the majority of persistent left superior venae cavae, blood duplication of the inferior vena cava include: congenital heart disease, drains into the right atrium via the coronary sinus. When this does not congenital absence of the right kidney, cloacal extrophy, renal ectopia happen, the coronary sinus is absent, and the persistent left superior with abdominal aneurysm, right retrocaval ureter, left retrocaval ureter vena cava drains directly into the atrium. Cyanosis reflects a persistent and congenital absence of the iliac anastomosis, abnormal left arm right-to-left shunt and affected individuals have a higher risk for para- drainage and transcaval ureter. doxical embolism. Radiographically, there is a paramediastinal bulge In situs inversus with dextrocardia, the inferior vena cava passes before the aortic arch. Electrocardiograms show a left P-wave axis. Diag- inferiorly along the left side instead of the right (as opposed to situs nosis can be confirmed by cardiac catheterization and angiography. inversus with levocardia, in which the inferior vena cava remains on Persistent left superior vena cava may be associated with extracardiac the right side). In situs ambiguus, otherwise known as heterotaxy, the conditions such as VACTERL association (vertebral defects, anal atresia, major organs are arranged ambiguously within the body. Prominent cardiac malformations, tracheo-oesophageal fistula with oesophageal azygos veins with interrupted inferior vena cava are associated with atresia, radial and renal dysplasia, and limb anomalies); trisomy 21; heterotaxy (Punn and Olson 2010). Situs ambiguus with polysplenia is 22q11; CHARGE association (coloboma, heart defects, choanal atresia, associated with an absence of portions of the inferior vena cava on the mental retardation, genital and ear anomalies); and 45 XO karyotype right side (with continuation through the azygos or hemiazygos vein), (Turner’s syndrome). transposition of the inferior vena cava to the left side, or duplication of If the superior vena cava is duplicated, the right superior vena cava the inferior vena cava with one on the right and one on the left. Situs may drain into the right atrium and the left superior vena cava into the inversus with asplenia is similar to that of polysplenia, in that the infe- left atrium. Although double superior vena cava is largely asympto- rior vena cava may be absent with azygos continuation or with the matic, it is usually (along with a sole left-sided superior vena cava) inferior vena cava to the left of the midline. In situs inversus totalis, associated with congenital cardiac anomalies, such as pulmonary steno- transposition of the inferior vena cava consists of a right-sided inferior sis, coarctation of the aorta, tetralogy of Fallot and atrial septal defects. vena cava. The inferior vena cava may have an abnormally high inser- tion into the right atrium. Congenital agenesis of the inferior vena cava may occur and may be completely asymptomatic because venous drain- age of the lower limbs occurs through anastomosed channels of the azygos and hemiazygos veins. That said, this condition may be associ- ated with a higher risk for deep vein thrombosis.
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GREAT vEssEls 1028.e2 7 NOITCEs REFERENCES Baliga RR, Neinaber CA, Isselbacher EM et al 2007 Aortic Dissection and Norton JA, Barie PS, Bollinger RR et al 2008 Surgery: Basic Science and Related Syndromes. Ann Arbor, MI: Springer. Clinical Evidence (2nd ed). New York: Springer. Berdjas D, Turina MI 2011 Operative Anatomy of the Heart. Berlin: Springer. Osborn AG 1998 Diagnostic Cerebral Angiography. Philadelphia: Lippin- Bergman RA, Thompson SA, Afifi AK et al 1988 Compendium of Human cott, Williams & Wilkins. Anatomic Variation. Baltimore: Urban & Schwarzenberg. Punn R, Olson I 2010 Anomalies associated with a prominent azygos vein Deutsch J, Savides TJ 2005 Normal Thoracic Anatomy in Digital Human on echocardiography in the pediatric population. J Am Soc Echocardi- Anatomy and Endoscopic Ultrasonography. Hamilton, ON: BC Decker. ogr 23:282–5. Kaiser T, Kellenberger CJ, Albisetti M et al 2008 Normal values for aortic Sanjeev S, Karpawich PP 2006 Superior vena cava and innominate vein diameters in children and adolescents–assessment in vivo by contrast- dimensions in growing children: an aid for interventional devices and enhanced CMR-angiography. J Cardiovasc Magn Reson 10:56. transvenous leads. Pediatr Cardiol 27:414–19. Kervancioglu P, Kervancioglu M, Tuncer CM 2006 Echocardiographic study Smith A, McKay R 2004 A Practical Atlas of Congenital Heart Disease. of aortic root diameter in healthy children. Saudi Med J 27:27–30. London: Springer. Loukas M, Groat C, Khangura R et al 2009 The normal and abnormal anatomy of the coronary arteries. Clin Anat 22:114–28.
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COMMENTARY Technical aspects and applications of 7.1 diagnostic radiology Jonathan D Spratt Magnetic resonance imaging tions for the treatment of reperfusion injury and research into the physiology of solid tumours and angiogenesis. There is every reason to believe that continued efforts to push the envelope of high-field- Magnetic resonance imaging (MRI) produces images by first magnet- strength applications will open new vistas in what appears to be a izing a patient in the bore of a powerful magnet and then broadcasting never-ending array of potential clinical applications. short pulses of radiofrequency (RF) energy at 46.3 MHz that resonate T1 weighted images best accentuate fat and other soft tissues, mobile protons (hydrogen nuclei) in the fat, protein and water of the whereas fluid is low-signal; these images are nicknamed the ‘anatomy patient’s soft tissues and bone marrow. The protons produce RF echoes weighting’ amongst radiologists who publish or teach anatomy. T2 when their resonant energy is released; their density and location can weighted images reveal fluid as high signal as well as fat. Fat suppression be exactly correlated into an image matrix by complex mathematical sequences using T2 ‘fat sat’ (T2FS) or short tau inversion recovery (STIR) algorithms. are very sensitive in highlighting the soft tissue or bone marrow oedema The spinning proton of the hydrogen nucleus acts like a tiny bar that almost invariably accompanies pathological states such as inflam- magnet, aligning either with or against the magnetic field, and produc- mation or tumours. Contrast-enhanced images with gadolinium, when ing a small net magnetic vector. RF energy from various types of coil, used with T1 fat saturation (T1FS) sequences, also exquisitely highlight either built into the scanner or attached to specific body parts, generates hypervascularity, particularly that associated with tumours and inflam- a second magnetic field perpendicular to the static magnetic field that mation, especially in pathologies where the blood–brain barrier is com- rotates or ‘flips’ the protons away from the static magnetic field. When promised. Metallic artefact reduction sequences (MARS) are superior in the RF pulse is switched off, the protons flip back (relax) to their origi- imaging periprosthetic soft tissues after joint replacement or other nal position of equilibrium, emitting the RF energy they had acquired orthopaedic metalwork implantation. into the antenna around the patient. This information is then ampli- fied, digitized and spatially encoded by the array processor. MR tractography MRI systems are graded according to the strength of the magnetic field they produce. Routine high-field systems are those capable of producing a magnetic field strength of 3–7 T (Tesla), using a supercon- MRT is a three-dimensional modelling technique used to represent ducting electromagnet immersed in liquid helium. Open magnets for neural tracts visually using data collected by DTI or, more recently, by claustrophobic patients and limb scanners use permanent magnets of HARDI, with results presented in two- and three-dimensional images 0.2–0.75 T. For comparison, Earth’s magnetic field varies from 30 to (Nucifora et al 2007). 60 µT. MRI does not present any recognized biological hazard. Patients In addition to the long tracts that connect the brain to the rest of who have any form of pacemaker or implanted electro-inductive device, the body, there are complicated neural networks formed by short con- ferromagnetic intracranial aneurysm clips, certain types of cardiac valve nections among different cortical and subcortical regions, their exist- replacement or intraocular metallic foreign bodies must never be exam- ence revealed by histochemistry and postmortem biological techniques. ined because there is a high risk of death or blindness. Many extracra- Central nervous system tracts are not identifiable by direct examination, nial vascular clips and orthopaedic prostheses are now ‘MRI-friendly’ CT or conventional MRI scans, explaining the paucity of their descrip- but may cause local artefacts; newer sequences exist to reduce artefact. tion in neuroanatomy atlases and the poor understanding of their Loose metal items, ‘MR-unfriendly’ anaesthetic equipment and credit functions. cards must be excluded from the examination room. Pillows contain- The MRI sequences used look at the symmetry of water diffusion in ing metallic coiled springs have been known nearly to suffocate the brain. Bundles of fibre tracts make the water diffuse asymmetrically patients, and heavy floor buffing equipment has been found wedged in a ‘tensor’, the major axis parallel to the direction of the fibres. There in the magnet bore because domestic staff had been suboptimally is a direct relationship between the number of fibres and the degree of informed. anisotropy. DTI assumes that the direction of least restriction corre- New methods of analysing normal and pathological brain anatomy sponds to the direction of white matter tracts. Diffusion MRI was intro- are now at the forefront of research. These are MR spectroscopy (MRS); duced in 1985. In the more recent evolution of the technique into functional MRI (fMRI); diffusion tensor imaging (DTI); high angular diffusion tensor MRI (DTI), the relative mobility of the water molecules resolution diffusion imaging (HARDI) for MR tractography (MRT, see from the origin is modelled as an ellipsoid rather than a sphere. This below); and molecular MRI (mMRI), which has taken on a new direc- allows full characterization of molecular diffusion in the three dimen- tion since the description of the human genome. sions of space and the formation of tractograms. Barriers cause uneven MRS assesses function within the living brain. It capitalizes on the anisotropic diffusion. In white matter, the principal barrier is the myelin fact that protons residing in differing chemical environments possess sheath, whereas bundles of axons provide a barrier to perpendicular slightly different resonant properties (chemical shift). For a given diffusion and a path for parallel diffusion along the orientation of the volume of brain, the distribution of these proton resonances can be fibres. Anisotropic diffusion is expected to be increased overall in areas displayed as a spectrum. Discernible peaks can be seen for certain neu- of high mature axonal order. Conditions where barriers offered by the rotransmitters: N-acetylaspartate varies in multiple sclerosis, stroke and myelin sheaths or the axons are disrupted, e.g. in trauma, tumours and schizophrenia while choline and lactate levels have been used to evalu- inflammation, reduce anisotropy and yield DTI data used to seed ate certain brain tumours. various tractographic assessments of the brain (p. 391). Data sets may fMRI depends on the fact that haemoglobin is diamagnetic when be rotated continuously into various planes in order to appreciate the oxygenated but paramagnetic when deoxygenated. These different structure better; colour may be assigned based on the dominant direc- signals can be weighted to the smaller vessels, and hence closer to the tion of the fibres. A leading clinical application of MRT is in the active neurones, by using larger magnetic fields. mMRI uses biomarkers presurgical mapping of eloquent regions. Intraoperative electrical stim- that interact chemically with their surroundings and alter the image ulation (IES) provides a clinical gold standard for the existence of according to molecular changes occurring within the area of interest, functional motor pathways that can be used to determine the accuracy potentially enabling early detection and treatment of disease and basic and sensitivity of fibre-tracking algorithms. pharmaceutical development and quantitative testing. Intersecting tracts or partial volume averaging of adjacent pathways High-field-strength magnets give significant improvement in spatial with different fibre orientations are the reasons why DTI does not accu- resolution and contrast. MR images of the microvasculature of the live rately describe the microstructure in complex white matter voxels that human brain that allow close comparison with the detail seen in his- contain more than one fibre population, e.g. in the centrum semiovale, tological slides have been acquired at 8 T. This has significant implica- where major white matter tracts such as the pyramidal tract, the e67
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Technical aspecTs and applicaTions of diagnosTic radiology e68 7 noiTces superior longitudinal fasciculus and the corpus callosum intersect. This radiation dose to the target organ. For example, 99mtechnetium or has hindered preoperative mapping of the pyramidal tract in brain 123iodine may be used to detect thyroid disease, but certain thyroid tumour patients. HARDI permits more accurate delineation of pathways diseases or thyroid cancer may be treated solely or in part with 131iodine. within complex regions of white matter. The q-ball reconstruction of The difference in the agent used depends on the type and energy levels HARDI data provides an orientation distribution function (ODF) that of the radiation particle that the radioisotope emits. can be used to determine the orientations of multiple fibre populations Radionuclides used in nuclear medicine are often chemically bound contributing to a voxel’s diffusion MR signal, mapping fibre trajectories to a complex called a tracer. The way the body handles a tracer may through regions of complex tissue architecture in a clinically feasible differ in disease or pathological processes. For example, the tracer used timeframe. in bone imaging is methylene-diphosphonate (MDP) bound to 99mtech- netium. MDP attaches to hydroxyapatite in bone; altered bone physiol- ogy, such as occurs in a fracture, metastatic bone disease or arthritic Ultrasound change, produces an increase in biochemical bone activity and an accu- mulation of MDP that is seen as a focal ‘hot spot’ of the radiopharma- Uniquely, ultrasound images do not depend on the use of electromag- ceutical on a bone scan. netic wave forms. The properties of high-frequency sound waves (lon- 99mTechnetium is the major workhorse radioisotope of nuclear medi- gitudinal waves) and their interaction with biological tissues are cine. It can be eluted from a molybdenum/technetium generator stored responsible for the production of ‘echograms’ (Desser and Jeffrey 2001). within a nuclear medicine department, allowing for easy access. It has a A sound wave of appropriate frequency (diagnostic range 3.5–20 MHz) short half-life (6 hours), which allows for ease of medical imaging is produced by piezo-electric principles. Image production is deter- and disposal. Its pharmacological properties allow it to be easily bound mined by attenuation and reflection as the beam passes through tissues. to various tracers and it emits gamma rays that are of suitable energy Attenuation is caused by the loss of energy due to absorption, reflection for medical imaging. In addition to 99mtechnetium, the most com- and refraction in soft tissues, resulting in a reduction in signal intensity. mon intravenous radionuclides used in nuclear medicine are 123iodine Reflection of sound waves within the range of the receiver produces the and 131iodine, 201thallium, 67gallium, 18fluorodeoxyglucose (FDG) and image, and the echotexture is dependent on tiny differences in acoustic 111indium-labelled leukocytes. The most common gaseous/aerosol radio- impedance between different tissues. Blood flow and velocity can be nuclides used are 133xenon, 81mkrypton, 99mtechnetium (Technegas) and measured (using the Doppler principle) in duplex mode. 99mtechnetium diethylene triamine pentaacetic acid (DTPA). Techniques such as harmonic imaging and the use of ultrasound The images obtained from nuclear medicine imaging can be single contrast agents (stabilized microbubbles) have enabled non-invasive or multiple. Image sets may be represented by time sequence imaging determination of myocardial perfusion. These contrast agents also (e.g. cine), such as dynamic imaging or cardiac gated sequences, or by clearly improve the detection of metastases in the liver and spleen. spatial sequence imaging, where the gamma camera is moved relative Ultrasound is the most common medical imaging technique for pro- to the patient, e.g. in SPECT imaging. Spatial sequence imaging allows ducing elastograms, in which stiffness or strain images of soft tissue are the images to be presented as a slice-stack much in the way that CT or used to detect or classify tumours. Cancer is 5–28 times stiffer than the MRI images are displayed. It may also be fused with concomitant CT background of normal soft tissue; when a mechanical compression or or MRI to provide combined physiological and anatomical imaging. vibration is applied, a tumour deforms less than the surrounding tissue. A PET scan is a specialized type of nuclear medicine imaging that Elastography may be used, for example, to measure the stiffness of the measures important body functions, such as blood flow, oxygen use or liver in vivo or in the detection of breast or thyroid tumours. A correla- glucose metabolism. It involves short-lived radioactive tracer isotopes tion between liver elasticity and the cirrhosis score has been shown (Yeh that emit positrons (positively charged subatomic particles with the et al 2002, Foucher et al 2006). same mass and magnitude of charge as electrons). The radioisotopes Interpretation of anatomy and pathology from static ultrasound are chemically incorporated into biologically active molecules: most images is more difficult than that from other imaging modalities: commonly, the sugar FDG (2-deoxy-2-[fluorine-18]fluoro-D-glucose). compare the real-time nature ultrasound in Video 14.1 with the static An hour after injection, FDG becomes concentrated into the tissues of images in Fig 14.4. The technique is highly operator-dependent and interest; images are obtained as the isotope undergoes positron emis- provides unique information on tissue structure and form not obtained sion decay. A positron travels only a few millimetres before reacting from other imaging techniques. with an electron by annihilation, producing a pair of gamma photons that move in opposite directions. The PET scan detectors process only those photon pairs that are detected simultaneously (coincident detec- Nuclear medicine tion) to create an image of tissue activity with respect to that particular isotope. These images may subsequently be fused with CT or MR Historically, the field of nuclear medicine began in 1946 when images. The short half-life of the isotopes limits PET imaging; close radio active iodine was administered as an ‘atomic cocktail’ to treat access to a cyclotron for generation of the isotopes plays an important thyroid cancer. Since that time, nuclear medicine has advanced to the role in the feasible location of a PET scanner. Typical isotopes used in point where it was recognized in the early 1970s as a diagnostic sub- medical imaging and their half-lives are: 11carbon (about 20 min), specialty. 13nitrogen (about 10 min), 13oxygen (about 2 min) and 18fluorine Unlike diagnostic radiology, where an image is created by passing (about 110 min). energy through the body from an external source, nuclear medicine creates an image by measuring the radiation emitted from tracers taken Angiography/interventional radiology internally. Overall, the radiation dosages are comparable with CT and vary depending on the examination. Nuclear medicine also differs from most other imaging modalities in that the tests demonstrate the physio- Angiographic imaging was first described in 1927, when Egas Moniz, a logical function of a specific area of the body. In some instances, this physician and neurologist, introduced contrast X-ray cerebral angiogra- physiological information may be fused with the more anatomical phy. (Moniz was awarded the Nobel Prize for his work in 1949.) In imaging of CT or MRI, combining the strengths of anatomy and func- 1953, the field was revolutionized by the Seldinger technique, in which tion for diagnosis. no sharp needles remained inside the vascular lumen during imaging. Nuclear medicine uses pharmaceuticals that have been labelled with Although angiography initially involved X-ray and fluoroscopic imaging a radionuclide (radiopharmaceuticals) and which are administered to of blood vessels and organs of the body after injecting radiopaque patients by intravenous injection, ingestion or inhalation (the method contrast agents into the blood stream, it has evolved to encompass so of administration depends on the type of examination and the organ much more. Many of the procedures currently performed by angiogra- or organ process to be imaged). Emitted radiation is detected and phy may be diagnostic; following the advent of minimally invasive imaged with specialized equipment such as gamma cameras, positron procedures performed with image guidance, the name of the discipline emission tomography (PET) or single photon emission computed changed to interventional radiology (or vascular and interventional tomography (SPECT). Radiation may be measured from parts of the radiology). body by the use of probes, or samples may be taken from patients and Angiograms are typically performed by gaining access to the blood measured in counters. vessels, through either the femoral artery, femoral vein or jugular vein, Radiopharmaceuticals may be used to image a disease process or to depending on the area of interest to be imaged (e.g. cerebral, coronary treat diseases. Those used for imaging emit a gamma ray (γ) and those or pulmonary angiograms). Following vascular access, catheters are used for treatment emit a beta (β) particle. Gamma rays are of higher directed to the specific location to be imaged by the use of guidewires, energy in order to pass through the body and be detected by a detection and contrast agents are injected through these catheters to visualize the camera, whereas β particles travel only short distances and emit their vessels or the organ with X-ray imaging. Imaging of the arterial and
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Technical aspects and applications of diagnostic radiology e69 1.7 yraTneMMoc venous circulation of the arms and legs may demonstrate peripheral attenuation coefficient of all the tissues in the path of the X-ray beam vascular disease. form the image. CT obtains a series of different angular X-ray projec- Treatment and/or interventions can often be performed through tions that are processed by a computer to give a section of specified similar catheter-based examinations. Such procedures might involve thickness. The CT image comprises a regular matrix of picture elements angioplasties, where a balloon mechanism is placed across an area of (pixels). All of the tissues contained within the pixel attenuate the X-ray narrowing (stenosis) in a vessel or lumen. With controlled inflation of projections and result in a mean attenuation value for the pixel. This the balloon, the area of narrowing can be widened. value is compared with the attenuation value of water and is displayed Imaging in diagnostic or interventional procedures may produce still on a scale (the Hounsfield scale). Water is said to have an attenuation or motion (cine) images. The technique often used, digital subtraction of 0 Hounsfield units (HU); air typically has an HU number of −1000; angiography (DSA), involves taking images at 2–30 frames per second fat is approximately −100 HU; soft tissues are in the range +20 to to allow imaging of the flow of blood through vessels. A preliminary +70 HU; and bone is usually greater than +400 HU. image of the area is taken before the contrast is injected; this ‘mask’ Modern multislice helical CT scanners can obtain images in sub- image is then electronically subtracted from all subsequent images, second times, and imaging of the whole body from the top of the head leaving only the vessels filled with contrast. For optimal subtraction, to the thighs can take as little as a single breath-hold of only a few the patient must remain motionless. seconds. The fast scan times allow dynamic imaging of arteries and Angiograms of the heart may be performed to visualize the size and veins at different times after the injection of intravenous contrast agents. contractility of the chambers and the anatomy of the coronary vessels. The continuous acquisition of data from a helical CT scanner allows The thorax may also be studied to evaluate the pulmonary arteries and reconstruction of an image in any plane (multiplane reconstruction, veins for vascular malformations, blood clots and possible origins of MPR), commonly sagittal and coronal, as may be seen in many of the haemoptysis. In the investigation of atherosclerotic disease, vascular images throughout this forty-first edition of Gray’s Anatomy. This malformations or tumoral vascularization, the neck is often imaged in orthogonal imaging greatly improves the understanding of the three- order to visualize the vessels that supply the brain in their entirety, from dimensional aspects of radiological anatomy and now forms part of the the points at which they arise from the aortic arch to their termination standard practice of assessing disease. as cerebral vessels. Renal artery imaging may elucidate the cause of No specific preparation is required for most CT examinations of the hypertension in selected patients, and imaging of the mesenteric vessels brain, spine or musculoskeletal system. Studies of the chest, abdomen may identify the origin of gastrointestinal bleeding or mesenteric and pelvis, and those of the brain with complex histories, usually angina. require intravenous contrast medium that contains iodine because this In addition to angiograms and venograms, the field of interventional defines vascular relationships and differentiates normal and pathologi- radiology also includes such procedures as coil embolization of aneu- cal soft tissues more effectively. Opacification of the bowel in CT studies rysms and vascular malformations; balloon angioplasty and stent place- of the abdomen and pelvis may be accomplished by oral ingestion of ment; chemoembolization directly into tumours; drainage catheter a water-soluble contrast medium from 24 hours prior to the examina- insertion; embolization (e.g. uterine artery for treatment of fibroids); tion, in order to outline the colon, combined with further oral intake thrombolysis to dissolve blood clots; tissue biopsy (percutaneous or 0–60 minutes prior to the scan, in order to outline the stomach and transvascular); radiofrequency ablation and cryoablation of tumours; small bowel. This procedure is much less frequently performed with the line insertions for specialized vascular access; inferior vena cava filter latest generation of scanners, which exquisitely differentiate various placements; vertebroplasty; nephrostomy placement; gastrostomy tube enhancing layers within the bowel wall. Occasionally, direct insertion placement for feeding; dialysis access; transjugular intrahepatic porto- of rectal contrast to show the distal large bowel may be required. systemic shunt (TIPS) placement; biliary interventions; and, most Generally, all studies are performed with the patient supine and recently, endovenous laser ablation of varicose veins. images are obtained in the transverse or axial plane. Modern CT scan- ners allow up to 25° of gantry angulation, which is particularly valuable in spinal imaging. Occasionally, direct coronal images are obtained in Computed tomography the investigation of cranial and maxillofacial abnormalities; in these cases, the patient lies prone with the neck extended and the gantry The limitation of all plain radiographic techniques is the two- appropriately angled, but this technique has largely been superseded dimensional representation of three-dimensional structures; the linear by the orthogonal imaging described above. REFERENCES Desser TS, Jeffrey RB 2001 Tissue harmonic imaging techniques: physical Nucifora PG, Verma R, Lee SK et al 2007 Diffusion-tensor MR imaging and principles and clinical applications. Semin Ultrasound CT MR 22: tractography: exploring brain microstructure and connectivity. Radiol- 1–10. ogy 245:367–84. Foucher J, Chanteloup E, Vergniol J et al 2006 Diagnosis of cirrhosis by Yeh WC, Li PC, Jeng YM et al 2002 Elastic modulus measurements of human transient elastography (FibroScan): a prospective study. Gut 55:403–8. liver and correlation with pathology. Ultrasound Med Biol 28:467–74.
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COMMENTARY 7.2 Endobronchial ultrasound Natalie M Cummings History tively, compared to 69% and 88% for EBUS­TBNA alone. A more recent study of 44 patients, where the same operator performed EBUS­TBNA and then EUS­FNA by inserting the EBUS bronchoscope into the It is more than 35 years since the first description of blind transbron­ oesophagus, found that the sensitivity, specificity and accuracy of chial needle aspiration (TBNA) biopsies of paratracheal masses was mediastinal lymph node staging using combined EBUS/EUS­FNA were published (Wang et al 1978). Prior to this, surgery had been the only all 100%, compared to 79%, 100% and 84%, respectively, for EBUS way to obtain tissue from mediastinal masses or lymph nodes. TBNA alone (Lee et al 2014). The ASTER trial randomized 241 patients to is less invasive than surgery but the blind nature of the technique dict­ either combined EBUS/EUS­FNA or conventional surgical staging ates that sampling only bulky masses or nodal tissue results in an (Annema et al 2010). Where endoscopic staging showed no evidence of acceptable yield. In the early 1990s, the first report of the new technique locally advanced disease, the patient underwent surgical staging (n = 65). of ‘endobronchial sonography’ appeared (Hürter and Hanrath 1992). Sensitivity was significantly greater for combined surgical/endoscopic A small ultrasound catheter was passed through the working channel staging (94% versus 79%, P = 0.02) with similar NPVs (93% versus 86%, of a bronchoscope, giving a 360° (radial) ultrasound image. Biopsies P = 0.18) and complication rates. A head­to­head study of EBUS­TBNA could be taken by inserting standard biopsy forceps through a sheath versus the surgical approach of video­assisted mediastinoscopy (VAM) left in place to mark the correct position once the ultrasound catheter in 153 patients was published in 2011 (Yasufuku et al 2011). No signifi­ was removed. In 2003, the first report of a prototype bronchoscope, cant differences were found between the two procedures in determining incorporating a curved linear array electronic transducer at the end of the true pathological N­stage, although the authors admitted that the the bronchoscope, was published (Krasnik et al 2003). When the trans­ EBUS­TBNA yield may have been improved by the fact that the proce­ ducer was closely applied to the bronchial wall, ultrasound scanning of dures were all carried out under general anaesthetic by thoracic sur­ mediastinal structures (to a depth of 5 cm) was possible and a 22­gauge geons who were extremely familiar with mediastinal anatomy. At needle inserted through the biopsy channel and into the mass in ques­ present, the European Society of Thoracic Surgeons continue to recom­ tion was visible in real time. This meant that smaller lesions could be mend that patients with mediastinal lymphadenopathy on PET/CT and biopsied more accurately, with reduced potential for the wrong area negative endoscopic staging proceed to VAM because of the higher NPV to be sampled inadvertently. This new biopsy technique was termed (de Leyn et al 2014). However, mediastinoscopy can be avoided if endo­ endobronchial ultrasound (EBUS)­TBNA or fine needle aspiration scopic staging is positive. (EBUS­FNA). Technique Other uses Although the initial procedures took place under general anaesthetic, Although most commonly used in lung cancer investigation, EBUS is most EBUS procedures today take place under conscious sedation and increasingly employed to diagnose other causes of mediastinal lymph­ local anaesthetic. Using computed tomography (CT), with or without adenopathy and paramediastinal masses. Von Bartheld et al (2013) positron emission tomography (PET) scanning, the areas that require carried out a randomized controlled trial demonstrating that EBUS­ or sampling are identified. These lymph nodes or masses are then found EUS­FNA was superior to combined endobronchial and transbronchial during bronchoscopy using the ultrasound scanning probe. The infla­ biopsy (conventionally, the method of choice to obtain a tissue diag­ tion of a small water­filled balloon around the scanning probe can nosis in sarcoidosis) in the detection rate of non­caseating granulomas. improve contact with the bronchial wall, and thus image quality, Sensitivity for the diagnosis of Mycobacterium tuberculosis has been although in most cases it is not needed. A needle is inserted through reported at 85–94% (Sun et al 2013, Navani et al 2011), whilst for the working channel of the bronchoscope and suction applied, via a lymphoma it may be as high as 89% and even higher for relapsed rather syringe, at the proximal end of the needle. Under direct vision, the than de novo disease (Moonim et al 2013). Controversy remains about needle is passed several times through the lesion in order to obtain a whether the cytological sample obtained at EBUS can give sufficient cytological specimen. Suction is removed and the needle withdrawn information about lymphoma subtype compared to the larger samples from the bronchoscope. The specimen is either smeared on to slides obtained by core or surgical biopsies that have been traditionally and air­dried, or placed into pots containing liquid preservative for favoured. At present, the British Thoracic Society feels that there is insuf­ laboratory processing (Medford et al 2010). The power Doppler facility ficient evidence to justify the use of EBUS­TBNA in lymphoma diagno­ enables safer identification of vessels to avoid puncture of these sis (du Rand et al 2011) but this may change in the future as endoscopists structures. and cytopathologists become more skilled. Using EBUS, the diagnosis of metastatic extrathoracic malignancy (Ozgül et al 2013), chondrosar­ Diagnosis and staging of lung cancer coma (Wang et al 2014), malignant pleural mesothelioma (Lococo et al 2014), vertebral body tumour (Ojha et al 2014), pulmonary artery aneurysm (Lerner and Riker 2014), parathyroid adenoma (Buderi et al The main use of EBUS in today’s clinical practice is in the diagnosis and 2014) and various other benign pathologies have all been reported in staging of lung cancer. Surgical sampling of the mediastinum, whilst the literature. remaining the gold standard, has a number of limitations, including invasiveness and cost. In 2009, a new lymph node map was published Complications by the International Association for the Study of Lung Cancer (Rusch et al 2009). Using this as a guide, EBUS can access lymph node stations 2R, 2L, 3P, 4R, 4L, 7, 10R, 10L, 11R and 11L. When combined with A recent review of 190 studies published between 1995 and 2012, endoscopic ultrasound (EUS), where an endoscope fitted with a linear comprising 16,181 patients, found a serious adverse event rate of 0.05% ultrasound transducer is inserted into the oesophagus, additional sta­ for EBUS, increasing to 0.14% with the addition of figures for EUS (von tions 8 and 9 can be sampled, as well as the left suprarenal gland, the Bartheld et al 2014). Abscess formation, sepsis, pneumothorax and left lobe of the liver and the coeliac axis nodes, if necessary. Stations 5 other respiratory complications accounted for the EBUS adverse events, and 6 can only be accessed via a surgical approach. whereas EUS had higher rates of infectious complications (including Wallace et al (2008) showed, in 42 patients with malignant media­ mediastinitis), oesophageal perforation and haemorrhage. The results stinal lymphadenopathy, that the sensitivity and negative predictive of the AQuIRE registry, published in 2013, reported a 1.44% complica­ e70 value (NPV) of combined EBUS/EUS­FNA were 93% and 97%, respec­ tion rate in 1,317 patients undergoing EBUS, including pneumothorax,
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Endobronchial ultrasound e71 2.7 YRATNEMMOC bleeding, sustained hypoxia and respiratory failure (Eapen et al 2013); to yield greater amounts of tumour RNA when compared to the other it is unclear how many of these cases also feature in the figures of the methods (although this only reached significance when compared to aforementioned meta­analysis. Single case reports of needle breakage bronchoscopy). Certain genetic changes (particularly in the EGFR and (Ozgül et al 2014) and pneumomediastinum/pneumopericardium ALK genes) may determine the chemotherapy agent of choice; a further (Ortiz et al 2014) have also been published. However, the procedure is study has demonstrated that 52 of 55 samples obtained by EBUS­TBNA generally accepted to be safe. in patients with NSCLC contained sufficient material for fluorescent in situ hybridization (FISH) analysis for ALK rearrangement or amplifica­ The future tion (Neat et al 2013). Yarmus et al (2013) found that four needle passes (in conjunction with rapid on­site cytopathology evaluation) In this era of increasingly personalized medicine, it is important for any yielded adequate amounts of tissue for EGFR and KRAS mutation analy­ sampling technique to provide sufficient tissue for molecular analysis. sis on tumour DNA as well as ALK rearrangement testing by FISH In a recent study of 106 patients with non­small cell lung cancer (Yarmus et al 2013). (NSCLC), 101 samples taken at either standard bronchoscopy, EBUS­ The applications of EBUS continue to expand and with increased TBNA or CT­guided core biopsy were sufficient to yield RNA for further experience of both the operators and the cytopathologists examining molecular testing (Schmid­Bindert et al 2013). EBUS­TBNA was found the samples, the technique goes from strength to strength. REFERENCES Annema JT, van Meerbeeck JP, Rintoul RC et al 2010 Mediastinoscopy vs Ortiz R, Hayes M, Arias S et al 2014 Pneumomediastinum and pneumoperi­ endosonography for mediastinal nodal staging of lung cancer: a rand­ cardium after endobronchial ultrasound­guided transbronchial needle omized trial. JAMA 304:2245–52. aspiration. Ann Am Thorac Soc 11:680–1. Buderi SI, Saleh HZ, Theologou T et al 2014 Endobronchial ultrasound­ Ozgül MA, Cetinkaya E, Tutar N et al 2013 Endobronchial ultrasound­ guided biopsy to diagnose large posterior mediastinal parathyroid guided transbronchial needle aspiration for the diagnosis of intratho­ adenoma prior to video­assisted thoracoscopic resection. BMJ Case Rep racic lymphadenopathy in patients with extrathoracic malignancy: a May 13:2014. study in a tuberculosis­endemic country. J Cancer Res Ther 9:416–21. De Leyn P, Dooms C, Kuzdzal J et al 2014 Revised ESTS guidelines for preop­ Ozgül MA, Cetinkaya E, Tutar N et al 2014 An unusual complication of erative mediastinal lymph node staging for non­small­cell lung cancer. endobronchial ultrasound­guided transbronchial needle aspiration Eur J Cardiothorac Surg 45:787–98. (EBUS­TBNA): the needle breakage. Ann Thorac Cardiovasc Surg 20 Du Rand IA, Barber PV, Goldring J et al 2011 British Thoracic Society guide­ Supplement:567–9. line for advanced diagnostic and therapeutic flexible bronchoscopy in Rusch VW, Asamura H, Watanabe H et al 2009 The IASLC lung cancer adults. Thorax 66 Suppl 3:iii1–21. staging project: a proposal for a new international lymph node map in Eapen GA, Shah AM, Lei X et al 2013 Complications, consequences, and the forthcoming seventh edition of the TNM classification for lung practice patterns of endobronchial ultrasound­guided transbronchial cancer. J Thorac Oncol 4:568–77. needle aspiration: results of the AQuIRE registry. Chest 143:1044–53. Schmid­Bindert G, Wang Y, Jiang H et al 2013 EBUS­TBNA provides highest Hürter T, Hanrath P 1992 Endobronchial sonography: feasibility and pre­ RNA yield for multiple biomarker testing from routinely obtained small liminary results. Thorax 47:565–7. biopsies in non­small cell lung cancer patients – a comparative study of three different minimal invasive sampling methods. PLoS One Krasnik M, Vilmann P, Larsen SS et al 2003 Preliminary experience with a 8:e77948. new method of endoscopic transbronchial real time ultrasound guided biopsy for diagnosis of mediastinal and hilar lesions. Thorax 58: Sun J, Teng J, Yang H et al 2013 Endobronchial ultrasound­guided trans­ 1083–6. bronchial needle aspiration in diagnosing intrathoracic tuberculosis. Ann Thorac Surg 96:2021–7. Lee KJ, Suh GY, Chung MP et al 2014 Combined endobronchial and trans­ esophageal approach of an ultrasound bronchoscope for mediastinal von Bartheld MB, Dekkers OM, Szlubowski A et al 2013 Endosonography staging of lung cancer. PLoS One 9:e91893. vs conventional bronchoscopy for the diagnosis of sarcoidosis: the GRANULOMA randomized clinical trial. JAMA 309:2457–64. Lerner AD, Riker DR 2014 Use of endobronchial ultrasonography in the diagnosis of a pulmonary artery aneurysm. Ann Thorac Surg 97: von Bartheld MB, van Breda A, Annema JT 2014 Complication rate of e139–41. endosonography (endobronchial and endoscopic ultrasound): a sys­ tematic review. Respiration 87:343–51. Lococo F, Rossi G, Agostini L et al 2014 ‘Dry’ pleural mesothelioma success­ fully diagnosed on endobronchial ultrasound (EBUS)­guided trans­ Wallace MB, Pascual JM, Raimondo M et al 2008 Minimally invasive endo­ bronchial needle aspiration (TBNA). Intern Med 53:467–9. scopic staging of suspected lung cancer. JAMA 299:540–6. Medford AR, Bennett JA, Free CM et al 2010 Endobronchial ultrasound­ Wang KP, Terry P, Marsh B 1978 Bronchoscopic needle aspiration biopsy of guided transbronchial needle aspiration (EBUS­TBNA): applications in paratracheal tumors. Am Rev Respir Dis 118:17–21. chest disease. Respirology 15:71–9. Wang R, Folch E, Paul M et al 2014 The use of CP­EBUS­TBNA in the diag­ Moonim MT, Breen R, Fields PA et al 2013 Diagnosis and subtyping of de nosis of chondrosarcoma in a patient with Maffucci syndrome. J Bron­ novo and relapsed mediastinal lymphomas by endobronchial ultra­ chology Interv Pulmonol 21:177–80. sound needle aspiration. Am J Respir Crit Care Med 188:1216–23. Yarmus L, Akulian J, Gilbert C et al 2013 Optimizing endobronchial ultra­ Navani N, Molyneaux PL, Breen RA et al 2011 Utility of endobronchial sound for molecular analysis. How many passes are needed? Ann Am ultrasound­guided transbronchial needle aspiration in patients with Thorac Soc 10:636–43. tuberculous intrathoracic lymphadenopathy: a multicentre study. Yasufuku K, Pierre A, Darling G et al 2011 A prospective controlled trial of Thorax 66:889–93. endobronchial ultrasound­guided transbronchial needle aspiration Neat MJ, Foot NJ, Hicks A et al 2013 ALK rearrangements in EBUS­derived compared with mediastinoscopy for mediastinal lymph node staging of transbronchial needle aspiration cytology in lung cancer. Cytopathology lung cancer. J Thorac Cardiovasc Surg 142:1393–400.e1. 24:356–64. Ojha S, Ie S, Boyd M et al 2014 Vertebral body tumor biopsy: an expanded role of endobronchial ultrasound­guided transbronchial needle aspira­ tion. J Bronchology Interv Pulmonol 21:85–7.
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Abdomen and pelvis: overview and CHAPTER 59 surface anatomy GENERAL STRUCTURE AND FUNCTION OF THE MUSCULOSKELETAL FRAMEWORK OF THE ABDOMINOPELVIC CAVITY ABDOMEN AND PELVIS Although often considered separately, the abdomen and pelvis form the The walls of the abdominopelvic cavity consist of five lumbar vertebrae largest continuous visceral cavity of the body. Together, they provide and their intervening intervertebral discs (lying in the posterior midline); multiple vital functions, including: housing and protection of the diges- the muscles of the anterior abdominal wall lying anteriorly (rectus tive and urinary tracts and of the internal reproductive organs; a conduit abdominis) and anterolaterally (transversus abdominis, internal for neurovascular communication between the thorax and lower limb; oblique and external oblique); the muscles of the posterior abdominal support and attachment for the external genitalia; access to and from wall (psoas, quadratus lumborum and the diaphragm); the bony ‘basin’ the internal reproductive organs and urinary tract; assistance with formed by the walls of the false and true pelvis; the muscles of the pelvic physio logical functions such as respiration, defecation and micturition; floor and perineum lying inferiorly; and the diaphragm lying superiorly support for the vertebral column in weight-bearing, maintenance of (Fig. 59.1). In addition, the upper abdominal cavity gains protection posture and movement; and, in women, the ability to support human from the lower six ribs and their cartilages, even though these structures gestation. are technically part of the thoracic wall. Fig . 59 .1 The bony and muscular structures making up the abdominopelvic ‘cavity’ . The anterolateral abdominal muscles have been removed for clarity . Right cupola (of diaphragm) Medial arcuate ligament Lateral arcuate ligament Right crus Tip of eleventh rib Quadratus lumborum Tip of twelfth rib Psoas minor Iliac crest Psoas major Piriformis Iliacus Ischium Obturator internus Levator ani 1033
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AbdOmEN ANd PElvIS: OvErvIEw ANd SurfACE ANATOmy 1034 8 NOITCES The muscles of the abdominal wall play an important role in move- tion. Parasympathetic stimulation leads to opposing effects. Visceral ment of the trunk (flexion, extension and rotation). The anterolateral afferents also pass through these autonomic plexuses. muscles, in particular, provide assistance with rotation of the thorax in relation to the pelvis (or vice versa if the thorax is fixed). Sympathetic innervation The abdominal cavity is somewhat kidney-shaped in horizontal cross-section due to the posterior indentation of the vertebral column. The cell bodies of neurones of the sympathetic supply of the abdomen Consequently, there are two distinct paravertebral gutters on either and pelvis lie in the intermediolateral grey matter of the first to the side of the spine. The lordosis of the lumbar spine combined with the twelfth thoracic and the first two lumbar spinal segments. Myelinated backward angulation of the sacrum gives each paravertebral gutter a axons from these neurones travel in the ventral ramus of the spinal parabola shape in sagittal section. In standing, the pelvic brim lies at nerve of the same segmental level, leaving it via a white ramus com- an angle of about 55° to the horizontal such that the anterior supe- municans to enter a thoracic or lumbar paravertebral sympathetic gan- rior iliac spines and pubic tubercles are in approximately the same glion. Visceral branches may exit at the same level or ascend or descend coronal plane. The mean angle between the upper border of the first several levels in the sympathetic chain before exiting; they leave the sacral vertebra and the horizontal plane is about 40–45° (Woon et al ganglia without synapsing and pass medially, giving rise to the paired 2013). greater, lesser and least splanchnic nerves, and the lumbar and sacral splanchnic nerves. Axons destined to supply somatic structures synapse Thoracoabdominal interface in the sympathetic ganglion of the same level, and postganglionic, unmyelinated axons leave the ganglion as one or more grey rami com- The diaphragm constitutes the interface between the thoracic and municantes to enter the spinal nerve of the same segmental level. abdominal cavities (Ch. 55). Three principal pathways exist between Greater splanchnic nerve the two cavities across the diaphragm: the caval opening in the central tendon transmits the inferior vena cava and right phrenic nerve; the On each side, the greater splanchnic nerve is derived from the medial, oesophageal hiatus, encircled by the right crus of the diaphragm, trans- visceral branches of the fifth to ninth thoracic sympathetic ganglia. It mits the oesophagus, vagal trunks and vessels; and the aortic hiatus, gives off branches to the descending aorta and enters the abdomen posterior to the median arcuate ligament of the diaphragm, transmits through the fibres of the ipsilateral crus of the diaphragm, on which it the aorta, thoracic duct and, usually, the azygos vein. The hemiazygos descends anteroinferiorly. The main trunk of the nerve enters the supe- vein usually enters the thorax through the left crus of the diaphragm. rior aspect of the coeliac ganglion, where most of the preganglionic Other lymphatics from the abdomen drain to the thorax alongside the fibres synapse (but not those destined for the suprarenal medulla). inferior vena cava and via small vessels passing through and around lesser splanchnic nerve the diaphragm. Thoracic splanchnic nerves reach the abdomen through the diaphragmatic crura and behind the medial arcuate ligaments, On each side, the lesser splanchnic nerve is derived from the medial, and the left phrenic nerve pierces the muscle of the left hemidiaphragm. visceral branches of the tenth and eleventh thoracic ganglia (or ninth The subcostal vessels pass into the abdomen beneath the lateral arcuate and tenth). It enters the abdomen running through the lowermost fibres ligaments of the diaphragm. Anteriorly, the superior epigastric vessels of the ipsilateral crus of the diaphragm or under the medial arcuate pass between the costal and xiphoid attachments of the diaphragm. ligament, and then lies on the crus as it runs anteroinferiorly. The trunk Neurovascular structures also cross between the thorax and abdomen of the nerve joins the aorticorenal ganglion and may give branches to within the subcutaneous tissues. the lateral aspect of the coeliac ganglion. It occasionally joins the greater and least splanchnic nerves as a single splanchnic nerve. Pelvis–lower limb interface least splanchnic nerve On each side, the least splanchnic nerve is derived from the medial, The pelvis forms an integral part of the bony structure of both the visceral branches of the eleventh and/or twelfth thoracic ganglia. It abdominopelvic cavity and the lower limb. It transmits the weight of enters the abdomen medial to the sympathetic chain under the medial the upright body, as well as providing a stable platform for movement arcuate ligament of the diaphragm and runs inferiorly to join the renal of the hip joint and bipedal locomotion. Its bony surfaces provide plexus. The trunk of the nerve enters the aorticorenal ganglion and may attachment sites for the muscles of the buttock and thigh (Ch. 80), the give branches to the lateral aspect of the coeliac ganglion. It is some- pelvic floor and perineal membrane, the abdominal wall and lower times part of the lesser splanchnic nerve, when it forms a twig that back. The pelvis also transmits the neurovascular structures that supply enters the renal plexus just below the aorticorenal ganglion. the lower limb. There are four principal pathways between the pelvis The thoracic splanchnic nerves are subject to considerable individual and lower limb: the interval beneath the inguinal ligament anterior to variation in their origin and distribution (Loukas et al 2010). For the superior pubic ramus and ilium, which transmits the femoral neu- example, the greater splanchnic nerve may receive a contribution from rovascular structures and lymphatics; the greater and lesser sciatic the fourth or tenth thoracic sympathetic ganglia or originate only from foramina, which transmit the gluteal vessels and nerves, sciatic nerve, the sixth to ninth ganglia. and internal pudendal vessels and pudendal nerve; and the obturator foramen, which transmits the obturator nerve, vessels and lymphatics. lumbar sympathetic system Autonomic nerves travel with the arterial supply to the lower limb and The lumbar part of each sympathetic trunk usually contains four inter- with the branches of the sacral plexus. Neurovascular structures also connected ganglia lying on the anterolateral aspects of the lumbar cross between the lower limb and pelvis within the subcutaneous vertebrae along the medial margin of psoas major (see Figs 59.2, 62.14) tissues. (Murata et al 2003). Superiorly, it is continuous with the thoracic sym- pathetic trunk posterior to the medial arcuate ligament. Inferiorly, it passes posterior to the common iliac vessels and is continuous with the GENERAL ARRANGEMENT OF ABDOMINOPELVIC sacral sympathetic trunk. On the right side, it lies posterior to the infe- AUTONOMIC NERVES rior vena cava; on the left, it is posterior to the lateral aortic lymph nodes. It is anterior to most of the lumbar vessels but may pass behind What follows is a brief overview of the autonomic nervous system in some lumbar veins. the abdominopelvic region; descriptions of the neurovascular supply to On each side, the first, second and, sometimes, the third lumbar individual organs are given in the relevant chapters. The autonomic ventral spinal rami are connected to the lumbar sympathetic trunk by supply to the abdominal and pelvic viscera is via the abdominopelvic white rami communicantes. All lumbar ventral rami are joined near part of the sympathetic chain and the greater, lesser and least splanchnic their origins by long, slender, grey rami communicantes from the four nerves (sympathetic), and the vagus and pelvic splanchnic nerves (para- lumbar sympathetic ganglia. Their arrangement is irregular: one gan- sympathetic). Numerous interconnections occur between plexuses and glion may give rami to two or three lumbar ventral rami, one lumbar ganglia, particularly in the major plexuses around the abdominal aorta; ventral ramus may receive rami from two ganglia, or grey rami may hence, the descriptions tend to be simplifications based on the ‘main’ leave the sympathetic trunk between ganglia (Murata et al 2003). supply to each organ (Fig. 59.2). The details of the terminations of these fibres are given in the description of the microstructure of the gut Somatic and vascular branches wall. Sympathetic nerve branches accompany the lumbar arteries round the As a general rule, sympathetic neurones from the abdominopelvic sides of the vertebral bodies, medial to the fibrous arches to which psoas autonomic plexuses inhibit visceral smooth muscle motility and glan- major is attached, to provide sympathetic innervation to the lumbar dular secretions, induce sphincter contraction and cause vasoconstric- somatomes. Branches from the lumbar ganglia innervate the abdominal
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General arrangement of abdominopelvic autonomic nerves 1035 95 rETPAHC Fig . 59 .2 The overall arrangement of the autonomic plexuses of the abdominal and pelvic viscera . Anterior and posterior vagal trunks Superior mesenteric Coelic plexus and ganglia plexus and ganglia T12 sympathetic ganglion Left aorticorenal plexus and ganglion Right renal ganglion and plexus Intermesenteric L1–4 sympathetic plexuses ganglia Inferior mesenteric plexus and ganglia Right lumbar Superior hypogastric sympathetic chain plexus Hypogastric nerve Inferior hypogastric plexus aorta and common, external and internal iliac arteries, forming delicate Damage to these nerves, e.g. during aortoiliac surgery, can result in nerve plexuses that extend along the vessels. Other postganglionic sym- sexual dysfunction. pathetic nerves to vessels and skin travel with somatic nerves. Thus, the femoral nerve carries vasoconstrictor sympathetic nerves to the femoral Pelvic sympathetic system artery and its branches in the thigh, as well as sympathetic fibres in its The sacral region of the sympathetic trunk usually consists of four or cutaneous branches. Postganglionic fibres travelling with the obturator five ganglia located medial or anterior to the anterior sacral foramina nerve supply the obturator artery and the skin of the medial thigh. beneath the presacral fascia (Oh et al 2004). Occasionally, one or two Sympathetic denervation of vessels in the lower limb can be effected by coccygeal ganglia are present. The sacral sympathetic trunk is continu- removing or ablating the upper three lumbar ganglia and intervening ous above with the lumbar sympathetic trunk, and preganglionic fibres parts of the sympathetic trunk; this procedure may be useful in treating descend from the lower lumbar spinal cord segments via this route. The some varieties of vascular insufficiency of the lower limb. first sacral sympathetic ganglion is the largest. More caudal ganglia become progressively smaller (Blaszczyk 1981). The sacral sympathetic Lumbar splanchnic nerves chain is often asymmetric, with absent or fused ganglia, and cross- Four lumbar splanchnic nerves pass as medial branches from the communications between each side are frequent. Each ganglion sends ganglia to join the coeliac, inferior mesenteric and superior hypogastric at least one grey ramus communicans to its adjacent spinal nerve plexuses. The first lumbar splanchnic nerve, from the first ganglion, but up to 11 such branches from a single ganglion have been reported gives branches to the coeliac, renal and inferior mesenteric plexuses. (Potts 1925). The second nerve joins the inferior part of the intermesenteric or infe- The pelvic sympathetic chain converges caudally to form a rior mesenteric plexus. The third nerve arises from the third or fourth solitary retroperitoneal structure, the ganglion impar (or ganglion of ganglion and joins the superior hypogastric plexus. The fourth lumbar Walther), which lies at a variable level between the sacrococcygeal splanchnic nerve from the lowest ganglion passes anterior to the joint and the tip of the coccyx; it is occasionally paired, unilateral common iliac vessels to join the lower part of the superior hypogastric or absent (Oh et al 2004). It conveys sympathetic efferents to and plexus, or the hypogastric nerves. It is important to note that lumbar nociceptive afferents from the perineum and terminal urogenital splanchnic sympathetic nerves contribute to the superior and inferior regions. Ganglion impar blockade may be used to treat intractable hypogastric plexuses and, therefore, contribute to the innervation of the perineal pain of sympathetic origin in patients with pelvic cancers bladder neck, ductus deferens and prostate, among other structures. (Toshniwal 2007).
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AbdOmEN ANd PElvIS: OvErvIEw ANd SurfACE ANATOmy 1036 8 NOITCES Somatic and vascular branches gastric branch, and run beneath the peritoneum, deep to the posterior Grey rami communicantes containing postganglionic sympathetic wall of the upper part of the lesser sac, to reach the coeliac plexus. Their nerves pass from the pelvic sympathetic ganglia to the sacral and coc- synaptic relays with postganglionic neurones are situated in the mye- cygeal spinal nerves. There are no white rami communicantes at this nteric (Auerbach’s) and submucosal (Meissner’s) plexuses in the wall level. The postganglionic fibres are distributed via the sacral and coc- of the gut (see below). cygeal plexuses (Woon and Stringer 2014). Thus, sympathetic fibres in Pelvic splanchnic nerves the tibial nerve are conveyed to the popliteal artery and its branches in the leg and foot, whilst those in the pudendal and superior and inferior Pelvic splanchnic nerves to the pelvic viscera travel in the anterior rami gluteal nerves accompany these arteries to the perineum and buttocks. of the second, third and fourth sacral spinal nerves. They leave the Small branches also travel with the median and lateral sacral arteries. nerves as they exit the anterior sacral foramina and pass in the presacral tissue as a fine network of branches that are distributed to three prin- Sacral splanchnic nerves cipal destinations. Most pass anterolaterally into the network of nerves Sacral splanchnic nerves pass directly from the ganglia to the inferior that form the inferior hypogastric plexus; from here, they pass to the hypogastric plexus and, from there, to pelvic viscera; they usually arise pelvic viscera. Some join directly with the hypogastric nerves and ascend from the first two sacral sympathetic ganglia. out of the pelvis, as far as the superior hypogastric plexus; from here, they are distributed with branches of the inferior mesenteric artery Parasympathetic innervation (p. 1153). A few run superolaterally in the presacral tissue, over the pelvic brim anterior to the left iliac vessels, and pass directly into the tissue of the retroperitoneum and the mesentery of the sigmoid and The parasympathetic neurones innervating the abdomen and pelvis lie descending colon. either in the dorsal motor nucleus of the vagus nerve or in the interme- The pelvic splanchnic nerves are motor to the smooth muscle of the diolateral grey matter of the second, third and fourth sacral spinal hindgut and bladder wall, supply vasodilator fibres to the erectile tissue segments. The vagus nerves supply parasympathetic innervation to the of the penis and clitoris, and are secretomotor to the hindgut. abdominal viscera as far as the distal transverse colon, i.e. they supply the foregut and midgut. The hindgut is supplied by parasympathetic Abdominopelvic autonomic plexuses fibres travelling via the pelvic splanchnic nerves (see below); the overlap and ganglia between these two supplies is variable. The vagal trunks are derived from the oesophageal plexus and enter the abdomen via the oesopha- geal hiatus, closely related to the anterior and posterior walls of the The abdominopelvic autonomic plexuses are somewhat variable and abdominal oesophagus (see Fig. 56.6). The anterior vagal trunk is often fuse or are closely interrelated. The following descriptions recog- mostly derived from the left vagus and the posterior from the right nize their main features (Figs 59.3–59.4). vagus. The nerves supply the intra-abdominal oesophagus and stomach Coeliac plexus directly. The anterior trunk gives off a hepatic branch, which innervates the liver parenchyma and vasculature, the biliary tree including the The coeliac plexus is located at the level of the twelfth thoracic and first gallbladder, and the structures in the free edge of the lesser omentum. lumbar vertebrae, and is the largest major autonomic plexus. It is a The posterior trunk supplies branches to the coeliac plexus; these fibres dense network that unites the coeliac ganglia, and surrounds the coeliac frequently constitute the largest portion of the fibres contributing to the artery and the root of the superior mesenteric artery. It is posterior to plexus. They arise directly from the posterior vagal trunk and from its the stomach and lesser sac, and anterior to the crura of the diaphragm Sympathetic Parasympathetic Greater splanchnic nerve (T5–9) Posterior vagal trunk T12 Lesser splanchnic nerve (T10,11) Coeliac plexus T12g L1 Superior mesenteric plexus L1g Intermesenteric plexus L2 First lumbar sympathetic nerve L2g Inferior mesenteric plexus Second lumbar sympathetic nerve Lumbar splanchnic nerves L3 Superior hypogastric plexus L3g Third lumbar sympathetic nerve L4 Retroperitoneal parasympathetic fibres Fourth lumbar sympathetic nerve L4g Inferior hypogastric nerve Inferior hypogastric plexus S1g Sacral splanchnic nerves Pelvic splanchnic nerves S2g Key S2 T12g – 12th thoracic sympathetic ganglion S1g – 1st sacral sympathetic ganglion S3g Nervous structures L1g – 1st lumbar sympathetic ganglion S2g – 2nd sacral sympathetic ganglion S3 Sympathetic fibres Parasympathetic fibres L2g – 2nd lumbar sympathetic ganglion S3g – 3rd sacral sympathetic ganglion S4g S4 Ganglion L3g – 3rd lumbar sympathetic ganglion S4g – 4th sacral sympathetic ganglion Plexus tissue L4g – 4th lumbar sympathetic ganglion Nerve fibres Fig . 59 .3 The autonomic plexuses innervating the abdominal and pelvic viscera: schematic diagram .
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General arrangement of abdominopelvic autonomic nerves 1037 95 rETPAHC Fig . 59 .4 The autonomic Branches of posterior vagal trunk plexuses of the abdominal Greater splanchnic nerve and pelvic viscera . Lesser splanchnic nerve Coeliac plexus and ganglia Middle colic artery Superior mesenteric plexus and ganglion Left renal vein First and second lumbar nerves Intermesenteric plexus Right colic artery Inferior mesenteric plexus and ganglion Left ureter Third and fourth lumbar nerves Sigmoid branches of inferior mesenteric artery Lumbar sympathetic chain Retroperitoneal parasympathetic fibres External iliac artery Internal iliac artery Inferior hypogastric plexus Inferior hypogastric plexus Sacral sympathetic chain Sacral parasympathetic roots Communication with Fig . 59 .5 Distribution of phrenic plexus the upper abdominal autonomic plexuses . Right coeliac ganglion Right aorticorenal ganglion Coeliac plexus Right suprarenal gland Left greater splanchnic nerve Left lesser splanchnic nerve Right kidney Superior mesenteric plexus Left renal plexus Intermesenteric plexus Aorta and the beginning of the abdominal aorta, and lies medial to the supra- Anaesthesia or ablation of these nerves (coeliac plexus block) is some- renal glands. The plexus and ganglia receive the greater and lesser times undertaken to treat intractable pain from pancreatic disorders. splanchnic nerves and branches from the vagal trunks. The plexus is in continuity with small branches along adjacent arteries and is connected Coeliac and aorticorenal ganglia to the phrenic, splenic, hepatic, superior mesenteric, suprarenal, renal The coeliac ganglia are irregular neural masses, measuring approxi- and gonadal plexuses (Fig. 59.5). Visceral afferents in the coeliac plexus mately 2 cm across, located between the origin of the coeliac trunk and convey pain and other sensations from upper abdominal viscera. superior mesenteric artery, medial to the suprarenal glands and anterior
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AbdOmEN ANd PElvIS: OvErvIEw ANd SurfACE ANATOmy 1038 8 NOITCES to the crura of the diaphragm (Zhang et al 2006). They vary in number, internal iliac vessels and the attachments of levator ani and obturator size, shape and precise location; there are often two, one on each side. internus lie laterally, and the superior vesical and obliterated umbilical The right ganglion is frequently posterior to the inferior vena cava, and arteries superiorly. In males, the inferior hypogastric plexus lies postero- the left ganglion often lies posterior to the origin of the splenic artery. laterally on either side of the seminal vesicles, prostate and the base of The ipsilateral greater splanchnic nerve joins the upper part of each the urinary bladder. In men, the point where the vas (ductus) deferens ganglion and the lesser splanchnic nerve joins the lower part. The lower- crosses the ureter provides an approximate guide to the upper limit of most part of each ganglion forms a distinct subdivision, usually termed the plexus (Mauroy et al 2003). The upper border of the plexus lies the aorticorenal ganglion, which receives the ipsilateral lesser splanch- beneath the peritoneum of the rectovesical pouch and is in contact nic nerve and gives origin to the majority of the renal plexus (which, with the lateral aspect of the base of the bladder. The anterior border most commonly, lies anterior to the origin of the renal artery). reaches the posterior aspect of the prostate; at its inferior limit, the cavernous (deep, cavernosal) nerve passes forwards to reach the postero- Phrenic plexus lateral aspect of the prostate (see Fig. 75.11). In females, each plexus The phrenic plexus is a periarterial extension of the coeliac plexus lies lateral to the uterine cervix, vaginal fornix and the posterior part of around the right inferior phrenic artery, adjacent to the right crus of the the urinary bladder, often extending into the broad ligaments of the diaphragm (Rusu 2006). It contains one or two phrenic ganglia and a uterus. The upper limit of the plexus corresponds approximately to the definable nerve trunk that connects the coeliac plexus and phrenic level where the uterine artery crosses the ureter in the base of the broad nerve. The plexus supplies branches to the suprarenal glands and ligament (Azaïs et al 2013). diaphragm. The inferior hypogastric plexus is formed mainly from pelvic splanchnic (parasympathetic) and sacral splanchnic (sympathetic) Superior mesenteric plexus and ganglion branches; a smaller contribution is derived from sympathetic fibres The superior mesenteric plexus lies in the pre-aortic connective tissue (from the lower lumbar ganglia), which descend into the plexus from posterior to the pancreas, around the origin of the superior mesenteric the superior hypogastric plexus via the hypogastric nerves. It gives origin artery. It is an inferior continuation of the coeliac plexus, and includes to a complex network of small pelvic branches, which supply the pelvic branches from the posterior vagal trunk and coeliac plexus. Its branches viscera either directly or indirectly via periarterial plexuses. The branches accompany the superior mesenteric artery and its divisions. The supe- of the inferior hypogastric plexus supply the vas deferens, seminal vesi- rior mesenteric ganglion lies superiorly in the plexus, usually above the cles, prostate, accessory glands and penis in males; the ovary, Fallopian origin of the superior mesenteric artery. tubes, uterus, uterine cervix and vagina in females; and the urinary bladder and distal ureter in both sexes. The plexus plays a key role in Intermesenteric plexus continence and sexual function. Like other parts of the abdominal aortic autonomic plexus, the interme- senteric plexus is not a discrete structure but is part of a continuous Hypogastric nerves The hypogastric nerves are usually paired nerve periarterial nerve plexus connected to the gonadal, inferior mesenteric, bundles but may consist instead of multiple filaments. They contain iliac and superior hypogastric plexuses. It lies on the lateral and anterior sympathetic fibres (mostly descending from the superior hypogastric aspects of the aorta, between the origins of the superior and inferior plexus) and parasympathetic fibres (ascending from the inferior mesenteric arteries, and consists of numerous fine, interconnected nerve hypogastric plexus). The nerves run between the superior and inferior fibres and a few ganglia continuous superiorly with the superior hypogastric plexuses on each side behind the presacral fascia medial to mesenteric plexus and inferiorly with the superior hypogastric plexus. the internal iliac vessels and lateral to the anterior sacral foramina. It is not well characterized but receives parasympathetic and sympa- thetic branches from the coeliac plexus and additional sympathetic Other autonomic plexuses and ganglia rami from the first and second lumbar splanchnic nerves. Additional plexuses are described for abdominopelvic viscera, such as the hepatic and gonadal plexuses. Each tends to lie around the main Inferior mesenteric plexus arterial supply to the organ. They receive both sympathetic and para- The inferior mesenteric plexus lies around the origin of the inferior sympathetic fibres from one or more of the major autonomic plexuses mesenteric artery and is distributed along its branches. It is formed and have one or more ganglia. Thus, autonomic ganglia supplying the predominantly from the aortic plexus, supplemented by sympathetic testis are found around the origin of the testicular arteries from the fibres from the first and second lumbar splanchnic nerves and ascend- abdominal aorta and have connections with the renal, lumbar and ing pelvic parasympathetic fibres from the inferior hypogastric plexus intermesenteric autonomic plexuses (Motoc et al 2010). (via the hypogastric nerves and superior hypogastric plexus). Disrup- tion of the inferior mesenteric plexus alone rarely causes clinically Para-aortic bodies significant disturbances of autonomic function. Superior hypogastric plexus The para-aortic bodies (also known as paraganglia or, collectively, as The superior hypogastric plexus lies anterior to the aortic bifurcation, the organ of Zuckerkandl) are collections of neural crest-derived chro- the left common iliac vein, median sacral vessels, fifth lumbar vertebral maffin tissue found in close relation to the aortic autonomic plexuses. body and sacral promontory, and between the common iliac arteries. They are relatively large in the fetus, reach a maximum size at around It is occasionally referred to as the presacral nerve, but is seldom a single 3 years of age, and have usually regressed by adulthood. They are most nerve and is prelumbar rather than presacral. It lies within extraperito- commonly found as a pair of bodies lying anterolateral to the aorta in neal connective tissue in the midline, extending a little to the left. The the region of the inferior mesenteric and superior hypogastric plexuses, breadth of the plexus and its constituent nerves varies; appearances but multiple smaller collections may be present. Occasionally, they are range from a reticular-like arrangement to a band-like structure or one found as high as the coeliac plexus or as low as the inferior hypogastric or two distinct nerve trunks (Paraskevas et al 2008). The medial attach- plexus in the pelvis, or may be closely applied to the sympathetic ment of the sigmoid mesocolon and upper limit of the mesorectum lie ganglia of the lumbar chain. Scattered cells that persist into adulthood anterior to the lower part of the plexus, separated from it by a thin layer may, rarely, be the sites of paraganglioma (extra-adrenal phaeochromo- of loose connective tissue. The plexus is formed by branches from three cytoma) (Subramanian and Maker 2006). main sources: the aortic plexus (sympathetic and parasympathetic), lumbar splanchnic nerves (sympathetic) and pelvic splanchnic nerves GENERAL ARRANGEMENT OF ABDOMINOPELVIC (parasympathetic), which ascend from the inferior hypogastric plexus via the right and left hypogastric nerves. Visceral afferents also pass VASCULAR SUPPLY through the plexus. The hypogastric nerves lie in loose connective tissue just posterolateral to the upper mesorectum and pass over the pelvic The major vessels that occupy the abdomen and pelvis not only supply brim medial to the internal iliac vessels. The superior hypogastric plexus the viscera, retroperitoneal structures and much of the bony and soft conveys branches to the inferior mesenteric plexus and to the ureteric, tissue walls of both cavities, but also course through the cavities en route gonadal and common iliac nerve plexuses; additional small branches to supply the lower limbs. The arteries and systemic veins of the turn abruptly forwards into the upper mesorectum to travel with the abdomen and pelvis lie predominantly posteriorly in the abdomen and superior rectal artery. posterolaterally in the pelvis. From the caval and aortic openings in the diaphragm, they follow the general parabolic shape of the lumbar Inferior hypogastric plexus spine. The pelvic divisions follow the contours of the brim and side The inferior hypogastric plexus lies in the thin extraperitoneal connec- wall of the true pelvis (Figs 59.6–59.7). The individual parts of the tive tissue on the pelvic side wall anterolateral to the mesorectum. The aortoiliac and iliocaval systems are described in the relevant chapters.
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General arrangement of abdominopelvic autonomic nerves 1039 95 rETPAHC Fig . 59 .6 The overall arrangement of the aortoiliac arterial tree of the abdomen and pelvis . Left inferior phrenic artery Coeliac trunk Right suprarenal Left renal artery artery Superior Abdominal aorta mesenteric artery Left gonadal artery Right second, third and fourth lumbar arteries Inferior mesenteric artery Right common iliac artery Right iliolumbar Left internal artery iliac artery Right external iliac artery Arterial supply to the gastrointestinal tract (Ch. 69). Anastomoses between the territories of the superior and infe- rior mesenteric arteries are less numerous; the most consistent is the marginal artery of the colon (Ch. 66). The arterial supply to the gastrointestinal tract is derived from the ante- rior midline visceral branches of the aorta. There are usually three Portal venous system anterior branches: the coeliac trunk and the superior and inferior mesenteric arteries. Major variants in the origin of the arteries are uncommon (Ch. 62). Accessory or replaced branches to the abdominal The (hepatic) portal system, like all portal venous systems, connects two viscera are more common. The inferior mesenteric artery almost always capillary beds: that of the abdominal and pelvic parts of the gut from arises separately but replaced, accessory or anastomotic vessels may the abdominal part of the oesophagus to the lower anal canal, together arise from the proximal superior mesenteric artery or its branches. with all derived organs other than the liver (i.e. the pancreas, gallblad- Occasionally, these may contribute to the arterial supply of the inferior der and spleen), and the hepatic sinusoidal ‘capillary’ bed. The intra- mesenteric artery (Horton and Fishman 2002). hepatic portal vein ramifies and ends in the hepatic sinusoids; from The coeliac trunk and its branches supply the part of the foregut that here, blood drains to central veins that converge to form the hepatic extends from the distal oesophagus to the mid part of the descending veins which drain into the inferior vena cava (Ch. 67). In adults, the duodenum, together with associated viscera (liver, biliary tree, spleen, portal vein has no valves. In fetal and early postnatal life, valves are dorsal pancreas, greater and lesser omenta). The superior mesenteric demonstrable in tributaries of the portal vein but they usually atrophy artery supplies the midgut, which extends from the mid descending with further maturation. duodenum to the distal third of the transverse colon (including Portal vein jejunum, ileum, caecum, appendix, ascending and transverse colon). The inferior mesenteric artery supplies the part of the hindgut that The portal vein is formed behind the neck of the pancreas at the level extends from the distal transverse colon to the upper anal canal. Even of the L1/2 intervertebral disc (in the transpyloric plane) from the in the absence of accessory arteries, numerous anastomoses exist convergence of the superior mesenteric and splenic veins (Fig. 59.8). It between these vascular territories. For example, anastomoses around the is approximately 8 cm long in the adult and ascends obliquely to the head of the pancreas and the duodenum are formed between the ante- right behind the first part of the duodenum, the common bile duct and rior and posterior superior pancreaticoduodenal arteries and the ante- gastroduodenal artery; at this point, it is directly anterior to the inferior rior and posterior inferior pancreaticoduodenal arteries, and between vena cava. It enters the right border of the lesser omentum and ascends the posterior superior pancreaticoduodenal artery and jejunal arteries anterior to the epiploic foramen to reach the right end of the porta
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AbdOmEN ANd PElvIS: OvErvIEw ANd SurfACE ANATOmy 1040 8 NOITCES Fig . 59 .7 The overall arrangement of the iliocaval venous system of the abdomen and pelvis . Inferior vena cava Hemiazygos vein Left suprarenal vein Right subcostal Left renal vein vein Left gonadal vein Right first lumbar vein Left lumbar veins Right ascending lumbar vein Right gonadal vein Right iliolumbar Left internal vein iliac vein Right common iliac vein Left external iliac vein hepatis, where it divides into right and left main branches, which the hindgut traverses the pelvic floor; in these sites, the gut tube is sur- accompany the corresponding branches of the hepatic artery into the rounded by a connective tissue adventitia. Neural elements invade the liver. In the lesser omentum, the portal vein lies posterior to both the gut from neural crest tissue (Ch. 17). The smooth muscle of the mus- common bile duct and the hepatic artery. It is surrounded by the hepatic cularis externa layers of the alimentary canal is supplemented with nerve plexus and accompanied by lymphatics and some lymph nodes. striated muscle at the beginning (from the branchial arches) and end of the gut tube. Tributaries of the portal vein The mature gut wall has four main layers: mucosa, submucosa, The main extrahepatic tributaries of the portal vein are the left gastric muscularis externa and serosa (Fig. 59.9). The mucosa (mucous mem- (coronary) vein and the posterior superior pancreaticoduodenal vein brane) is the innermost layer and is subdivided into a lining epithelium, (Ch. 67). Within the liver, the left branch receives the obliterated an underlying lamina propria (a layer of loose connective tissue, where umbilical vein via the ligamentum teres, which connects to its vertical many of the glands are also found) and a thin layer of smooth muscle, portion. the muscularis mucosae. The submucosa is a strong and highly vascular- ized layer of connective tissue. The muscularis externa consists of inner circular and outer longitudinal layers of smooth muscle; an incomplete GENERAL MICROSTRUCTURE OF THE GUT WALL oblique muscle layer is present only in the stomach. The external surface is bounded by a serosa or adventitia, depending on its position The gut wall displays a common structural plan that is modified region- within the body. ally to take account of local functional differences. The general micro- structure is best appreciated by reference to the development of the gut Mucosa (Ch. 60). Much of the alimentary canal originates as a tube of endo- derm enclosed in splanchnopleuric mesoderm. Its external surface faces the embryonic coelom, and the endodermal lining forms the epithe- Epithelium lium of the canal and also the secretory and ductal cells of various The epithelium is the site of secretion and absorption, and provides a glands that secrete into the lumen, including the pancreas and liver. The defence against various threats, including microorganisms. Its protec- splanchnopleuric mesoderm forms the connective tissue, muscle layers, tive function against mechanical, thermal and chemical injury is par- blood vessels and lymphatics of the wall, and its external surface ticularly evident in the oesophagus and anal canal, where it is thick, becomes the visceral mesothelium or serosa. There is no serosa sur- stratified and covered in mucus, which serves as a protective lubricant. rounding the cervical and thoracic portions of the gut, or below where At other sites, the epithelium lining the gut wall is single-layered, and
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General microstructure of the gut wall 1041 95 rETPAHC Fig . 59 .8 The overall arrangement of the portal venous system draining the abdominal viscera . Inferior vena cava Short gastric veins Portal vein Splenic vein Pancreatico- Left gastroepiploic vein duodenal veins Superior mesenteric vein Inferior mesenteric vein Middle colic vein Left colic vein Marginal colic veins Ileocolic vein Sigmoid veins Superior rectal vein either cuboidal (in glands) or columnar. It contains cells modified for mucosae are found inside the villi or between the tubular glands of the absorption, as well as various types of secretory cell. stomach and large intestine. By its contraction, the muscularis mucosae The barrier function and selectivity of absorption depend on tight can alter the surface configuration of the mucosa locally, allowing it to junctions over the entire epithelium. The surface area of the lumen adapt to the shapes and mechanical forces imposed by the contents of available for secretion or absorption is increased by the presence of the lumen, and in the intestinal villi, promoting vascular exchange and mucosal folds, crypts, villi and glands (see Fig. 59.9). Microvilli on the lymphatic drainage. surfaces of individual absorptive cells amplify the area of apical plasma membrane in contact with the contents of the gut. Some glands lie in Submucosa the lamina propria and some in the submucosa; others (the liver and pancreas) are totally external to the wall of the gut. All of these glands The submucosa contains large bundles of collagen and is the strongest drain into the lumen of the gut through individual ducts. The epithe- layer of the gut wall. However, it is also pliable and deformable, and lium also contains scattered neuroendocrine (enteroendocrine) cells. can therefore adjust to changes in the length and diameter of the gut. Lamina propria Its contained arterial network is relatively dense and supplies both the mucosa and the muscle coat. The submucosa extends into the rugae of The lamina propria consists of compact connective tissue, often rich in the gastric wall, the plicae circulares of the small intestine (but not the elastin fibres, which supports the surface epithelium and contains nutri- villi), and the folds that project into the lumen of the colon and rectum. ent vessels and lymphatics. Lymphoid follicles are present in many regions of the gut, most notably in Peyer’s patches. Cells within the Muscularis externa lamina propria are the source of growth factors that regulate cell turn- over, differentiation and repair in the overlying epithelium. The muscularis externa usually consists of distinct inner circular and Muscularis mucosae outer longitudinal layers that create waves of peristalsis responsible for The muscularis mucosae is particularly well developed in the oesopha- the movement of ingested material through the lumen of the gut. In gus and in the large intestine, especially in the terminal part of the the stomach, where movements are more complex, there is an incom- rectum. In addition, single muscle cells originating from the muscularis plete oblique layer of muscle, internal to the other two layers. The
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AbdOmEN ANd PElvIS: OvErvIEw ANd SurfACE ANATOmy 1042 8 NOITCES Layers of the gut wall A. Mucosa B. Submucosa C. Muscularis externa D. Serosa Epithelium A Lamina propria Muscularis mucosae B Submucosa Inner Colon circular layer Ileum C Jejunum Outer longitudinal Duodenum layer Stomach Secretions Oesophagus of liver and D Serosa pancreas Fig . 59 .9 The general arrangement of the alimentary canal to show the layers of the gut wall at the levels indicated . circular muscle layer is invariably thicker than the longitudinal muscle, stomach, or partitions them, as occurs at the pyloric sphincter. The except in the colon, where the longitudinal muscle is condensed into muscle maintains a constant volume, so that shortening of a segment three cords (taenia coli). of the gut wall is accompanied by an increase in thickness of the The muscularis externa is composed almost exclusively of smooth muscle layer. muscle, except in the upper oesophagus, where smooth muscle blends Intestinal smooth muscle exhibits variable and changing degrees of with striated muscle. Although the upper oesophageal musculature contraction on which rhythmic (or phasic) contractions are superim- resembles that of the pharynx, it is entirely under involuntary control. posed. Slow waves of rhythmic electrical activity, driven by changes in For most of its length, the smooth muscle of the gut wall consists of membrane potentials in pacemaker cells (interstitial cells), spread ill-defined bundles of cells, typically visceral in type, and somewhat throughout the thickness of the circular and longitudinal smooth larger than vascular smooth muscle cells. They are approximately muscle coats. After spreading circumferentially, slow waves can move 500 µm long, regardless of body size, and are electrically and mechani- in either oral or anal directions, causing segmental contraction. The cally coupled. Their fasciculi lack a perimysium but have sharp distances of propagation and the patterns of this spontaneous activity boundaries. vary between areas of the intestine. Neural regulation of slow and The arrangement of the musculature allows a segment of gut to phasic contractions involves excitatory and inhibitory transmitters that undergo extensive changes in diameter (to virtual occlusion of the are released from the myenteric plexus. This motor control is closely lumen) and length, although elongation is limited by the presence of coordinated with mucosal absorption and secretion, and is mediated mesenteries. The coordinated activity of the two muscle layers pro- via intrinsic nerves in the submucous plexus. The peristaltic reflex duces a characteristic motor behaviour that is mainly propulsive and occurs during passage of luminal contents down the intestine. It directed aborally (peristalsis), combined with a non-propulsive motor involves ascending contraction and descending relaxation; the sensory activity that either mixes the luminal contents, as occurs in the limb is mediated by sensory neurones that respond to either mucosal
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General microstructure of the gut wall 1043 95 rETPAHC stimulation (intrinsic primary afferents) or muscle stretch (extrinsic The latter is not essential for function, as evidenced by intestinal activity afferents). after transplantation of the extrinsically denervated gut. In contrast, neuropathies affecting the enteric nervous system, such as Hirsch- Interstitial cells sprung’s disease, are potentially life-threatening. For a detailed descrip- Interstitial cells of Cajal (ICCs) are found throughout the entire length tion of the enteric nervous system, see Furness et al (2014). of the gastrointestinal tract, where they lie in close contact with nerve terminals; they have numerous gap junctions with each other and with Extrinsic innervation smooth muscle cells. Distinct networks are found in the myenteric Extrinsic innervation of the gut is from sympathetic, parasympathetic plexus between the circular and longitudinal muscle. Looser arrange- and visceral sensory nerves. The cell bodies of preganglionic parasym- ments exist within the individual muscle layers and the submucosa of pathetic efferent axons are found in the vagal dorsal motor nucleus in the gut, and isolated or small groups of ICCs are also found in the the medulla oblongata and in the sacral segments of the spinal cord. subserosal region. ICCs originate from mesenchymal cells and resemble Their main target in the gut is the enteric neurones of the myenteric smooth muscle cells but have fewer contractile elements and their plexus. Vagal efferents play a major role in oesophageal propulsion, intermediate filaments contain vimentin rather than desmin. They are gastric acid secretion and emptying, gallbladder contraction and pan- involved in the generation of pacemaker signals, the propagation of creatic exocrine secretion. Pelvic efferents innervate the distal colon and electrical slow wave activity, neuromuscular transmission, and mech- rectum. Sympathetic efferent neurones have their cell bodies in the anosensation (p. 1135) (Sanders et al 2014). Defective ICC function has intermediolateral grey matter (lamina VII) of the thoracolumbar seg- been implicated in a wide range of gastrointestinal motility disorders ments of the spinal cord; those destined for the smooth muscle of the (Al-Shboul 2013), and in the development of gastrointestinal stromal gut mostly pass through the sympathetic chain without synapsing and tumours (Roggin and Posner 2012). relay in prevertebral ganglia (coeliac, mesenteric and pelvic), whereas Cells with a similar morphology have been found in association those mediating vasoconstriction synapse in the sympathetic chain or with smooth muscle at many other sites, such as the urethra, ductus prevertebral ganglia. Postganglionic sympathetic fibres are distributed deferens, prostate, bladder, corpus cavernosum, ureter, uterine tube, and with the branches of the coeliac trunk and mesenteric arteries to three uterus. They may act as electrical pacemakers in the urethra and ureter principal targets: the myenteric and submucosal ganglia (causing inhi- but their role at other sites is less certain (Drumm et al 2014). bition), blood vessels (inducing vasoconstriction) and sphincter muscle (inducing contraction). Serosa and adventitia Visceral sensory endings are distributed throughout the layers of the gut wall. They respond to various stimuli, including excessive muscular A layer of connective tissue, of variable thickness, lies external to the contraction or distension, ischaemia and inflammation; their cell muscularis externa. In many places, it contains adipose tissue. Where bodies are located in the nodose ganglion of the vagus nerve (vagal the gut is covered by visceral peritoneum, the external layer is a serosa, afferents) and in thoracic and lumbosacral dorsal root ganglia (visceral consisting of mesothelium overlying a thin layer of connective tissue. afferents, which run with sympathetic efferents). Their central projec- In extraperitoneal regions, the surfaces of the gut in contact with the tions reach the brainstem and spinal cord, respectively. Vagal afferents peritoneum are covered by serosa, while other parts are covered by con- are more numerous in the foregut than the midgut and are concerned nective tissue that blends with the surrounding fasciae and is referred with physiological responses such as satiety, whereas pain and discom- to as an adventitia. fort are mediated by spinal pathways. Vascular plexuses Intrinsic innervation The intrinsic innervation of the gut is derived from enteric neurones Vascular plexuses are present at various levels of the wall, especially in distributed throughout its wall in thousands of small ganglia, each the submucosa and mucosa; they connect with vessels that supply the consisting of neuronal cell bodies supported by enteric glial cells; it is surrounding tissues or those entering through the mesentery, and estimated that there are between 200 and 600 million neurones in the accompany the ducts of outlying glands. human enteric nervous system. Enteric neurones are derived from neural crest cells. The enteric nervous system innervates the gut from Innervation oesophagus to anus, together with the pancreas and biliary tree. The majority of enteric neurones in the wall of the gut are found in The gut wall is densely innervated by both the enteric nervous system two ganglionated plexuses (Fig. 59.10). The most extensive of these is (intrinsic control) and the autonomic nervous system (extrinsic control). the myenteric (Auerbach’s) plexus, which consists of a network of nerve Myenteric plexus Circular muscle Longitudinal muscle Deep muscular plexus Inner SMP Outer SMP Submucosal artery Mucosa Muscularis mucosae Fig . 59 .10 The organization of the enteric nervous system in the human small intestine . There are two ganglionated plexuses: the myenteric plexus between the longitudinal and circular layers of the external musculature, and the submucosal plexus (SMP), which has outer and inner components . Nerve fibre bundles connect the ganglia and form plexuses innervating the longitudinal muscle, circular muscle, muscularis mucosae, intrinsic arteries and the mucosa . Axons of extrinsic origin also run in these nerve fibre bundles . There are also innervations of gastroenteropancreatic (GEP) endocrine cells and gut-associated lymphoid tissue (GALT), which are not shown here . (Redrawn with permission from Furness JB . The enteric nervous system and neurogastroenterology . Nat Rev Gastroenterol Hepatol 2012;9:286–294 . Reprinted with permission from Nature Publishing Group .)
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AbdOmEN ANd PElvIS: OvErvIEw ANd SurfACE ANATOmy 1044 8 NOITCES fibres and small ganglia lying between the circular and longitudinal mesenteric and splenic veins behind the neck of the pancreas); the layers of the muscularis externa. It runs in continuity from the oesopha- hilum of the left kidney (the hilum of the right kidney is slightly lower); gus to the anus. The submucosal (Meissner’s) plexus has outer and the origin of the renal arteries; the level of the duodenojejunal flexure inner components, and is present throughout the intestine but absent (Mirjalili 2012b); and the termination of the spinal cord. The pylorus or minimal in the oesophagus and stomach. may be found in the transpyloric plane but is not a constant feature. Interconnecting, non-ganglionated nerve plexuses lie at various The subcostal plane is defined by a line that joins the lowest point levels in the wall of the gut, including the lamina propria (mucosal of the costal margin on each side (usually, the tenth costal cartilage); it plexus), at the interface between the submucosa and muscularis externa, is most commonly at the level of the second lumbar vertebra (range between the circular and longitudinal muscles (the non-ganglionated T12/L1 disc to upper L3) (Mirjalili et al 2012a). part of the myenteric plexus), and within the serosa. The supracristal plane joins the highest point of the iliac crest on Individual enteric neurones function in one of several ways: as affer- each side. It serves as a useful landmark when performing a lumbar ent (sensory) nerves responding to mechanical and chemical stimuli; puncture or spinal injection, and usually lies at the level of the L4 body as efferent (motor) nerves innervating epithelial cells (influencing or L4/5 disc and its spinous process (see Fig. 78.16). The bifurcation of absorption, secretion and/or the release of hormones), smooth muscle the abdominal aorta lies approximately in this plane (Mirjalili et al (excitatory or inhibitory), arterioles (vasoconstriction or vasodilation) 2012a). and lymphoid tissue; or as interneurones that relay and integrate The transtubercular plane joins the tubercles of the iliac crests and signals. Collectively, they are involved in a hierarchy of enteric reflexes is traditionally reported to lie at the level of the body of L5, near its that include local reflexes within the gut wall; reflexes mediated through upper border. It is an approximate landmark for the origin of the infe- prevertebral sympathetic ganglia; and reflexes mediated through the rior vena cava from the confluence of the common iliac veins. central nervous system (the gut–brain axis). The functions of enteric The plane of the pubic crest is in line with the upper border of the neurones may be further modulated by local environmental factors, e.g. pubic symphysis. In supine individuals, this plane frequently intersects enteric glia, gut microbiota and feeding state, and by general factors in the tip of the coccyx and the femoral head (Mirjalili et al 2012a), but the host, e.g. the immune system, stress and disease (Brierley and there are variations relating to the degree of lumbar lordosis, sacral Linden 2014). Pathological states become manifest by abnormal secre- inclination and pelvic tilt. tion, impaired absorption, disordered gastrointestinal motility and Abdominal regions pain. The abdomen can be divided into nine regions using the subcostal, transtubercular and two paramedian planes (Fig. 59.11A). These regions SURFACE ANATOMY OF THE ABDOMEN are used in clinical practice for descriptive localization of a patient’s AND PELVIS pain or tenderness, or the position of a mass, and can be used to refer- ence the position of abdominal viscera. From superior to inferior, the ABDOMINAL PLANES AND REGIONS nine regions are: the epigastrium, flanked by the right and left hypo- chondrium; the umbilical, or central, flanked by the right and left lumbar; and the suprapubic or hypogastrium, flanked by the right and For descriptive purposes, the abdomen can be divided into regions left iliac fossae. In practice, these regions are often loosely defined using a combination of horizontal and vertical planes that are based without strict reference to their boundaries. An alternative system of on skeletal landmarks. Published descriptions of surface anatomy description involves dividing the abdomen into quadrants using the largely apply to adults, in whom attempts have been made to validate median plane and a horizontal line passing through the umbilicus. or update standard descriptions using cross-sectional imaging. The extent to which many of these surface projections can be extrapolated to children is uncertain; some differences are inevitable, particularly in ANTERIOR ABDOMINAL WALL infants, given their different visceral and body proportions (Stringer 2011). In this chapter, descriptions of the surface projections of abdomi- Skeletal landmarks nal structures refer to the most commonly encountered arrangement The superior boundary of the anterior abdominal wall is formed by seen in adults. However, it is important to note that there is consider- several clear landmarks (Fig. 59.11B). The xiphoid process is palpable able individual variation in surface anatomy, compounded further by at the inferior sternum, in the midline. From here, the costal margins potential variations related to age, sex, posture, respiration, body mass can be felt passing inferolaterally from the seventh costal cartilage at the and ethnicity (Mirjalili and Stringer 2012). xiphisternal joint to the tip of the twelfth rib (the latter is often difficult Vertical lines and planes to feel in the obese or if it is short). The lower border of the ninth costal The midline (or median plane) passes through the xiphoid process and cartilage can usually be defined as a distinct ‘step’ along the costal the pubic symphysis. There are two paramedian lines, left and right, margin. The lowest part of the costal margin lies in the mid-axillary line that extend from the mid-clavicular point to the mid-inguinal point, a and is formed by the inferior margin of the tenth costal cartilage. point midway between the anterior superior iliac spine and the pubic The inferior boundary of the anterior abdominal wall is formed, symphysis (Fig. 59.11A); this line crosses the costal margin just lateral from lateral to medial, by the iliac crest, which descends to the anterior to the tip of the ninth costal cartilage. In the upper abdomen, it approxi- superior iliac spine; the inguinal ligament, which runs obliquely down- mates to the lateral border of rectus abdominis. wards to the pubic tubercle; and the pubic crest, which extends from the pubic tubercle laterally to the pubic symphysis in the midline. The Horizontal lines and planes pubic tubercle is palpable on the anterosuperior surface of the pubic Several horizontal reference planes have been defined but, with modern bone approximately 2 cm lateral to the midline. The prominent tendon cross-sectional imaging, their clinical utility for positioning abdominal of adductor longus (best felt with the hip flexed, abducted and exter- viscera has become limited. Nevertheless, they help to conceptualize nally rotated) attaches to the pubis directly below the pubic tubercle, the relative positions of abdominal viscera with respect to vertebral and can therefore be used to verify its position. levels and bony surface landmarks. The posterolateral boundary of the anterior abdominal wall is the The xiphisternal joint most often lies in the same horizontal (axial) mid-axillary line. plane as the T9 vertebra (Mirjalili et al 2012b). Soft tissue landmarks The transpyloric plane lies midway between the suprasternal notch of the manubrium and the upper border of the pubic symphysis. This umbilicus corresponds to a plane that is approximately midway between the The umbilicus is an obvious but inconstant landmark. In the supine xiphisternal joint and the umbilicus, or slightly below (Mirjalili et al adult, it usually lies around the L4 level (range L2/3 disc to upper S1) 2012a). Posteriorly, the plane intersects the lower half of the body of (Mirjalili et al 2012b). The umbilicus may lie at a lower level in the the first lumbar vertebra, the L1/2 intervertebral disc, or the upper half erect position, and in children, the obese and in individuals with a of the body of the second lumbar vertebra in most individuals (range pendulous abdomen. lower T12 to lower L2); it sits higher in males (lower L1–L1/2) than females (lower L2) (Mirjalili et al 2012a). Anteriorly, it intersects the rectus abdominis costal margin at the ninth costal cartilage, where the linea semilunaris In a thin, muscular individual, the tendinous intersections of rectus crosses, and where a distinct ‘step’ may be palpable in the rib margin. abdominis may be visible, especially when the muscle is tensed by The following structures lie approximately within the transpyloric plane lifting the head against resistance or by sitting up; the intersections are (Mirjalili et al 2012a, 2012b): the origin of the superior mesenteric usually situated at the level of the umbilicus, the level of the xiphoid artery; the origin of the portal vein (from the confluence of the superior process and midway between these two points (Fig. 59.11B).
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Surface anatomy of the abdomen and pelvis 1045 95 rETPAHC A B 10 10 1 2 3 1 2 3 4 D1 5 D2 D4 6 11 D3 7 4 5 6 8 9 10 12 7 8 9 C T11 T12 1 L1 L2 L3 2 L4 L5 Fig . 59 .11 A, Nine regions of the anterior abdominal wall . Key: 1, right hypochondrium; 2, epigastrium; 3, left hypochondrium; 4, right lumbar; 5, umbilical/central; 6, left lumbar; 7, right iliac fossa; 8, suprapubic/hypogastrium; 9, left iliac fossa; 10, paramedian line; 11, subcostal plane; 12, transtubercular plane . B, The surface projection of the abdominal viscera . Key: 1, diaphragm position: right dome level with fifth intercostal space and left dome with sixth rib; 2, liver: mapped between three points: right fifth rib/intercostal space mid-clavicular line, left fifth intercostal space/sixth rib mid-clavicular line and right tenth costal cartilage mid-axillary line; 3, zone of gastro-oesophageal junction position (white): mainly located posterior to left seventh costal cartilage, at approximately T11; 4, transpyloric plane; 5, zone of gallbladder fundus position (white); 6, duodenum: four parts marked D1–D4; 7, linea semilunaris; 8, position of small intestine mesentery; 9, linea alba; 10, tendinous intersection of rectus abdominis . C, The surface position of the spleen and kidneys . Key: 1, spleen; sits deep to ribs 10–12 with long axis aligned with rib 11; 2, supracristal plane . (C, Derived with permission from Mirjalili SA, McFadden SL, Buckenham T, Stringer MD . 2012b A reappraisal of adult abdominal surface anatomy . Clin Anat 25:844–50 .) linea alba Inferior epigastric artery The linea alba is usually only visible in thin, muscular individuals. It is The inferior epigastric artery lies along the medial border of the deep wider and more obvious above the umbilicus, and is almost linear and inguinal ring immediately above the inguinal ligament. Up to the level less visible below this level (Ch. 61) (Fig. 59.11B; see Fig. 61.2). of the umbilicus, it follows a course that lies approximately 40% of the distance between the midline and a sagittal plane running through the linea semilunaris anterior superior iliac spine (Epstein et al 2004). The surface anatomy The linea semilunaris lies along the lateral margin of the rectus sheath of the artery is particularly important in laparoscopic surgery because and is visible as a shallow, curved groove in muscular individuals, par- trocar insertion may injure the vessel, causing a rectus sheath hae- ticularly when the abdominal muscles are tensed, e.g. by sitting up from matoma or intra-abdominal bleeding. The artery can be avoided if a the lying position (Fig. 59.11B). It passes from the ninth costal cartilage trocar is inserted at least two-thirds of the distance along a horizontal to the pubic tubercle. line between the midline and a sagittal plane passing through the ante- rior superior iliac spine. mid-inguinal point Superficial reflexes The mid-inguinal point lies at the midpoint of a line between the pubic symphysis and the anterior superior iliac spine. In adults, it is the Cremasteric reflex approximate surface marking of the femoral artery (just below the liga- Stroking the skin of the medial side of the thigh evokes a reflex con- ment) and the deep inguinal ring (just above the ligament) (Hale et al traction of cremaster, which elevates the ipsilateral testis. The reflex is 2010). mediated by the genitofemoral nerve (L1 and L2 nerve roots), although
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AbdOmEN ANd PElvIS: OvErvIEw ANd SurfACE ANATOmy 1046 8 NOITCES the afferent arc of the reflex may be via sensory fibres in the ilioinguinal line to the left fifth intercostal space/sixth rib in the mid-clavicular line, nerve. The reflex is usually absent if there is torsion of the testicle. and can be mapped with the contour of the diaphragm (Mirjalili et al 2012c). This border curves slightly downwards at its centre and crosses Superficial abdominal reflex the midline behind the xiphisternal joint. The right border of the liver Gently stroking each of the four quadrants of the anterior abdominal is curved to the right and joins the upper and lower right limits. The wall normally elicits a visible contraction of ipsilateral abdominal upper border of the liver may be defined by dullness to percussion when muscles. The reflex can be used to help localize lesions in the spinal compared with the resonance of the lungs above. cord but is now of minor clinical significance because of the availability of neuroimaging and the difficulties of eliciting the reflex in multipa- Gallbladder rous women, the elderly and the obese (Gosavi and Lo 2014). The fundus of the gallbladder is commonly identified with the tip of the ninth costal cartilage (in the transpyloric plane), near the junction of the linea semilunaris with the costal margin (see Fig. 59.11B). Recent INTRA-ABDOMINAL VISCERA data have shown that the fundus lies in the transpyloric plane in approximately one-third of supine individuals and below the plane in The surface markings of the intra-abdominal viscera are variable and most others (Mirjalili et al 2012b). depend on age, sex, body habitus, nutritional state, phase of ventilation and body position. The availability of cross-sectional and ultrasound Spleen medical imaging of the abdominal viscera has led to a decline in the use The spleen is traditionally described as sitting on the left posterolateral of surface anatomy, except for descriptive purposes. The following abdominal wall deep to ribs 9–11. Recent data show that the spleen sits descriptions are, at best, regarded as the most common or approximate deep to ribs 10–12 in 50% of subjects and deep to ribs 9–11 in 25% of markings in a healthy supine adult (Fig. 59.11B,C). The spinous proc- supine individuals; its long axis corresponds most closely to the elev- esses of the lumbar vertebrae can be used to locate vertebral levels, with enth rib or tenth rib, respectively, and passes anterior to the mid-axillary the lower part of the spinous process marking the level of the interverte- line in most subjects (Mirjalili et al 2012b) (see Fig. 59.11C). The spleen bral disc below the correspondingly numbered vertebra. extends from a point about 5 cm to the left of the posterior midline at the level of the eleventh thoracic spine and extends about 3 cm anterior Diaphragm to the mid-axillary line. Its normal size approximates roughly to that In the supine position at end-tidal inspiration, the dome of the dia- of the individual’s clenched fist. phragm is most frequently located level with the fifth intercostal space in the mid-clavicular line on the right and the sixth rib in the mid- clavicular line on the left, and ranges from the fourth intercostal space RETROPERITONEAL VISCERA to below the costal margin (Mirjalili et al 2012c) (see Fig. 59.11B) (see Ch. 55 for further discussion of the diaphragm). These levels are The surface projections of the retroperitoneal viscera are reasonably approximate, not only because of individual variation but also because reliable but have limited clinical utility since most interventions and diaphragmatic excursion in the erect position during quiet breathing is procedures are guided by medical imaging. about 2 cm and increases to about 7 cm during deep breathing (Bous- suges et al 2009). The dome of the diaphragm can reach as high as the Pancreas fourth rib on maximal expiration. The surface projection of the head of the pancreas lies within the duo- Stomach denal curve on the right side of the second lumbar vertebra; the neck lies in the transpyloric plane, level with the L1/2 intervertebral disc; and The gastro-oesophageal junction lies to the left of the midline, posterior the body passes obliquely up and to the left towards the spleen, lying to the left seventh costal cartilage, at the level of the eleventh thoracic slightly above the transpyloric plane, near the tail. vertebra (range upper T10 to L1/2), with the level being lower in females and higher in the obese (Mirjalili et al 2012b) (see Fig. 59.11B). The Kidney stomach lies in a curve within the left hypochondrium and epigastrium, The right kidney usually lies, on average, 2 cm lower than the left, although, when distended, it may lie as far down as the umbilical or although, in 10% of cases, the left kidney sits lower than the right suprapubic regions. The epigastrium is the usual place to auscultate for (Mirjalili et al 2012b). The vertebral limits of the left kidney are T12– a ‘succussion splash’ caused by gastric outlet obstruction or stasis, and L3 or L4, while those for the right kidney are L1–L4 (overall range is also the region where a thickened pylorus is palpable in infantile upper T11 to lower L5) (see Fig. 59.11C). The upper poles of both hypertrophic pyloric stenosis. kidneys lie anterior to rib 12, and they lie anterior to the rib 11 in 30% Duodenum (left) and 10% (right) of subjects. In supine adults at end-tidal inspira- The first part of the duodenum sometimes ascends above the transpy- tion, the centre of the renal hilum usually lies at L1/2 or L2 on the left loric plane; the second part usually lies just to the right of the midline, and at a slightly lower vertebral level on the right. It is important to alongside the second and third lumbar vertebrae; the third part usually note that both kidneys move vertically by a mean of about 2 cm during crosses the midline at the level of the third lumbar vertebra; and the deep respiration and both can descend by several centimetres when fourth part ascends to the left of the second lumbar vertebra, reaching moving from lying to standing (Schwartz et al 1994, Reiff et al 1999). the transpyloric plane in the region of the lower border of the first The length of the normal adult kidney, measured along its long axis, lumbar vertebra (see Fig. 59.11B). The duodenojejunal flexure com- is approximately 11.5 cm in men and 11.0 cm in women (Hale et al monly sits at L1 (range lower T11 to upper L3) (Mirjalili et al 2012b). 2010); the left kidney is a few millimetres longer than the right (Cheong et al 2007, Glodny et al 2009, Mirjalili et al 2012b). There is a small Small intestine and its mesentery reduction in renal length beyond 50 years of age (Glodny et al 2009). The small intestine mesentery runs obliquely in a line from a point just Each kidney is approximately 5–6 cm wide. Both its longitudinal and to the left of the lower border of the first lumbar vertebra (in the transverse axes are slightly oblique, such that the upper pole of each transpyloric plane) towards the right iliac fossa. kidney is nearer the midline and the hilum is more anterior than the lateral surface. The centre of the hilum is approximately 5–6 cm from Appendix the midline. The appendix is located in the right lower quadrant of the abdomen The lower pole of the normal right kidney may occasionally be felt but is highly variable in its length and position. Studies analysing in thin individuals by bimanual palpation via the renal angle on full barium enemas in supine adults have shown the position of appendix inspiration. base is variably located and rarely precisely at McBurney’s point (a point two-thirds of the way along a line joining the anterior superior iliac Ureter spine to the umbilicus) (Ramsden et al 1993, Naraynsingh et al 2002). The ureter descends on either side from approximately the level of the transpyloric plane, slightly lower on the right, about 5 cm from the Liver midline. Each passes downwards just medial to the tips of the transverse At the end of normal tidal inspiration, the inferior border of the liver processes of the lumbar vertebrae. In the pelvic cavity, each ureter curves extends along a line that passes from the right tenth costal cartilage in medially to enter the base of the bladder. the mid-axillary line to the left fifth intercostal space/sixth rib in the mid-clavicular line (see Fig. 59.11B). It may be palpable in healthy adults Abdominal aorta and branches on deep inspiration. The superior border of the liver follows a line that The abdominal aorta begins at the level of the body of the twelfth passes from the right fifth rib or intercostal space in the mid-clavicular thoracic vertebra near the midline. It descends and bifurcates at
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1047 95 rETPAHC Key references approximately L4 (range lower L3 to lower L5), usually just to the left allows access to the peritoneum at a point where there is relatively little of the midline and up to 3 cm caudal to the umbilicus (Mirjalili et al extraperitoneal fat. Additional working ports are inserted through the 2012b). The position of the aortic bifurcation is shifted slightly proxi- anterior abdominal wall, avoiding major vessels such as the inferior mally with a greater degree of lumbar lordosis (Moussallem et al 2012). epigastric artery. The pulsations of the aorta can be felt in a thin, supine individual by Surgical incisions pressing firmly in the midline backwards on to the lower lumbar spine. An easily palpable aorta in an obese person should raise the suspicion Most surgical incisions are sited according to surgical imperatives rather of an aneurysm. than anatomical constraints. Access to the peritoneal cavity is gained by dividing or splitting muscles. Common approaches include the midline unpaired visceral arteries incision through the relatively avascular linea alba, the transverse The coeliac trunk arises from the aorta immediately after it enters the suprapubic (Pfannenstiel) incision for pelvic procedures, and, in infants abdomen at T12; the superior mesenteric artery arises most commonly and children, the upper abdominal transverse incision. In recent years, at L1, close to the transpyloric plane; and the inferior mesenteric artery progressively more abdominal surgery has been performed using usually arises at L3 (Mirjalili et al 2012b). laparo scopic procedures (minimally invasive or ‘keyhole’ surgery). renal arteries Intestinal stomas (ileostomy, colostomy) The renal arteries most commonly arise from between lower L1 and When possible, intestinal stomas are usually formed through transrec- upper L2, with the lower border of L1 (approximately, the transpyloric tus incisions. A cruciate incision is made in the anterior rectus sheath plane) being most common on both sides (Mirjalili et al 2012b). and the muscle fibres are split, avoiding injury to the epigastric vessels. This incision offers the advantage that fibres of rectus abdominis Iliac arteries support the stoma, providing a dynamic, contractile surround that The surface projection of the common iliac artery corresponds to the tends to reduce the risk of herniation occurring around the stoma. superior third of a broad line, which is slightly convex laterally, from the aortic bifurcation (see above) to a point midway between the ante- Suprapubic catheterization rior superior iliac spine and the pubic symphysis. The external iliac The urinary bladder may be accessed for short- or long-term catheteriza- artery corresponds to the inferior two-thirds of this line. tion through the anterior abdominal wall. As the bladder fills, the upper Inferior vena cava part of its dome comes to lie in the preperitoneal ‘space’ in the suprapu- bic region, where it can be relatively easily accessed by a midline trans- The inferior vena cava most commonly forms at L5 in the transtuber- cutaneous puncture through the linea alba. cular plane (range upper L4 to upper S1) approximately to the right of the midline (Mirjalili et al 2012b). The inferior vena cava leaves the Endoscopic surgery abdomen by traversing the diaphragm at the level of the eleventh tho- Endoscopic surgery is a broad term that encompasses all types of racic vertebra. surgery that are performed using flexible or rigid fibreoptic endoscopes inserted through natural body orifices or small surgical incisions. It PELVIS overlaps with the field of minimally invasive surgery. The aim is to minimize or eliminate external incisions and hasten the patient’s The posterior superior iliac spines lie at the level of the second sacral recovery, whilst providing optimum treatment of the pathology with segment (McGaugh et al 2007); some individuals have an overlying an acceptably low risk of complications. In the abdomen and pelvis, sacral dimple. This palpable bony landmark corresponds approximately therefore, it includes therapeutic procedures performed using an endo- to the termination of the dural sac (Senoglu et al 2013) and the middle scope inserted via the mouth (gastroscope or duodenoscope), anus of the sacroiliac joint. The second dorsal sacral foramina lies approxi- (proctoscope, sigmoidoscope or colonoscope), urethra (cystoscope or mately 2–3 cm medial to the posterior superior iliac spine on each side ureteroscope) or vagina, or via small surgical incisions in the anterior at an angle of 45° (McGrath and Stringer 2011). The latter is potentially or posterior abdominal wall (laparoscope and other endoscopic useful when localizing the branches of the dorsal sacral rami in the systems). treatment of refractory sacroiliac pain. A refinement of the technique is natural orifice transluminal endo- scopic surgery, in which abdominal operations are performed using an Sciatic nerve endoscope inserted through a natural orifice (e.g. mouth, anus, urethra) The sciatic nerve leaves the pelvis approximately one-third of the and then through an incision in the viscus that has been entered (e.g. way along a line between the posterior superior iliac spine and stomach, bladder, vagina). For example, pelvic and intra-abdominal the ischial tuberosity and enters the thigh approximately half way contents can be accessed through the vagina via the recto-uterine pouch. between the greater trochanter and ischial tuberosity (see Fig. 78.16) Hysterectomy, oophorectomy, pelvic organ prolapse repair and incon- (Currin et al 2014). tinence surgery are commonly performed using transvaginal techniques. Other surface landmarks for pelvic structures are described in This approach avoids the morbidity of abdominal incision but there Chapter 78. are risks of sciatic, femoral and common fibular nerve injury from prolonged surgery in the lithotomy position. A further development of endoscopic minimally invasive surgery has COMMON CLINICAL PROCEDURES been the introduction of robotically assisted surgery, which allows the surgeon to manipulate precision instruments from a console that is Pneumoperitoneum for laparoscopy remote from the patient whilst viewing the operative field in three A pneumoperitoneum is frequently established by accessing the perito- dimensions. The procedure is becoming increasingly common in neal cavity just below the umbilicus. An incision through the linea alba prostatectomy. KEY REFERENCES Furness JB, Callaghan BP, Rivera LR et al 2014 The enteric nervous system Mirjalili SA, Stringer MD 2012 The need for an evidence-based reappraisal and gastrointestinal innervation: integrated local and central control. of surface anatomy. Clin Anat 25:816–18. Adv Exp Med Biol 817:39–71. This issue of Clinical Anatomy features several original articles A comprehensive review of gastrointestinal innervation and the complexities reappraising surface anatomy of the trunk using cross-sectional CT imaging of the enteric nervous system. in supine adults. These articles provide a more evidence-based approach to key surface anatomy landmarks in the chest, abdomen and pelvis. Loukas M, Klaassen Z, Merbs W et al 2010 A review of the thoracic splanch- nic nerves and celiac ganglia. Clin Anat 23:512–22. A critical review of the thoracic splanchnic nerves.
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Abdomen and pelvis: overview and surface anatomy 1047.e1 95 rETPAHC REFERENCES Al-Shboul OA 2013 The importance of interstitial cells of Cajal in the gas- Mirjalili SA, McFadden SL, Buckenham T et al 2012a Anatomical planes: are trointestinal tract. Saudi J Gastroenterol 19:3–15. we teaching accurate surface anatomy? Clin Anat 25:819–26. Azaïs H, Collinet P, Delmas V et al 2013 Uterosacral ligament and hypogas- Mirjalili SA, McFadden SL, Buckenham T et al 2012b A reappraisal of adult tric nerve anatomical relationship. Application to deep endometriotic abdominal surface anatomy. Clin Anat 25:844–50. nodules surgery. Gynecol Obstet Fertil 41:179–83. Mirjalili S, Hale S, Buckenham T et al 2012c A reappraisal of adult thoracic Blaszczyk B 1981 Variation of ganglia of the pelvic segment of the sympa- surface anatomy. Clin Anat 25:827–34. thetic trunk in human fetuses. Folia Morphol (Warsz) 39:313–26. Motoc A, Rusu MC, Jianu AM 2010 The spermatic ganglion in humans: an Boussuges A, Gole Y, Blanc P 2009 Diaphragmatic motion studied by anatomical update. Rom J Morphol Embryol 51:719–23. m-mode ultrasonography: methods, reproducibility, and normal values. Moussallem CD, Abou Hamad I, El-Yahchouchi CA et al 2012 Relationship Chest 135:391–400. of the lumbar lordosis angle to the abdominal aortic bifurcation and Brierley SM, Linden DR 2014 Neuroplasticity and dysfunction after gastro- inferior vena cava confluence levels. Clin Anat 25:866–71. intestinal inflammation. Nat Rev Gastroenterol Hepatol 11:611–27. Murata Y, Takahashi K, Yamagata M et al 2003 Variations in the number and Cheong B, Muthupillai R, Rubin MF et al 2007 Normal values for renal position of human lumbar sympathetic ganglia and rami communi- length and volume as measured by magnetic resonance imaging. Clin J cantes. Clin Anat 16:108–13. Am Soc Nephrol 2:38–45. Naraynsingh V, Ramdass MJ, Singh J et al 2002 McBurney’s point: are we Currin SS, Mirjalili SA, Meikle G, Stringer MD 2014 Revisiting the surface missing it? Surg Radiol Anat 24:363–5. anatomy of the sciatic nerve in the gluteal region. Clin Anat doi: Oh CS, Chung IH, Ji HJ et al 2004 Clinical implications of topographic 10.1002/ca.22449. anatomy on the ganglion impar. Anesthesiology 101:249–50. Drumm BT, Koh SD, Andersson KE 2014 Calcium signalling in Cajal-like Paraskevas G, Tsitsopoulos P, Papaziogas B et al 2008 Variability in superior interstitial cells of the lower urinary tract. Nat Rev Urol 11:555–64. hypogastric plexus morphology and its clinical applications: a cadaveric Epstein J, Arora A, Ellis H 2004 Surface anatomy of the inferior epigastric study. Surg Radiol Anat 30:481–8. artery in relation to laparoscopic injury. Clin Anat 17:400–8. Potts TK 1925 The main peripheral connections of the human sympathetic Furness JB, Callaghan BP, Rivera LR et al 2014 The enteric nervous system nervous system. J Anat 59:129–35. and gastrointestinal innervation: integrated local and central control. Ramsden WH, Mannion RA, Simpkins KC et al 1993 Is the appendix where Adv Exp Med Biol 817:39–71. you think it is – and if not does it matter? Clin Radiol 47:100–3. A comprehensive review of gastrointestinal innervation and the complexities Reiff JE, Werner-Wasik M, Valicenti RK et al 1999 Changes in the size and of the enteric nervous system. location of kidneys from the supine to standing positions and the Glodny B, Unterholzner V, Taferner V et al 2009 Normal kidney size and its implications for block placement during total body irradiation. Int J influencing factors – a 64-slice MDCT study of 1.040 asymptomatic Radiat Oncol Biol Phys 45:447–9. patients. BMC Urol 9:1–19. Roggin KK, Posner MC 2012 Modern treatment of gastric gastrointestinal Gosavi TD, Lo YL 2014 Images in clinical medicine. Superficial abdominal stromal tumors. World J Gastroenterol 18:6720–8. reflex. N Engl J Med 370:e29. Rusu MC 2006 Considerations on the phrenic ganglia. Ann Anat Hale SJ, Mirjalili SA, Stringer MD 2010 Inconsistencies in surface anatomy: 188:85–92. the need for an evidence-based reappraisal. Clin Anat 23:922–93. Sanders KM, Ward SM, Koh SD 2014 Interstitial cells: regulators of smooth Horton KM, Fishman EK 2002 Volume-rendered 3D CT of the mesenteric muscle function. Physiol Rev 94:859–907. vasculature: normal anatomy, anatomic variants, and pathologic condi- Schwartz LH, Richaud J, Buffat L et al 1994 Kidney mobility during respira- tions. Radiographics 22:161–72. tion. Radiother Oncol 32:84–6. Loukas M, Klaassen Z, Merbs W et al 2010 A review of the thoracic splanch- Senoglu N, Senoglu M, Ozkan F et al 2008 The level of termination of the nic nerves and celiac ganglia. Clin Anat 23:512–22. dural sac by MRI and its clinical relevance in caudal epidural block in A critical review of the thoracic splanchnic nerves. adults. Surg Radiol Anat 35:579–84. Mauroy B, Demondion X, Drizenko A et al 2003 The inferior hypogastric Stringer MD 2011 Clinical anatomy of the newborn. In: Puri P (ed) Newborn plexus (pelvic plexus): its importance in neural preservation techniques. Surgery, 3rd ed. London: Hodder Arnold, pp. 29–38. Surg Radiol Anat 25:6–15. Subramanian A, Maker VK 2006 Organs of Zuckerkandl: their surgical sig- McGaugh JM, Brismee JM, Dedrick GS 2007 Comparing the anatomical nificance and a review of a century of literature. Am J Surg 192: consistency of the posterior superior iliac spine to the iliac crest as refer- 224–34. ence landmarks for the lumbopelvic spine: a retrospective radiological Toshniwal GR, Dureja GP, Prashanth SM 2007 Trans-sacrococcygeal study. Clin Anat 20:819–25. approach to ganglion impar block for management of chronic perineal McGrath MC, Stringer MD 2011 Bony landmarks in the sacral region: the pain: a prospective observational study. Pain Physician 10:661–6. posterior superior iliac spine and the second dorsal sacral foramina: a Woon JT, Perumal V, Maigne JY et al 2013 CT morphology and morpho- potential guide for sonography. Surg Radiol Anat 33:279–86. metry of the normal adult coccyx. Eur Spine J 22:863–70. Mirjalili SA, Stringer MD 2012 The need for an evidence-based reappraisal Woon JT, Stringer MD 2014 Redefining the coccygeal plexus. Clin Anat of surface anatomy. Clin Anat 25:816–18. 27:254–60. This issue of Clinical Anatomy features several original articles Zhang XM, Zhao QH, Zeng NL et al 2006 The celiac ganglia: anatomic study reappraising surface anatomy of the trunk using cross-sectional CT imaging using MRI in cadavers. Am J Roentgenol 186:1520–3. in supine adults. These articles provide a more evidence-based approach to key surface anatomy landmarks in the chest, abdomen and pelvis.
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CHAPTER Development of the peritoneal cavity, 60 gastrointestinal tract and its adnexae muscularis mucosa, the connective tissue of the submucosa, the mus­ POSTPHARYNGEAL FOREGUT cularis externa and the external connective tissue are all derived from the splanchnopleuric mesenchyme. The outer peritoneal epithelium is The primitive gut is divided by head­ and tail­folding into three main derived from the splanchnopleuric coelomic epithelium. compartments. The foregut extends from the buccopharyngeal mem­ Throughout the gut, blood vessels, lymphatics and lymph nodes brane to its continuation into the central midgut region via the cranial develop from local populations of angiogenic mesenchyme. The nerves, intestinal portal. The midgut extends between the intestinal portals and, which are distributed within the enteric and autonomic systems, are in the early embryo, is in wide communication with the yolk sac. The derived from the neural crest. There is a craniocaudal developmental hindgut extends from the caudal intestinal portal to the cloacal mem­ gradient along the gut, in that the stomach and small intestine develop brane. The cranial end of the foregut, the embryonic pharynx, is in advance of the colon. intimately associated with head and neck development (Ch. 36). The Figure 60.1 shows the fundamental relationship of the intraembry­ portion of foregut that passes dorsal to the pericardial cavity gives rise onic coelom to the developing gut. Figure 60.2 shows the gut in a stage to the respiratory diverticulum and oesophagus within the thorax (Chs 12 embryo in relation to the other developing viscera, especially the 36 and 52). Caudal to the developing diaphragm, the enteric gut is heart and liver. Figure 60.3 shows the overall development of the gut conventionally subdivided into three embryological portions: fore­, from stages 13 to 17. These diagrams should be compared. mid­ and hindgut. There are no corresponding fundamental morpho­ All regions of the gut develop from epithelial–mesenchymal inter­ logical and cytological distinctions between the three parts (Fig. 60.1), actions that are dependent on the sequential expression of a range of and so the foregut produces a portion of the duodenum, as does the basic and specific genes; on the regulation of the developmental clock, midgut, and the midgut similarly produces large intestine, as does the seen in all areas of development; and on endogenous regulatory mecha­ hindgut. The differences between the portions of the gut develop as a nisms and local environmental influences (Lebenthal 1989). Although result of interactions between the three embryonic tissue layers that give all these factors pertain to the whole range of developing tissues, local rise to the gut: namely, the endodermal inner epithelium, the thick layer differences in any one of these factors along the length of the develop­ of splanchnopleuric mesenchyme, and the outer layer of proliferating ing gut promote the differentiation of, for example, the gastric mucosa splanchnopleuric coelomic epithelium. and hepatocytes; the rotation of the midgut; and the final disposition The epithelial layer of the mucosa and connected ducts and glands of the sessile portions of the fully formed gastrointestinal tract. The are derived from the endodermal epithelium. The lamina propria and hedgehog (Hh) ligands, Shh, Ihh and Dhh are expressed in the develop­ ing gut: Shh and Ihh in the endodermal epithelium and Dhh in endothelial cells. These ligands bind to the Patched receptors (Ptch­1 and Ptch­2), which activate the transcription factor Gli3. Knockout of Shh and Ihh has been associated with oesophageal atresia, gut malrota­ tion, decreased development of the muscularis propria, enteric neurone anomalies and imperforate anus (Kolterud et al 2009). The gut is func­ tional prior to birth and able to interact with the extrauterine environ­ Pharynx ment in preterm infants. OESOPHAGUS Pericardial cavity Foregut The oesophagus can be distinguished from the stomach at stage 13 (embryo length 5 mm). It elongates during successive stages and its absolute length increases more rapidly than the embryo as a whole. Pericardioperitoneal canals Cranially, it is invested by splanchnopleuric mesenchyme posterior to the developing trachea and, more caudally, between the developing Septum transversum lungs and pericardioperitoneal canals posterior to the pericardium. Caudal to the pericardium, the terminal, pregastric segment of the Body wall, oesophagus has a short, thick, dorsal meso­oesophagus (from splanch­ somatopleuric mesenchyme Midgut nopleuric mesenchyme), while ventrally, it is enclosed in the cranial and coelomic epithelium stratum of the septum transversum mesenchyme. Each of the above is continuous caudally with its respective primitive dorsal and ventral mesogastria. Thus, the oesophagus has only limited areas related to a Epithelium of midgut, splanchnopleuric mesenchyme primary coelomic epithelium. However, it is important to note the and coelomic epithelium subsequent development of the para­oesophageal right and left pneu­ Peritoneal cavity matoenteric recesses (see Fig. 60.7), the relation of the ventral aspect of the middle third of the oesophagus to the oblique sinus of the pericar­ dium, and the relation of its lateral walls in the lower thorax to the mediastinal pleura. All the foregoing are secondary extensions from the primary coelom. Hindgut The oesophageal mucosa consists of two layers of cells by stage 15 Allantois (week 5), but the proliferation of the mucosa does not occlude the lumen at any time. The mucosa becomes ciliated at 10 weeks, and strati­ Fig. 60.1 Major epithelial populations within the early embryo. The fied squamous epithelium is present at the end of the fifth month; early gut tube is close to the notochord and neural tube dorsally. The occasionally, patches of ciliated epithelium may be present at birth. splanchnopleuric layer of the intraembryonic coelomic epithelium is in Circular muscle can be seen at stage 15 but longitudinal muscle has not contact with the foregut ventrally and laterally, with the midgut laterally, been identified until stage 21. Neuroblasts can be demonstrated in the 1048 and the hindgut ventrally and laterally. early stages; the myenteric plexuses have cholinesterase activity by
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Postpharyngeal foregut 1049 06 RETPAHC A Amniotic cavity B Atrioventricular canal Median thyroid rudiment Left atrium Pharynx Otocyst Bulbus Amniotic Pharynx cordis cavity (right Median ventricle) Lung bud thyroid Left horn rudiment Left Lung bud ventricle of sinus venosus Optic Foregut rudiment Septum Foregut Liver transversum Stomodeum, diverticulum Liver oronasal cavity Yolk duct diverticulum Hepatic Pericardial cavity trabeculae Gallbladder Left vitelline vein rudiment Yolk stalk Gallbladder rudiment Left umbilical artery Upper limb Postanal gut Upper limb bud bud Peritoneal cavity Cloacal membrane Midgut Midgut Cloacal membrane Notochord Cloaca Hindgut Allantois Hindgut Allantois Fig. 60.2 A, The digestive tube of a human embryo at stage 12, with 29 paired somites, a crown to rump length of 3.4 mm and an estimated age of 27 days. (Pharyngeal development is followed further in Figure 36.18.) B, Reconstruction of a human embryo at the end of the fourth week. The alimentary canal and its outgrowths are shown in median section. The brain is shown in outline but the spinal cord has been omitted. The heart is shown in perspective, and the left horn of the sinus venosus is cut just medial to the entrance of the common cardinal vein (see Fig. 52.8A–B). The somites are indicated in outline. 9.5 weeks and ganglion cells are differentiated by 13 weeks. It has been ous with the dorsal mesentery (mesenteron) of almost all of the remain­ suggested that the oesophagus is capable of peristalsis in the first tri­ der of the intestine, except its caudal short segment. mester. Periodic fetal swallowing can be seen on ultrasound from In human embryos of 10 mm (stages 15–16), the characteristic 16 weeks. The volume of amniotic fluid ingested increases during the gastric curvatures are already recognizable. Growth is more active along third trimester to more than 500 ml/day. Oesophageal atresia is one of the dorsal border of the viscus; its convexity markedly increases and the the more common obstructive conditions of the alimentary tract; it may rudimentary fundus appears. Because of more rapid growth along be indicated by polyhydramnios. There is evidence of maturation of the the dorsal border, the pyloric end of the stomach turns ventrally and lower oesophageal sphincter at 32 weeks, when, with the prevention of the concave lesser curvature becomes apparent (see Figs 60.3, 60.6). The free gastro­oesophageal reflex, stomach size increases (Hitchcock et al stomach is now displaced to the left of the median plane and, appar­ 1992). ently, becomes physically rotated, which means that its original right surface becomes dorsal and its left surface becomes ventral. Accordingly, Oesophagus at birth the right vagus is distributed mainly to the dorsal, and the left vagus mainly to the ventral, surfaces of the stomach. The dorsal mesogastrium increases in depth and becomes folded on itself. The ventral mesogas­ At birth, the oesophagus extends 8–10 cm from the cricoid cartilage to trium becomes more coronal than sagittal. The pancreaticoenteric the gastric cardiac orifice. It starts and ends one to two vertebrae, respec­ recess (see Fig. 60.7B(ii)), until this point usually described as a simple tively, higher than in the adult, extending from between the fourth to depression on the right side of the dorsal mesogastrium, becomes the sixth cervical vertebra to the level of the ninth thoracic vertebra (see dorsal to the stomach and excavates downwards and to the left between Fig. 14.7). Its average diameter is 5 mm and it possesses the constric­ the folded layers. It may now be termed the inferior recess of the bursa tions seen in the adult. The narrowest constriction is at its junction with omentalis. Put simply, the stomach has undergone two ‘rotations’. The the pharynx, where the inferior pharyngeal constrictor muscle functions first is 90° clockwise, viewed from the cranial end; the second is 90° to constrict the lumen; this region may be easily traumatized with clockwise, about an anteroposterior axis. The displacement, morpho­ instruments or catheters. In the neonate, the mucosa may contain scat­ logical changes and apparent ‘rotation’ of the stomach have been attrib­ tered areas of ciliated columnar epithelium but these disappear soon uted variously to its own and surrounding differential growth changes; after birth. Peristalsis along the oesophagus and at the lower oesopha­ extension of the pancreaticoenteric recess with changes in its mesen­ geal sphincter is immature at birth and results in frequent regurgitation chymal walls; and pressure, particularly that exerted by the rapidly of food in the newborn period. The pressure at the lower oesophageal growing liver. sphincter approaches that of an adult at 3–6 weeks of age. Mucosa STOMACH Mucosal and submucosal development can be seen in the eighth to At the end of the fourth and beginning of the fifth weeks, the stomach ninth weeks. No villi form in the stomach, unlike in other regions of can be recognized as a fusiform dilation cranial to the wide opening of the gut; instead, glandular pits can be seen in the body and fundus. the midgut into the yolk sac (see Figs 60.2 and 60.3). By the fifth week, These develop in the pylorus and cardia by weeks 10 and 11, when this opening has narrowed into a tubular vitelline intestinal duct, which parietal cells can be demonstrated. Although acid secretion has not soon loses its connection with the digestive tube. At this time, the been demonstrated in the fetal stomach before 32 weeks’ gestation, stomach is median in position and separated cranially from the peri­ preterm infants, from 26 weeks’ gestation onwards, are able to secrete cardium by the septum transversum (see Fig. 60.5A), which extends acid soon after birth. Intrinsic factor has been detected after 11 weeks. caudally on to the cranial side of the vitelline intestinal duct and ven­ This increases from the fourteenth to the twenty­fifth week, at which trally to the somatopleure. Dorsally, the stomach is related to the aorta time the pylorus, which contains more parietal cells than it does in the and, reflecting the presence of the pleuroperitoneal canals on each side, adult, also contains a relatively larger quantity of intrinsic factor. The is connected to the body wall by a short dorsal mesentery, the dorsal significance of the early production of intrinsic factor and the late pro­ mesogastrium (see Figs 60.5B and 60.6). The latter is directly continu­ duction of acid by the parietal cells is not known. Chief cells can be
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DEvEloPmEnT of THE PERiTonEAl CAviTy, gAsTRoinTEsTinAl TRACT AnD iTs ADnExAE 1050 8 noiTCEs Site of palatine tonsil Thymus A B Pharyngeal pouches Tubotympanic recess Inferior parathyroid Adenohypophysial pouch Ultimobranchial body Lateral thyroid Pharynx Internal carotid artery Superior parathyroid Thyroid Lung bud Pulmonary artery Groove for sinus venosus Stomach Aortic sac Oesophagus Septum transversum Dorsal pancreas Trachea Lung Umbilical vesicle stalk Gallbladder Pulmonary vein Stomach Allantois Cut ends of hepatic trabeculae Junction of yolk sac Gallbladder Dorsal pancreas and intestine Postanal gut Bile duct Urachus Mesonephric duct Umbilical vesicle stalk Urorectal cleavage line Cloacal membrane Junction of umbilical vesicle and intestine Metanephros and ureter Approximate junction of colon and ileum Mesonephric duct C Adenohypophysis Thyroid D E Aortic sac Oesophagus Trachea Oesophagus Left primary bronchus Trachea Left primary bronchus and branches Umbilical vesicle stalk Hepatic ducts Trachea Primary intestinal loop Gallbladder Stomach Oesophagus Ventral pancreas Urogenital Urachus Dorsal pancreas sinus Stomach Caecum Gallbladder Metanephros Mesonephric duct Hepatic ducts Bile duct Caecum Dorsal pancreas Ventral pancreas Fundus of stomach Pyloric atrium Bladder Hepatic ducts Body of stomach Gallbladder Mesentery Primary intestinal loop Dorsal pancreas Mesonephric duct Ureter Bile duct Ventral pancreas Metanephros Renal pelvis (cranial and caudal poles) Vermiform appendix Urachus Colon Bladder Metanephric kidney 0.2 mm Collecting tubules Ureter Mesonephric duct Fig. 60.3 The shape of the endodermal epithelium of the gut at succeeding stages. The scale is constant, illustrating the enormous growth of the gut over a 13-day period. A, Stage 13. B, Stage 14. C, Stage 15. D, Stage 16. E, Stage 17. Note the separation of the respiratory diverticulum; the elongation of the foregut and expansion of the stomach; the formation of the hepatic and pancreatic diverticula; the lengthening of the midgut loop, which protrudes into the umbilical cord; and the separation of the cloaca into enteric and allantoic portions. (Modified from O’Rahilly and Müller. Developmental Stages in Human Embryos 1987 Carnegie Institution of Washington. Pub 637.)
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Postpharyngeal foregut 1051 06 RETPAHC identified after weeks 12–13, although they cannot be demonstrated to atresia), or with anomalies of the bile duct. In 40–60% of cases, the contain pepsinogen until term. Mucous neck cells actively produce atresia is complete and pancreatic tissue fills the lumen. The condition mucus from week 16. Gastrin­producing cells have been demonstrated can be diagnosed on ultrasound examination, which reveals a typical in the antrum between 19 and 20 weeks, and gastrin levels have been double bubble appearance, caused by fluid enlarging the stomach and measured in cord blood and in the plasma at term. Cord serum con­ the proximal duodenum. Polyhydramnios is invariably present and tains gastrin levels 2–3 times higher than those in maternal serum. often is the indication for the scan. Duodenal atresia commonly occurs with other developmental defects, e.g. cardiac and skeletal anomalies, Muscularis and in Down’s syndrome. The stomach muscularis externa develops its circular layer at 8–9 weeks, DORSAL AND VENTRAL MESENTERIES when neural plexuses are developing in the body and fundus. The longitudinal muscle develops slightly later. Few studies note a time of OF THE FOREGUT appearance of the oblique layer. The pyloric musculature is thicker than the rest of the stomach; in general, the thickness of the total muscula­ The epithelium of the stomach and duodenum does not rotate relative ture of the stomach at term is reduced, compared to the adult. to its investing mesenchyme. The rotation includes the coelomic epi­ thelial walls of the pericardioperitoneal canals, which are on each side Serosa of the stomach and duodenum and form its serosa, and the elongating dorsal mesogastrium or the much shorter dorsal mesoduodenum. A ventral mesogastrium can be seen when the distance between the The serosa of the stomach is derived from the splanchnopleuric coe­ stomach and liver increases. Whereas the dorsal mesogastrium takes lomic epithelium. No part of this serosa undergoes absorption. The origin from the posterior body wall in the midline, its connection to original left side of the gastric serosa faces the greater sac; the right side the greater curvature of the stomach, which lengthens as the stomach faces the lesser sac. grows, becomes directed to the left as the stomach undergoes its first Stomach at birth rotation. With the second rotation, a portion of the dorsal mesogas­ trium now faces caudally (see Fig. 60.6). The ventral mesogastrium remains as a double layer of coelomic epithelium, which encloses mes­ The stomach exhibits fetal characteristics until just after birth, when the enchyme and forms the lesser omentum (see Fig. 60.7). initiation of pulmonary ventilation, the reflexes of coughing and swal­ Movement of the stomach is associated with an extensive lengthen­ lowing, and crying cause the ingestion of large amounts of air and ing of the dorsal mesogastrium, which becomes the greater omentum; liquid. Once postnatal swallowing has started, the stomach distends to this now, from its posterior origin, droops caudally over the small four or five times its contracted state, and shifts its position in relation intestine, then folds back anteriorly and ascends to the greater curvature to the state of expansion and contraction of the other abdominal of the stomach. The greater omentum is, therefore, composed of a fold viscera, and to the position of the body. In the neonate, the anterior containing, technically, four layers of peritoneum. The dorsal mesoduo­ surface of the stomach is generally covered by the left lobe of the liver, denum, or suspensory ligament of the duodenum, is a much thicker which extends nearly as far as the spleen (see Fig. 14.6B). Only a small structure, and it fixes the position of the duodenum when the rest of portion of the greater curvature of the stomach is visible anteriorly. The the midgut and its dorsal mesentery elongate and pass into the umbili­ capacity of the stomach is 30–35 ml in the full­term neonate, rising to cal cord. 75 ml in the second week and 100 ml by the fourth week (adult capac­ ity is, on average, 1000 ml). The mucosa and submucosa are relatively thicker than in the adult; however, the muscularis is only moderately SPECIAL GLANDS OF THE developed and peristalsis is not coordinated. At birth, gastric acid secre­ POSTPHARYNGEAL FOREGUT tion is low, which means that gastric pH is high for the first 12 postnatal hours. It falls rapidly with the onset of gastric acid secretion, usually Pancreas after the first feed. Acid secretion usually remains low for the first 10 days postnatally. Gastric emptying and transit times are delayed in the neonate. The pancreas develops from two evaginations of the foregut that fuse to form a single organ. A dorsal pancreatic bud can be seen in stage 13 embryos as a thickening of the endodermal tube that proliferates into DUODENUM the dorsal mesogastrium (see Fig. 60.3; Fig. 60.4). A ventral pancreatic bud evaginates in close proximity to the liver primordium but cannot The duodenum develops from the caudal part of the foregut and the be clearly identified until stage 14, when it appears as an evagination cranial part of the midgut. A ventral mesoduodenum, which is continu­ of the bile duct itself. At stage 16 (5 weeks), differential growth of the ous cranially with the ventral mesogastrium, is attached only to the wall of the duodenum results in movement of the ventral pancreatic foregut portion. Posteriorly, the duodenum has a thick dorsal mesoduo­ bud and the bile duct to the right side and, ultimately, to a dorsal posi­ denum, which is continuous with the dorsal mesogastrium cranially tion. It is not clear whether there is a corresponding shift of mesen­ and the dorsal mesentery of the midgut caudally. Anteriorly, the extreme chyme during this rotation. However, the ventral pancreatic bud and caudal edge of the ventral mesentery of the foregut extends on to the the bile duct rotate from a position within the ventral mesogastrium short initial segment of the duodenum. The liver arises as a diverticu­ (ventral mesoduodenum) to one in the dorsal mesogastrium (dorsal lum from the ventral surface of the duodenum at the foregut–midgut mesoduodenum), which is destined to become fixed on to the posterior junction, i.e. where the midgut is continuous with the yolk sac wall (the abdominal wall. By stage 17, the ventral and dorsal pancreatic buds cranial intestinal portal). The ventral pancreatic bud also arises from have fused, although the origin of the ventral bud from the bile duct is this diverticulum. The dorsal pancreatic bud evaginates posteriorly into still obvious. Three­dimensional reconstruction of the ventral and the dorsal mesoduodenum slightly more cranially than the hepatic dorsal pancreatic buds has confirmed that the dorsal pancreatic bud diverticulum. The rotation, differential growth, and cavitations related forms the anterior part of the head, the body and the tail of the pan­ to the developing stomach and omenta cause corresponding move­ creas, and the ventral pancreatic bud forms the posterior part of the ments in the duodenum, which forms a loop directed to the right, with head and the posterior part of the uncinate process. The ventral pan­ its original right side now adjacent to the posterior abdominal wall (see creatic bud does not form all of the uncinate process (Collins 2002a). Fig. 60.6). This shift is compounded by the migration of the bile duct The developing pancreatic ducts usually fuse in such a way that most and ventral pancreatic duct around the duodenal wall. Their origin of the dorsal duct drains into the proximal part of the ventral duct (see shifts until it reaches the medial wall of the second part of the fully Figs 60.3–60.4). The proximal portion of the dorsal duct usually per­ formed duodenum; the bile duct passes posteriorly to the duodenum sists as an accessory duct. The fusion of the ducts takes place late in and travels in the free edge of the ventral duodenum and ventral meso­ development or in the postnatal period; 85% of infants have patent gastrium. Local adherence and subsequent absorption of part of the accessory ducts, as compared to 40% of adults. Fusion may not occur duodenal serosa and the parietal peritoneum result in almost the whole in 10% of individuals, in which case separate drainage into the duode­ of the duodenum, other than a short initial segment, becoming retro­ num is maintained: so­called pancreatic divisum (pancreas divisum). peritoneal (sessile). Failure of the ventral pancreatic diverticulum to migrate will result in Duodenal atresia is a developmental defect found in 1 in 5000 live an anular pancreas, which may constrict the duodenum locally. births (Whittle 1999). It may be associated with an anular pancreas, The ventral pancreas does not always extend anterior to the superior which may compress the duodenum externally (20% of duodenal mesenteric vein but remains related to its right lateral surface. Initially,
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DEvEloPmEnT of THE PERiTonEAl CAviTy, gAsTRoinTEsTinAl TRACT AnD iTs ADnExAE 1052 8 noiTCEs A ductules, which terminate as blind­ending acini or as tubular, acinar elements. Oesophagus The ductal branching pattern and acinar structure of the pancreas are determined by the pancreatic mesenchyme. This mesenchyme gives rise to connective tissue between the ducts, which, in the fetus, appears to be important in stimulating pancreatic proliferation and maintaining the relative proportions of acinar, α and β cells during development. It also provides cell lines for smooth muscle within the pancreas. Ang­ iogenic mesenchyme invades the developing gland to produce blood and lymphatic vessels. Stomach The process of islet differentiation is divided into two phases (Collins 2002a). Phase I, characterized by proliferation of polyhormonal cells, Hepatic ducts occurs from weeks 9–15. Phase II, characterized by differentiation of monohormonal cells, is seen from week 16 onwards. The β cells, pro­ ducing insulin and amylin, differentiate first, followed by α cells, which Gallbladder Duodenum produce glucagon. The δ cells, which produce somatostatin, are seen after 30 weeks. The dorsal bud gives rise mostly to α cells, and the ventral bud to most of the pancreatic polypeptide­producing cells. The Ventral pancreatic outgrowth Dorsal pancreatic β cells develop from the duct epithelium throughout development and outgrowth into the neonatal period. Later, in weeks 10–15, some of the primitive ducts differentiate into acinar cells, in which zymogen granules or acinar cell markers can be detected at 12–16 weeks. The pancreas in the neonate has all of the normal subdivisions of the adult. The head is proportionately large in the newborn and there B Accessory duct (dorsal rudiment) Pyloric antrum is a smooth continuation between the body and the tail. The inferior Stomach border of the head of the pancreas is found at the level of the second lumbar vertebra. The body and tail pass cranially and to the left, and Biliary duct the tail is in contact with the spleen (see Fig. 14.6). Liver The liver is one of the most precocious embryonic organs and is the Cystic duct Dorsal pancreas main centre for haemopoiesis in the fetus. It develops from an endo­ dermal evagination of the foregut and from septum transversum mes­ enchyme, which is derived from the proliferating coelomic epithelium in the protocardiac region. The development of the liver is intimately related to the development of the heart. The vitelline veins, succeeded by the umbilical veins passing to the sinus venosus, are disrupted by Bile duct the enlarging septum transversum to form a hepatic plexus, the forerun­ ner of the hepatic sinusoids. (See Collins (2002b) for a detailed account Portal vein of hepatic development.) Principal duct (ventral rudiment) Early liver development Fig. 60.4 Development of the pancreas in a human embryo. A, An early As the head fold and early intraembryonic coelom form, the ventral stage, 7.5 mm embryo: lateral view. B, A later stage, 14.5 mm embryo: ventral view. parietal wall of the pericardial cavity gives rise to populations of cells termed precardiac or cardiac mesenchyme. Hepatic endoderm is induced to proliferate by this mesenchyme, although all portions of the the body of the pancreas extends into the dorsal mesoduodenum and early heart tube, truncus arteriosus, atria, ventricle, both endocardium then cranially into the dorsal mesogastrium. As the stomach rotates, and myocardium, have hepatic induction potency that is tissue­specific this portion of the dorsal mesogastrium is directed to the left, forming but not species­specific. As the heart and foregut become separated by the posterior wall of the lesser sac. The posterior layer of this portion the accumulation of the cardiac mesenchyme, the mesenchyme itself is of dorsal mesogastrium fuses with the parietal layer of the coelom wall renamed septum transversum. It is seen as a ventral mass, caudal to the (peritoneum), and the pancreas becomes mainly retroperitoneal (see heart, which passes dorsally on each side of the developing gut to join Fig. 60.7C). The region of fusion of the dorsal mesogastrium does not the mesenchyme proliferating from the walls of the pericardioperito­ extend so far left as to include the tail of the pancreas, which passes neal canals. The majority of the cells within the septum transversum into the splenorenal (lienorenal) ligament. The anterior border of the are destined to become hepatic mesenchyme. For details of the molecu­ pancreas later provides the main line of attachment for the posterior lar signalling of early hepatic development, see Lemaigre (2009). leaves of the greater omentum. In the stage 11 embryo, the location of the hepatic endoderm has been identified at the superior boundary of the rostral intestinal portal. Cellular development of the pancreas By stage 12, the hepatic endodermal primordium is directed ventrally The early specification of pancreatic endoderm involves the proximity and begins to proliferate as a diverticulum. There are two parts: a caudal of the notochord to the dorsal endoderm, which locally represses the part, which will produce the cystic duct and gallbladder; and a cranial expression of Shh transcription factor. Endoderm caudal to the pancre­ part, which forms the liver biliary system (see Fig. 60.3; Fig. 60.5A). atic region does not respond to notochordal signals. The ventral pan­ The cells start to express liver­specific molecular markers and glycogen creatic endoderm does not seem to undergo the same induction. storage. Pancreatic mesenchyme is derived from two regions. The mesenchyme Around the cranial portion of the hepatic diverticulum, the basal that surrounds the dorsal pancreatic bud proliferates from the splanch­ lamina is progressively disrupted and individual epithelial cells migrate nopleuric coelomic epithelium of the medial walls of the pericardio­ into the surrounding septum transversum mesenchyme. The previously peritoneal canals, whereas the ventral pancreatic bud is invested by smooth contour of the diverticulum merges into columnar extensions septum transversum mesenchyme and by mesenchyme derived from of endoderm, the epithelial trabeculae, which stimulate the hepatic the lower ventral walls of the pericardioperitoneal canals. mesenchymal cells to form blood islands and endothelium. The The primitive endodermal ductal epithelium provides the stem cell advance of the endodermal epithelial cells promotes the conversion of population for all the secretory cells of the pancreas. Initially, these progressively more hepatic mesenchyme into endothelium and blood endocrine cells are located in the duct walls or in buds developing from cells, and only a little remains to form the scanty liver capsule and them; later, they accumulate in pancreatic islets. The remaining primi­ interlobular connective tissue. This invasion by the hepatic epithelium tive duct cells will differentiate into definitive ductal cells. In the fetus, is completed in stage 13, when it approaches the caudal surface of the they develop microvilli and cilia but lack the lateral interdigitations pericardial cavity, and is separated from it only by a thin lamina of seen in the adult. Branches of the main duct become interlobular mesenchyme that will give rise to part of the diaphragm.
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Postpharyngeal foregut 1053 06 RETPAHC A Cranial B Foregut Pericardial cavity Oesophagus Lung Lungs Dorsal mesogastrium Septum transversum Pericardio- Ventral mesogastrium peritoneal canals Dorsal aorta Liver developing within Hepatic trabeculae septum transversum Spleen Putative common bile duct Gallbladder Biliary duct system Dorsal Fig. 60.5 Early development of the liver and the supra-umbilical peritoneal cavities. A, The hepatic endodermal primordium proliferates ventrally into Ventral the septum transversum mesenchyme. The endodermal cells forming the hepatic trabeculae will become hepatocytes; the septum transversum mesenchymal cells will become the endothelium of the liver sinusoids and early blood cells. The developing lung buds can be seen expanding C Oesophagus Stomach into the pericardioperitoneal cavities. B, The septum transversum Spleen mesenchyme and the stomach become enclosed by the right and left pericardioperitoneal canals (shown on transverse section). The apposition of the medial pericardioperitoneal walls forms the dorsal and ventral Developing liver mesogastria. The proximity of the lung buds to the developing stomach Ventral can be seen. The pleural and supra-umbilical peritoneal cavities are pancreatic bud transiently, and bilaterally, symmetrical above the umbilicus. C, The lower border of the ventral mesogastrium denotes the connection between the supra-umbilical peritoneal cavities: pleuroperitoneal canals, which can be Dorsal pancreatic identified by the position of the ventral pancreatic bud and common bile bud duct. The white arrows in B and C indicate the direction of movement of the dorsal and ventral mesogastria. During this early phase of development, the liver is far more highly diverticulum gives rise to the liver hepatocytes, the intrahepatic large vascularized than the rest of the gut. The hepatic capillary plexus is bile ducts (right and left hepatic ducts, segmental ducts, area ducts and connected bilaterally with the right and left vitelline veins. Dorsolater­ their first branches) and the small bile ducts (septal bile ducts, inter­ ally, they empty by multiple channels into enlarged hepatocardiac chan­ lobular ducts and bile ductules). The portal and hepatic veins arise nels, which lead to the right and left horns of the sinus venosus (see together from the vitelline veins. Early in development, the accumula­ Fig. 60.9); usually, the channel on the right side is most developed. tion of mesenchyme around these veins is similar, whereas later mes­ Both left and right channels bulge into the pericardioperitoneal canals, enchyme increases around the portal veins. This is a prerequisite for forming sites for the exchange of fluid from the coelom into the vascular bile duct development. Primitive hepatocytes surround the portal vein channels. The growth of the hepatic tissue in these regions is sometimes branches and associated mesenchyme, and form a sleeve of cells termed referred to as the left and right horns of the liver. the ductal plate. Individual cells of the ductal plate are termed cholan­ The liver remains proportionately large during its development and giocytes. Local hepatoblasts that are adjacent to the cholangiocytes constitutes a sizeable organ dorsal to the heart at stage 14, then more arrange themselves to delineate a bile duct lumen and then also switch caudally placed by stage 16. By this stage, hepatic ducts can be seen to a cholangiocyte lineage (Lemaigre 2009). As the bile ducts develop, separating the hepatic epithelium from the extrahepatic biliary system, angiogenic mesenchymal cells form blood vessels that connect to the but, even at stage 17, the ducts do not penetrate far into the liver. hepatic artery from 10 weeks. Thus, the portal triads are patterned by the portal vein radicles, which initially induce bile duct formation and Maturation of the liver then artery formation. The development of the biliary system extends At 3 months’ gestation, the liver almost fills the abdominal cavity and from the hilum to the periphery. Anomalies of the biliary tree are associ­ its left lobe is nearly as large as its right. When the haemopoietic activity ated with abnormalities of the branching pattern of the portal vein. The of the liver is assumed by the spleen and bone marrow, the left lobe developing bile ducts remain patent throughout development; the solid undergoes some degeneration and becomes smaller than the right. The stage of ductal development previously promulgated has been refuted. liver remains relatively larger than in the adult throughout the remain­ Atresia of the extrahepatic bile ducts has been noted, often in associa­ der of gestation. In the neonate, it constitutes 4% of the body weight, tion with extrahepatic atresia. The cause of this condition is not clear; compared to 2.5–3.5% in adults. It is in contact with the greater part inflammatory process may be involved, although some cases have fea­ of the diaphragm and extends below the costal margin anteriorly, and, tures of ductal plate malformation (Howard 2002). in some cases, to within 1 cm of the iliac crest posteriorly. The left lobe Development of extrahepatic biliary ducts covers much of the anterior surface of the stomach and constitutes nearly one­third of the liver (see Fig. 14.6). Although its haemopoietic The caudal part of the hepatic endodermal diverticulum forms the functions cease before birth, its enzymatic and synthetic functions are extrahepatic biliary system, the common hepatic duct, gallbladder, not completely mature at birth. Hepatocytes remain a heterogeneous cystic duct and common bile duct. population with different gene expressions and metabolic functions The bile duct, which originated from the ventral wall of the foregut within different hepatic lobule locations. This metabolic zonation (now duodenum), migrates with the ventral pancreatic bud, first to the becomes fully established after birth (Lemaigre 2009). right and then dorsomedially into the dorsal mesoduodenum. The right and left hepatic ducts arise from the cranial end of the common hepatic Development of intrahepatic biliary ducts duct from 12 weeks’ gestation. The development of the intrahepatic biliary ducts follows the branching Atresia of the extrahepatic bile ducts in neonates occurs alone or in pattern of the portal vein radicles (Collins 2002b). The cranial hepatic conjunction with a range of other anomalies, including situs inversus,
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DEvEloPmEnT of THE PERiTonEAl CAviTy, gAsTRoinTEsTinAl TRACT AnD iTs ADnExAE 1054 8 noiTCEs malrotation, polysplenia and cardiac defects. In such cases, the intra­ sure; these hernias usually resolve without treatment. Exomphalos is a hepatic bile ducts have a mature tubular shape but also show features ventral wall defect with midline herniation of the intra­abdominal of ductal plate malformation. contents into the base of the umbilical cord. Herniated viscera are In the neonate, the gallbladder has a smaller peritoneal surface than covered by the peritoneum internally and amnion externally. The in the adult, and its fundus often does not extend to the liver margin. omphalocele so formed ranges in size from a large umbilical hernia to It is generally embedded in the liver and, in some cases, may be covered a very large mass containing most of the visceral organs. Even after the by bands of liver. After the second year, the gallbladder assumes the exomphalos has been repaired, these babies will still have a deficient relative size it has in the adult. anterior abdominal wall. Gastroschisis is a para­umbilical defect of the anterior abdominal wall associated with evisceration of the abdominal organs. The organs MIDGUT are not enclosed in membranes; thus, gastroschisis can be detected by prenatal ultrasonography and differentiated from exomphalos (see Fig. 14.5B). Gastroschisis is thought to result from periumbilical ischaemia, The midgut forms the third and fourth parts of the duodenum, jejunum, caused by vascular compromise of either the umbilical vein or arteries. ileum and two­thirds of the way along the transverse colon; its develop­ The incidence of this condition appears to be increasing, especially in ment produces most of the small, and a portion of the large, intestine. babies born to young women less than 20 years old (Whittle 1999, In embryos of stages 10 and 11, it extends from the cranial to the caudal Ionescu et al 2014). intestinal portals and communicates directly with the yolk sac over its Congenital volvulus arises if the midgut loop does not rotate appro­ entire length. Although it has a dorsal wall, the lateral walls have not priately. A number of types of this condition are identified. Left­sided yet formed at these stages. By stage 12, the connection with the yolk colon occurs if the midgut loop has not rotated at all; mixed rotation sac has narrowed, such that the midgut has ventral walls cranially and results in the caecum lying inferior to the pylorus; and failure of appro­ caudally. This connection is reduced to a yolk stalk containing the vitel­ priate attachment of the peritoneum may result in the small intestine lointestinal duct during stage 13, at which time the yolk sac appears as being attached at only two points on the posterior abdominal wall. All a sphere in front of the embryo. Posterior to the midgut, the splanch­ of these arrangements lead to a risk of volvulus, which may result in nopleuric coelomic epithelia converge, forming the dorsal mesentery. necrosis of the gut. Ventrolaterally, the intraembryonic coelom is in wide communication The position and configuration of the duodenal loop are of particu­ with the extraembryonic coelom. At stage 14, the midgut has increased lar importance in children. The normal duodenal loop has a U­shaped in length more than the axial length of the embryonic body and, with configuration. The suspensory ligament of the duodenum (ligament of elongation of the dorsal mesentery, it bulges ventrally, deviating from Treitz) is usually found to the left of the body of the first or second the median plane. For all these stages, see Figure 60.3. lumbar vertebral body after normal gut rotation; any other position of this ligament may indicate some degree of gut malrotation. On barium PRIMARY INTESTINAL (OR MIDGUT) LOOP studies, the duodenojejunal flexure should, thus, lie to the left of the upper lumbar spine at the level of the pylorus. If the caecum has remained in the right upper quadrant, it may The midgut loop can first be seen at stage 15, when a bulge – the caecal become fixed in that position by peritoneal attachments passing to the bud – can be discerned on the lower limb of the loop, caudal to the right, the so­called Ladd’s bands. These may compress the underlying yolk stalk (which arises from the apex or summit of the loop). Later, duodenum and give rise to duodenal stenosis. The high positioning of the original proximal limb of the loop moves to the right and the distal the caecum close to the duodenal jejunal flexure – in some cases, in the limb to the left (see Fig. 60.3C). The longest portion of the dorsal midline – is associated with later development of volvulus. mesentery is at the level of the yolk stalk; there is less relative lengthen­ The identification of intestinal malrotation can be made by X­ray ing near the caudal end of the duodenum or the cranial half of the investigation. However, ultrasonography has the advantage of showing colon. The midgut extends into the umbilical coelom, having already the position of the superior mesenteric vein and artery. The vein should rotated through an angle of 90° (anticlockwise, viewed from the ventral lie to the right of the artery. Most cases of volvulus will show inversion aspect). This relative position is approximately maintained so long as of this normal relationship but malrotation can occur with apparently the protrusion persists, during which time the proximal limb that forms normally related vessels, particularly in malrotation with bowel obstruc­ the small intestine elongates greatly. It becomes coiled, and its adjacent tion due to Ladd’s bands and not volvulus. mesentery adopts a pleated appearance. The origin of the root of the mesentery is initially both median and vertical, while, at its intestinal attachment, it is elongated like a ruffle and folded along a horizontal UMBILICAL CORD zone. The mesenteric sheet and its contained vessels have spiralled through 90°. The distal, colic, part of the loop elongates less rapidly During the period when the midgut loop protrudes into the umbilical and has no tendency to become coiled. By the time the fetus has coelom, the edges of the ventral body wall are becoming relatively attained a length of 40 mm (10 weeks), the peritoneal cavity has closer, forming a more discrete root for the umbilical cord. Somatic enlarged and the relative size of the liver and mesonephros is much mesenchyme, which will form the ventral body wall musculature, less. The re­entry of the gut occurs rapidly and in a particular sequence, migrates into the somatopleuric mesenchyme and passes ventrally during which it continues the process of rotation. The proximal loop towards the midline. The umbilical cord forms all of the ventral body returns first, with the jejunum mainly on the left and the ileum mainly wall between the pericardial bulge and the developing external genita­ on the right of the subhepatic abdominal cavity. As they re­enter the lia. It encloses a portion of the extraembryonic coelom, the umbilical abdominal cavity, the coils of jejunum and ileum slide inwards over the coelom, into which midgut loop protrudes. When the midgut loop is right aspect of the descending mesocolon, and so displace the descend­ abruptly returned to the abdominal cavity, the more recognizable ing colon to the left. The transverse colon passes superiorly to the origin umbilical cord forms. The vitellointestinal duct and vessels involute. of the root of the mesentery (Fig. 60.6). The caecum is the last to The cranial end of the allantois becomes thinned and its lumen partially re­enter and, at first, lies on coils of ileum on the right. Later develop­ obliterated, and it forms the urachus. The mesenchymal core of the ment of the colon leads to its elongation and to the establishment of umbilical cord is derived by coalescence from somatopleuric amniotic the hepatic and splenic flexures. A timetable for intestinal rotation in mesenchyme, splanchnopleuric vitellointestinal (yolk sac) mesen­ staged human embryos is given by Kim et al (2003). chyme and splanchnopleuric allantoic (connecting stalk) mesenchyme. These various layers become fused and are gradually transformed into Anomalies of midgut rotation the viscid, mucoid, connective tissue (Wharton’s jelly) that characterizes the more mature cord. The changes in the circulatory system result in If the midgut loop fails to return to the abdominal cavity at the appro­ a large, cranially orientated, left umbilical vein (the right umbilical vein priate time, a range of ventral defects can result. Failure of obliteration regresses), and two spirally disposed umbilical arteries (see Fig. 52.19). of the vitellointestinal duct connecting the midgut to the yolk sac results in Meckel’s diverticulum. This may present as a short segment of vitel­ MATURATION OF THE SMALL INTESTINE line duct attached to the original ventral side of the ileum; it may remain attached to the umbilicus as a fistula; or it may remain as a liga­ Mucosa mentous attachment to the umbilicus. An umbilical hernia occurs when loops of gut protrude into a widened umbilical cord at term. The degree of protuberance may The exact timing of the cellular morphogenesis of the gut is difficult increase when the infant cries, which raises the intra­abdominal pres­ to establish, especially as it undergoes a proximodistal gradient in
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midgut 1055 06 RETPAHC Gut tube Oesophagus Stomach A Ventral mesogastrium Dorsal mesogastrium B Spleen Dorsal Septum transversum aorta Septum transversum Biliary duct system Umbilical vein Dorsal mesentery Yolk sac Dorsal pancreatic bud Umbilical Ventral coelom pancreatic bud Allantois Rotation Umbilical artery Midgut loop entering beginning umbilical coelom Caecum Liver Lesser Gastrosplenic C omentum ligament D Falciform ligament Splenorenal ligament Gallbladder Gallbladder Caecum Early epiploic foramen Expanding greater omentum Ventral pancreatic Colon bud Jejunum and ileum Superior mesenteric artery (axis of midgut rotation) Fig. 60.6 The major developmental sequences of the subdiaphragmatic embryonic and fetal guts, together with their associated major glands, peritoneum and mesenteries: left anterolateral aspect. A–F, The development sequence spans 1.5 months to the perinatal period. A–B, The top white arrows show the relative movements of the dorsal and ventral mesogastria that result in the longitudinal rotation of the stomach and limited entry to the lesser sac (see also Fig. 60.5). C–D, The lower white arrows associated with the midgut indicate the relative movements and rotation of the midgut loop within the umbilical coelom, and as it returns to the abdominal cavity. Continued maturation. Developmental differences between parts of the small ner’s glands are present in the duodenum from 15 weeks and the mus­ intestine or colon have not yet been correlated with age. The endoder­ cularis mucosa can be seen in the small intestine from 18 weeks. mal cells of the small intestine proliferate and form a layer some three Whereas mitotic figures are initially seen throughout the endoder­ to four cells thick, with mitotic figures throughout. From 7 weeks, blunt mal layer of the small intestine prior to villus formation, by 10–12 weeks projections of the endoderm have begun to form in the duodenum and they are limited to the intervillous regions and the developing crypts. proximal jejunum; these are the developing villi, which increase in It is believed that an ‘adult’ turnover of cells may exist when rounded­up length until, in the duodenum, the lumen becomes difficult to discern. cells can be observed at the villus tips, in position for exfoliation. The The concept of occlusion of the lumen and recanalization, which is absorptive enterocytes have microvilli at their apical borders before described in many accounts of development, does not match the cyto­ 9 weeks. An apical tubular system appears at this time, and is com­ differentiation that occurs in the gut epithelia. Thus, it is no longer posed of deep invaginations of the apical plasma membrane and thought that there is secondary recanalization of the gut lumen. By membrane­bound vesicles and tubules; many lysosomal elements 9 weeks, the duodenum, jejunum and proximal ileum have villi, and (meconium corpuscles) appear in the apical cytoplasm. These latter the remaining distal portion of ileum develops villi by 11 weeks. The features are more developed in the ileum than jejunum, are most villi are covered by a simple epithelium. Primitive crypts, epithelial prominent at 16 weeks, and diminish by 21 weeks. There are abundant downgrowths into the mesenchyme between the villi, appear between deposits of glycogen in the fetal epithelial cells, and it has been sug­ 10 and 12 weeks and similarly follow a craniocaudal progression. Brun­ gested that, prior to the appearance of hepatic glycogen, the intestinal
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DEvEloPmEnT of THE PERiTonEAl CAviTy, gAsTRoinTEsTinAl TRACT AnD iTs ADnExAE 1056 8 noiTCEs E F Duodenum is retropositioned Caecum Layers of greater omentum Arrows here indicate gut undergoing continued rotation Caecum Transverse colon G H Duodenum Root of greater omentum Spleen Transverse mesocolon Ascending Ascending colon now colon retroperitoneal Jejunoileal Transverse mesentery mesocolon Descending Descending colon now colon retroperitoneal Sigmoid mesocolon Sigmoid colon Caecum Pelvic mesocolon Fig. 60.6, cont’d The major developmental sequences of the subdiaphragmatic embryonic and fetal guts, together with their associated major glands, peritoneum and mesenteries: left anterolateral aspect. E–F, The lower white arrows associated with the midgut indicate the relative movements and rotation of the midgut loop within the umbilical coelom, and as it returns to the abdominal cavity. G–H, The approximate disposition in the adult abdomen of the gut (G) and the mesenteric roots, showing their lines of attachment and principal contained vessels (H). epithelium serves as a major glycogen store. Goblet cells are present in contains vernix and cellular debris, salivary, biliary, pancreatic and small numbers by 8 weeks, Paneth’s cells differentiate at the base of the intestinal secretions, and sloughed enterocytes. As the mixture passes crypts in weeks 11 and 12, and enteroendocrine cells appear between along the gut, water and solutes are removed and cellular debris and weeks 9 and 11. M cells (membrane or microfold cells) are present proteins concentrated. Meconium contains enzymes from the pancreas from 14 weeks. and proximal intestine in higher concentrations in preterm than in Intestinal subepithelial myofibroblasts (ISEMFs) have been described full­term babies. within the villus cores and adjacent to the intervillous space at the base of the crypts from week 21. They are arranged as a syncytium between Muscularis layer the epithelium and the muscularis mucosae, where they contribute to the extracellular matrix. They demonstrate α­smooth muscle actin (SMA) expression (McLin et al 2009). It is not clear whether these cells The muscularis layer is derived from the splanchnopleuric mesenchyme, derive from splanchnopleuric mesenchyme fibroblasts, smooth muscle as it is in other parts of the gut. Smooth muscle myoblasts are character­ precursors or neural crest. They migrate from the crypts to the villous ized by expression of α­SMA. Longitudinal muscle can be seen from axis in a manner similar to enterocytes. 12 weeks. At 26–30 weeks, the gut shows contractions without regular Meconium can be detected in the lumen of the intestine by the periodicity; from 30–33 weeks, repetitive groups of regular contractions sixteenth week. It is derived from swallowed amniotic fluid, which have been seen in preterm neonates.
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Primitive hindgut 1057 06 RETPAHC Serosa MATURATION OF THE LARGE INTESTINE The small intestine possesses only a dorsal mesentery. The movement The similarity of development of the small and large intestines is further of the root of this dorsal mesentery, and the massive lengthening of its mirrored in their cytological differentiation. Fetal gut, from 11 weeks, enteric border in order to match the longitudinal growth of the gut tube, shows dipeptidase activity in the colon as well as in the small intestine. reflect the spiralizing of the midgut loop in the umbilical coelom. Throughout preterm development, meconium corpuscles are seen in the colon and in the small intestine; they are believed to be the phago­ Small intestine at birth cytosed remains of neighbouring cells that have died as a result of programmed cell death. There is little direct evidence of colonic function in the human fetus The radial patterning of the small intestine is completed before birth, and neonate. However, the specific results of mammalian studies are with differentiation of the crypt–villous axis. Specification of the space being correlated to human studies where possible. A number of distinct between villi, crypt depth and villous length is a dynamic process and important differences between the function of adult and fetal colon dependent on the establishment of the intestinal microbiota. In the have been reported. neonate, the small intestine forms an oval­shaped mass with its greater diameter transversely orientated in the abdomen, rather than vertically Mucosa as in the adult. The mass of the small intestine inferior to the umbilicus is compressed by the urinary bladder, which is anterior at this point. The small intestine is 300–350 cm long at birth and its width, when The absorption of glucose and amino acids does not take place through empty, is 1–1.5 cm. The ratio between the length of the small and the the colonic mucosa in adult life, but there is evidence of direct absorp­ length of the large intestine at birth is similar to the adult ratio. The tion of these nutrients during development. At birth, the normal cycle mucosa and submucosa are fairly well developed and villi are present of bile acids is not mature. In the adult, bile is secreted by the liver, throughout the small intestine; however, some epithelial differentiation stored in the gallbladder and then secreted into the intestine, where it is incomplete. The muscularis is very thin, particularly the longitudinal is absorbed by the jejunum and ileum. In the fetus and neonate, the layer, and there is little elastic tissue in the wall. There are few or no transport of bile acids by an active process from the ileum does not circular folds in the small intestine, and the jejunum and ileum have occur, and so bile salts pass on into the colon. In the adult, the presence little fat in their mesentery. of bile salts in the colon stimulates the secretion of water and electrolytes, which results in diarrhoeal syndrome; however, the fetal and neonatal colon seems protected from this effect. The colon is not considered a PRIMITIVE HINDGUT site of significant nutrient absorption in the adult, and yet neonates are unable to assimilate the full lactose load of a normal breast feed from the small intestine and a large proportion of it may be absorbed from Just as the foregut has an extensive ventral endodermal diverticulum, the colon. Thus, it appears that the colon fulfils a slightly different role which contributes to a system separate from the gut, so, too, the hindgut in the preterm and neonatal period, conserving nutrient absorption and has a ventral diverticulum – the allantois – destined for a different minimizing fluid loss until the neonate has adjusted to extrauterine life, system. However, unlike the respiratory diverticulum of the foregut, the oral feeding and the establishment of the symbiotic bacterial flora. allantois is formed very early in development, prior even to formation of the embryonic endoderm and tail­folding. With the reorganization of the caudal region of the embryo at stage 10, part of the allantois is Muscularis drawn into the body cavity. The early embryonic hindgut thus consists of a dorsal tubular region extending from the caudal intestinal portal The muscularis is present and functioning by the eighth week, when to the cloacal membrane, and a ventral blind­ending allantois extend­ peristaltic waves have been observed. The specific orientation of the ing from the cloacal region into the connecting stalk. The slightly longitudinal muscle layer into taeniae coli occurs in the eleventh to dilated cavity, lined by endoderm, that cranially receives the enteric twelfth weeks, when haustra appear. The enteric nerves are present in hindgut proper and the root of the allantoenteric diverticulum is termed Meissner’s and Auerbach’s plexuses at 8 and 12 weeks, respectively; the endodermal cloaca. It is closed ventrally by the cloacal membrane there is a craniocaudal migration of neurones into the gut wall. A (endoderm opposed to proctodeal ectoderm), and it also has, tran­ normal distribution of ganglion cells has been noted in preterm babies siently, a small recess of endoderm in the root of the tail, the postanal of 24 weeks, although there is a region devoid of ganglia just above the gut. As elsewhere, the hindgut, allantois and endodermal cloaca are anal valves. Anomalous migration of neural crest cells to the gut may encased in splanchnopleuric mesenchyme. Proliferation of the mesen­ give rise to Hirschsprung’s disease (see below). Puborectalis appears in chyme and endoderm in the angle of the junction of hindgut and 20–30 mm embryos, following opening of the anal membrane. allantois produces a urorectal septum (see Fig. 72.4B). Continued pro­ liferation of the urorectal septum and elongation of the endodermal Serosa structures thrust the endodermal epithelium towards the cloacal mem­ brane, with which it fuses centrally, separating the presumptive rectum The development of the serosa of the intestine is considered with the and upper anal canal (dorsally) from the presumptive urinary bladder development of the peritoneal cavity (see below). and urogenital sinus (ventrally) (see Fig. 72.4C). The cloacal membrane is thus divided into anal (dorsal) and urogenital (ventral) membranes. The nodal centre of division is the site of the future perineal body, the Colon at birth functional centre of the perineum. In the neonate, the colon is typically 66 cm long and averages 1 cm in width. The caecum is relatively smaller than in the adult; it tapers into ENTERIC HINDGUT the vermiform appendix. The ascending colon is shorter in the neonate, reflecting the shorter lumbar region. The transverse colon is relatively The development of the large intestine, whether derived from mid­ or long, whereas the descending colon is short, but twice the length of the hindgut, seems to be similar. The proximal end of the colon can be first ascending colon (see Fig. 14.6B). The sigmoid colon may be as long as identified at stage 15, when an enlargement of a local portion of gut the transverse colon; it often touches the inferior part of the anterior on the caudal limb of the midgut loop defines the developing caecum. body wall on the left and, in about half of neonates, part of the sigmoid An evagination of the distal portion of the caecum forms the vermiform colon lies in the right iliac fossa. The muscularis, including the taeniae appendix at stage 17 (see Fig. 60.3E). Apart from the embryonic studies coli, is poorly developed in the colon, as it is in the small intestine. of Streeter (1942), there is little information about the development of Appendices, epiploicae and haustra are not present, which gives a the large intestine in humans. The early endodermal lining of the colon smooth external appearance to the colon. Haustra appear within the appears stratified, and mitoses occur throughout the layers. A series of first 6 months. The rectum is relatively long; its junction with the anal longitudinal folds arise initially at the rectum and caecum, and later in canal forms at nearly a right angle. the regions of colon between these two points. The folds segment into villi with new villi forming between. The developing mucosa invagi­ nates into the underlying mesenchyme between the villi to form glands ANAL CANAL that increase in number by splitting longitudinally from the base upwards. The villi gradually diminish in size and are absent by the time Mesenchymal proliferation occurs around the rim of the ectodermal of birth. aspect of the anal membrane, which thus comes to lie at the bottom
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DEvEloPmEnT of THE PERiTonEAl CAviTy, gAsTRoinTEsTinAl TRACT AnD iTs ADnExAE 1058 8 noiTCEs of a depression, the proctodeum (see Fig. 72.7E). With the absorption clear whether these cells migrate in from distant sources or differentiate and disappearance of the anal membrane, the anorectum communi­ from the investing mesenchyme. The endodermal epithelium overlying cates with the exterior. The lower part of the anal canal is formed from the lymphoid aggregates is often distorted into a dome shape. The cells the proctodeal ectoderm and underlying mesenchyme, but its upper within the dome are a mixed population of enterocytes, endocrine cells, part is lined by endoderm. The line of union corresponds with the goblet cells and M cells. M cells are specialized to provide a mechanism edges of the anal valves in the adult. The dual origin of the anal canal for the transport of microorganisms and intact macromolecules across is reflected in its innervation: the endodermal portion is innervated by the epithelium to the intraepithelial space and lamina propria. They autonomic nerves, and the ectodermal proctodeum is innervated by have been observed in the fetus by 17 weeks; it is believed that they are spinal nerves. formed by a specialized epithelial–mesenchymal interaction of the In the fourth and fifth weeks, a small part of the hindgut, the post­ endoderm and underlying lymphoid­type mesenchyme. anal gut, projects caudally beyond the anal membrane (see Fig. 60.3B); There are similarly specialized epithelial cells between the entero­ it usually disappears before the end of the fifth week. cytes. Intraepithelial leukocytes typically account for 15% of the epithe­ Imperforate anus is a term used to describe many different anorectal lial cells of the gut in the adult. They have been observed at 11 weeks, anomalies. The most common is anal agenesis, which is found in with a distribution of 2–3 intraepithelial leukocytes per 100 gut epithe­ almost half of all cases of imperforate anus. The condition is usually lial cells. Both T and B lymphocytes have been described in the develop­ associated with a fistula, which opens into the vulva (females) or into ing gut wall. For an account of the development of the immune cells the urethra (males). It is more rare for the anal membrane to fail to of the gut, consult Butzner and Befus (1989). The neonatal gut becomes perforate. The condition cannot reliably be diagnosed prenatally by colonized by a range of bacterial flora; some of these exist in a symbiotic ultrasound diagnosis, and it may be confused with Hirschsprung’s relationship with their host, and some of them may be considered disease (see below) and colonic atresia. The prognosis is good for low pathogenic. lesions of the anal canal. The principal concern, in all cases, is the degree of bowel control, urinary control and, in some cases, sexual ULTRASOUND ANTENATAL IMAGING OF function, which is compromised by the condition. Anorectal anomalies may be indicators of other anomalies, e.g. those forming the ‘VATER’ THE FETAL GUT syndrome (vertebral, anal, tracheo­oesophageal and renal anomalies). The abdominal circumference, routinely estimated at 20 weeks, is cal­ culated from the anteroposterior diameter and the transverse abdomi­ ENTERIC NERVOUS SYSTEM nal diameter perpendicular to it, taken at the widest part of the abdomen. The section usually includes one entire rib and the stomach Enteric neurones are derived from cranial (vagal) neural crest cells at cavity (termed stomach bubble) and can be confirmed on the left side somite levels 1–7 and from 28 onwards (see Fig. 17.19 and p. 251). of the body (see Fig 14.4G). Anteriorly, the connection of the umbilical After neurulation, the crest cells begin their ventral migration and invade cord can be confirmed (see Fig 14.4H). Anomalies of the anterior body the gut via the dorsal mesentery (see Fig. 17.11). Glial cells associated wall, exomphalos and gastroschisis, are readily detected. In exompha­ with the gut have been identified as arising from similar levels. It is los, a mass of peritoneal organs herniate through the base of the umbili­ thought that the vagal and sacral neural crest cells have intrinsic differ­ cal ring; in gastroschisis, loops of small intestine and colon float free ences in their ability to colonize the gut. The local splanchnopleuric in the amniotic fluid (see Fig. 14.5B) (Ionescu 2014). mesenchyme patterns the crest cells, such that those that enter the gut layers attain an enteric fate, whereas those that remain outside the gut FUNCTIONAL MATURITY OF THE GUT AT BIRTH become committed as parasympathetic postganglionic neurones. The enteric neurones also migrate to the glands of the gut, e.g. the pancreas. Migrating vagal neural crest cells reach the midgut by week 5 and the The postnatal maturation of the gut is dependent on the establishment entire length of the gut is colonized by week 7. Maturation of the of an intestinal microbiota, which, in turn, is affected by gestational myenteric plexus follows a craniocaudal progression. The submucosal age, mode of delivery, type of feeding and any medical interventions. plexus arises from centripetally migrating cells from the myenteric plexus In cases of chorioamnionitis, preterm infants ingest bacterial products 2–3 days later (Burns et al 2009). Interstitial cells of Cajal, which derive from the amniotic fluid; it has been suggested that this may be associ­ from splanchnopleuric mesenchyme, do not mature in a craniocaudal ated with preterm labour (Neu and Mai 2012). Normal, term, vaginal progression. They are seen around the myenteric ganglia along the entire delivery establishes the initial colonization of the neonatal gut with gut from weeks 12–14 (Burns et al 2009). There is evidence that mucosal maternal vaginal and intestinal flora. Two­way interactions between enteric glial cells, which move into the mucosa after birth, interact with enteric microbes in a biofilm within the luminal glycocalyx of entero­ the colonizing intestinal flora, suggesting a microbiota­driven homeo­ cytes modify intestinal permeability, increase T and B lymphocyte static mechanism for gut function (Kabouridis et al 2015). numbers within the mucosal lamina propria and mesenteric lymph nodes, and stimulate postnatal immune development (Vaarala 2012, Wynn and Neu 2012, Martin et al 2012, Patel et al 2012, Gritz and Hirschsprung’s disease Bhandari 2015). Delivery by caesarean section results in the establish­ ment of skin microbiota, different intestinal microbes and low micro­ Hirschsprung’s disease (commonly called megacolon) is usually charac­ biota diversity. Failure to develop an appropriate, dynamic, microbiota terized by an aganglionic portion of gut that does not display peristalsis, is thought to be associated with allergic and inflammatory conditions and a dilated segment of structurally normal colon proximal to this site. in later life (Wynn and Neu 2012). (For further reading, see Neu (2012), Histologically, there is either an absence or a reduction in the number Bäckhed et al (2015), Rodríguez et al (2015).) of ganglia and postganglionic neurones in the myenteric plexus of the The onset of feeding also contributes to gut maturity. Breast milk is affected segment of gut; postganglionic innervation of the muscle layers a source of epidermal growth factor, which promotes postnatal mucosal is also often defective. It is believed that the condition is caused by a development and helps mucosal repair. Breast feeding also affects the failure of neural crest cells to colonize the gut wall appropriately production of immunoglobulin A (IgA) in the gut mucosa (Vaarala (Gershon 2010). A variable length of large intestine may be affected; the 2012). Undernutrition leads to villous atrophy and, in the preterm lower and mid­rectum are the most common sites but, in severe cases, infant, parenteral nutrition is associated with changes in intestinal the rectum, sigmoid, descending and even proximal colon can be agan­ structure and function that may lead to increased intestinal permeabil­ glionic. Occasionally, aganglionosis affects only a very short length of ity (Martin et al 2012). Antibiotic therapy within the neonatal period rectum proximal to the anorectal junction and the degree of functional can lead to changes in, and the establishment of, the normal intestinal obstruction is minimal; in these cases of ‘ultra­short­segment Hirschs­ microbiota (Martin et al 2012). prung’s disease’, clinical anomalies arise later in life. Infants with Hir­ The first passage of faeces of the newborn is termed meconium. This schsprung’s disease show delay in the passage of meconium, constipation, is a dark, sticky, viscid substance formed from the passage of amniotic vomiting and abdominal distension. fluid, sloughed mucosal cells, digestive enzymes and bile salts along the fetal gut. Meconium becomes increasingly solid as gestation advances but does not usually pass out of the fetal body while in utero. Fetal GUT-ASSOCIATED LYMPHOID TISSUE distress produced by anoxia may induce the premature defecation of meconium into the amniotic fluid, with the risk of its inhalation. At Individual lymphocytes appear in the lamina propria of the gut from birth, the colon contains 60–200 g of meconium. The majority of approximately week 12 of development, and lymphoid aggregates – neonates defecate within the first 24 hours after birth. Delayed passage Peyer’s patches – have been noted between 15 and 20 weeks; it is not of stool beyond this time is associated with Hirschsprung’s disease (see
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Peritoneal cavity 1059 06 RETPAHC above) or imperforate anus. The normal passage of meconium contin­ Mesenteries of the developing gut ues for the first 2 or 3 days after birth, and is followed by a transition to faecal stools by day 7. The cervicothoracic oesophagus develops between the pericardioperito­ neal canals. It is encased in prevertebral, retrotracheal and retrocardiac mesenchyme. As the pericardioperitoneal canals expand with the devel­ PERITONEAL CAVITY oping lung buds, and the diaphragm forms immediately below them; the oesophagus, at this level, has no true dorsal or ventral mesentery. The early development of the intraembryonic coelom, which gives rise At superior and intermediate thoracic levels, parts of the lateral aspects to the peritoneal cavity, is described on page 185. Figure 12.2 shows a of the oesophagus are closely related to the secondary, mediastinal, scheme of the shape of the early peritoneal cavity and indicates the parietal pleura. In the lower thorax, the oesophagus inclines ventrally mesenchymal populations derived from its epithelial walls. Initially, the anterior to the descending thoracic aorta. The dorsocaudally sloping peritoneal cavity associated with the lower end of the foregut has sepa­ midline diaphragm between oesophageal and aortic orifices may be rate right and left components: the pleuroperitoneal canals (see Fig. homologized with part of a dorsal meso­oesophagus, and is used in 60.1). At the level of the midgut, the pleuroperitoneal canals join a that context in descriptions of diaphragmatic development. A ventral confluent cavity surrounding the developing gut, which transitorily is midline diaphragmatic strip may also be considered to be a derivative in communication with the extraembryonic coelom. of a ventral meso­oesophagus; however, this region is more usually The description of the development of the peritoneal cavity that thought of as septum transversum. follows pertains to changes that occur as a consequence of the differ­ The alimentary tube, from the diaphragm to the start of the rectum, ential growth of the gut. initially possesses a sagittal dorsal mesentery. Its line of continuity with the dorsal parietal peritoneum (i.e. its ‘root’ or ‘line of reflection’) is, initially, also midline. The abdominal foregut, from the diaphragm to the future hepato­ PERITONEUM pancreatic duodenal papilla, also has a ventral mesentery. This extends from the ventrolateral margins of the abdominal oesophagus and as yet Peritoneum develops from a specific portion of the intraembryonic ‘unrotated’ primitive stomach and proximal duodenum, cranially to the coelomic walls. Initially, the intraembryonic coelomic epithelium is a future diaphragm and anteriorly to the ventral abdominal wall (to the pseudostratified germinal layer from which cellular progeny with dif­ level of the cranial rim of the umbilicus). Caudally, between umbilicus ferent fates arise in specific sites and at specific developmental times. and duodenum, it presents a crescentic free border. The portion that will give rise to the peritoneum is derived from the The midgut and hindgut have no ventral mesentery; thus, the pleural lower portion of the pericardioperitoneal canals and the somatopleure and supra­umbilical peritoneal cavities are, initially and transiently, and splanchnopleure associated with the lower foregut, midgut and bilaterally symmetrical above the umbilicus. Below the umbilicus, the upper portions of the hindgut (see Figs 12.2, 60.1). peritoneal cavity is freely continuous across the midline ventral to the The proliferative splanchnopleuric epithelium produces cell popula­ gut (see Fig. 60.5A). tions for the mucosa and muscularis of the gut, and also for the lamina propria and epithelium of the visceral peritoneum (the serosa of the Foregut mesenteries gut wall). The somatopleuric epithelium gives rise to the lamina propria and epithelium of the parietal peritoneum. The visceral and parietal The ventral and dorsal foregut mesenteries are relatively large compared peritoneal layers constitute a mesothelium, which denotes their origin with the slender endodermal tubes they encase; they are composed from the intraembryonic mesoderm of the coelomic wall. of mesenchyme sandwiched between two layers of splanchnopleuric As the gut grows, splanchnic mesenchyme accumulates around the coelomic epithelium. A complex series of recesses develop in the endodermal epithelium and the whole unit generally moves ventrally. splanchnopleuric mesenchyme and become confluent. As a result of There is a concomitant enlargement of the caudal ends of the develop­ foregut rotation, differential growth of the stomach, liver, pancreas ing pericardioperitoneal (pleuroperitoneal) canals and developing peri­ and spleen, and the completion of the diaphragm, the territories of toneal cavity. The medial walls of the intraembryonic coelom move the greater sac and lesser sac (omental bursa) are delimited, and the closer and there is a relative decrease in the mesenchyme between them. mesenteric complexes of these organs (omenta and ‘ligaments’) are The regions where the medial portions of the intraembryonic coelom defined (see Figs 60.6–60.7). come together are termed mesenteries. They are composed of two layers of peritoneum with intervening mesenchyme and contain the neuro­ Consequences of rotation of the stomach vascular structures that pass to and from the gut. At the caudal ends of the pleuroperitoneal canals, the gut has both ventral and dorsal mesenteries, whereas, caudal to this, there is only a dorsal mesentery A number of processes occur concurrently, which, conceptually, can be (see Fig. 60.6; Fig. 60.7). visualized as the movement of the right pleuroperitoneal canal to a The mesenteries attached to the gut lengthen to permit large move­ position posterior to the stomach, such that its communication with ments or rotations of the gut tube. Later, when part or the whole of the the remainder of the peritoneal cavity is reduced. These processes mesentery lies against the parietal peritoneum, their apposed surfaces include the differential growth of the walls of the stomach, the forma­ fuse and are absorbed, i.e. they become sessile. Only those viscera tion and specific local extension of the omenta (dorsal and ventral developed in direct apposition to one of the primary coelomic regions, mesogastria), and the growth of the liver and, particularly, of the vessels or a secondary extension of the latter, retain a partial or almost com­ and ducts that enter and leave the liver. These developments permit plete visceral serous cover. Thus, the original line of reflection of stomach expansion both anteriorly and posteriorly when food is mesenteries becomes altered, or, in some cases, the organ may become ingested, and free movement of peristalsis. The right pleuroperitoneal retroperitoneal. These mechanisms are significant throughout the sub­ canal forms a discrete region of the peritoneal cavity, the lesser sac, and diaphragmatic gut, but are predominant in the small and large intestine. the remaining left pleuroperitoneal canal and the remainder of the All serous membranes may vary their thickness, lines of reflection, peritoneal cavity form the greater sac. The entrance to the original right disposition, ‘space’ enclosed and their channels of communication, by pleuroperitoneal canal (lesser sac) becomes reduced in size. It is called a process of areal and thickness growth on one aspect, combined with the epiploic foramen, foramen of Winslow, or the aditus of the omental cavitation (leading to expanding embryonic recess formation) on the bursa (bursa omentalis). other. Early stages of lesser sac development Although all of the gut tube and its derived glands are associated with mesenteries formed as described above, the nomenclature for some portions of the gut and glands is different. Thus, the mesenteries The lesser sac is first indicated by the appearance of multiple clefts of the stomach are called omenta and the reflections of peritoneum in the para­oesophageal mesenchyme on both left and right aspects around the liver, which develop from a confluence of splanchnopleuric, of the oesophagus. Although they may become confluent, the left clefts somatopleuric and septum transversum­derived portions, are called are transitory and soon atrophy. The right clefts merge to form the ligaments. right pneumatoenteric recess that extends from the oesophageal end of The movements of the developing viscera within the peritoneal the lesser curvature of the stomach as far as the caudal aspect of the cavity occur with associated movements of the mesothelia that sur­ right lung bud. At its gastric end, it communicates with the general round them. The descriptions of peritoneal cavity development that peritoneal cavity and lies ventrolateral to the gut; more rostrally it follow are thus describing a sequence of changes that affect a complex lies directly lateral to the oesophagus. It is not, as commonly stated, space and its boundaries. a simple progressive excavation of the right side of the dorsal
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DEvEloPmEnT of THE PERiTonEAl CAviTy, gAsTRoinTEsTinAl TRACT AnD iTs ADnExAE 1060 8 noiTCEs A(i) A(ii) Oesophagus Extends cranially into pneumatoenteric recess Right lung bud Right pneumatoenteric recess Hepatoenteric Parietal recess (lesser Inferior vena cava peritoneum Inferior vena cava in caval fold omental recess) in caval fold Epiploic foramen Hepatoenteric recess Perigastric, retrogastric and greater omental Secondary dorsal mesogastrium recesses Lesser omentum, free border Retrogastric and perigastric recesses B(i) B(ii) Kidney Infracardiac bursa Suprarenal gland Line of fusion Diaphragm Pneumatoenteric recess (caudal part) Inferior vena cava Liver (early caudate lobe) Caval fold Spleen Hepatoenteric recess Stomach Spleen Pancreaticoenteric recess Pancreas (body) Stomach C(i) C(ii) Upper part of lesser sac: pneumatoenteric and hepatoenteric regions, Prerenal, retroperitoneal, body of pancreas Kidney covered by lesser omentum Entrance via epiploic foramen and canal Junction between upper and lower parts of lesser sac Lesser omentum Gastrosplenic ligament Tail of pancreas in splenorenal ligament Lower part of lesser sac: perigastric, retrogastric and greater omental D Lesser omentum Diaphragm E Liver Aorta Liver Gastrosplenic ligament Spleen Falciform ligament Splenorenal ligament Gallbladder Pancreas (body) Entrance to early epiploic foramen Expanding greater omentum Fig. 60.7 A–C, Stages of development of the subdiaphragmatic foregut and the right and left pericardioperitoneal/pleuroperitoneal canals, with particular reference to the terminal oesophagus, stomach, duodenum, spleen, the lesser sac of the peritoneum and the omenta, seen in semicoronal section (left column) and transverse section at the levels indicated by the arrows (right column). D–E, The lesser sac and dorsal and ventral mesogastria. mesogastrium. The right pneumatoenteric recess undergoes further meso­oesophagus; the much larger ventral mesogastrium, and the extension, subdivision and modification (see Fig. 60.7 A(i), B(i)). most caudal free border, is from the ventral mesoduodenum. As dif­ From its caudal end, a second process of cleft and cavity formation ferential growth of the duodenum occurs, the biliary duct is reposi­ occurs, which produces the hepatoenteric recess. This thins and tioned and most of the duodenum becomes sessile. The duodenal expands the splanchnopleure between the liver and the stomach and attachment of the free border and a continuous neighbouring strip of proximal duodenum, and reaches the diaphragm (see Fig. 60.7A(i), the lesser omentum become confined to the upper border of a short C(i)). The resulting, structurally bilaminar, mesenteric sheet is the segment of its superior part. The contrasting growth and positioning of lesser omentum. It is derived, cranially to caudally, from the small its attached viscera cause the free border to change gradually from the
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Peritoneal cavity 1061 06 RETPAHC horizontal to the vertical. It carries the bile duct, portal vein and meet and blend. It provides a mesenchymal route for the upper abdom­ hepatic artery, and its hepatic end is reflected around the porta hepatis. inal, transdiaphragmatic and transpericardial parts of the inferior vena An alternative name for this part of the lesser omentum is the hepa­ cava, and it is also prominent in the development of parts of the liver, toduodenal ligament; it forms the anterior wall of the epiploic lesser sac of peritoneum, and certain mesenteries. The left fold regresses foramen. The floor of the foramen is the initial segment of the superior whereas the right fold enlarges rapidly (see Fig. 60.7A). part of the duodenum, its posterior wall is the peritoneum covering The pneumatoenteric recess continues to expand to the right into the immediately subhepatic part of the inferior vena cava, and its roof the substance of the caval fold. It stops near the left margin of the the peritonealized caudate process of the liver. The major part of the hepatic part of the inferior vena cava, which remains extraperitoneal lesser omentum from the lesser gastric curvature passes in an approxi­ and crosses the base of the now roughly triangular bare area of the liver mately coronal plane to reach the floor of the increasingly deep groove and this new expanded line of reflection. With closure of the pleuro­ for the ductus venosus on the hepatic dorsum; this part is sometimes peritoneal canals, the rostral part of the right pneumatoenteric recess is called the hepatogastric ligament. sequestered by the diaphragm but often persists as a small serous sac in the right pulmonary ligament. The remaining caval fold mesen­ Ligaments of the liver chyme to the left of the inferior vena cava – which forms the right wall The liver is precociously large during development because of its early of the upper part of the lesser sac – becomes completely invaded by role in haemopoiesis. Thus, the liver mass projects into the abdominal embryonic hepatic tissue and is transformed into the caudate lobe of cavity with equal growth on the two sides of the peritoneal cavity. The the liver. This smooth, vertically elongated, mass projects into the ligaments associated with the liver develop from the ventral mesogas­ cavity of the lesser sac; both its posterior, and much of its anterior, trium – which passes from the foregut to the ventral abdominal wall, surfaces become peritonealized as a result of the increasing depth of down to the cranial rim of the intestinal portal – and from the reflec­ the groove for the ductus venosus and the attachment of the lesser tions of peritoneum from the liver to the diaphragm. omentum to its floor. The medial portions of the germinative coelomic epithelial walls, containing splanchnopleuric mesenchyme, septum transversum mesen­ Later stages of lesser sac development chyme and developing liver, constitute the early ventral mesogastrium (see Fig. 60.5). The mesenchyme between these layers is continuous superiorly with the septum transversum mesenchyme of the diaphragm. The lower (inferior) part of the lesser sac can be first seen in embryos The coelomic epithelial layers of the ventral mesogastrium almost touch of 8–9 mm crown–rump length, and the early pneumatoenteric and anterior and posterior to the liver, and are separated by a slender lamina hepatoenteric recesses are well established. Progressive differential of mesenchyme. They form the falciform ligament and the lesser gastric growth produces an elliptical transverse sectional profile, with a omentum, respectively, and where they are in contact with the liver right­sided lesser curvature, which corresponds to the original ventral directly, they form visceral peritoneum (see Fig. 60.7D). border of the gastric tube. The lesser omental gastric part of the ventral When the diaphragm is formed above the liver, local cavities coalesce mesogastrium remains attached to this border. The greater curvature of and open into the general coelomic cavity as extensions of the greater the stomach is a new, rapidly expanding, region; its convex profile (and lesser) sacs. In this way, almost all the ventrosuperior, visceral and projects mainly to the left, but also cranially and caudally (see Fig. some of the posterior aspects of the liver become peritonealized. The 60.7A(i), B(i), C(i)). The original dorsal border of the gastric tube now process of extending the greater sac continues over the right lobe and traverses the dorsal aspect of the expanding rudiment, curving along a stops when the future superior and inferior layers of the coronary liga­ line near the lesser curvature. The primitive dorsal mesogastrium is ment and the right triangular ligament are defined. Those, plus a medial transiently attached to it, and blends with the thick layer of compound boundary provided by an extension of the lesser sac, enclose the ‘bare gastric mesenchyme clothing the posterior aspect and greater curvature area’ of the liver, where loose areolar tissue of septum transversum of the miniature stomach. Because of its thickness, the mesenchyme origin persists. Later in development, when the haemopoietic function projects cranially, caudally and, particularly, to the left, beyond the of the liver declines, the left lobe becomes relatively smaller than the ‘new’ greater curvature of the endodermal lining of the stomach. right; this, presumably, accounts for the smaller size of the left triangu­ The processes already described in relation to the ventral mesenteries lar ligament. now supervene. Multiple clefts appear at various loci in the mesen­ Where the superior layers of the coronary and left triangular liga­ chyme, and there are local mesenchyme to epithelial transitions. The ments meet, they continue as a (bilaminar) ventral mesentery attached groups of clefts rapidly coalesce to form transiently isolated closed to the ventrosuperior aspects of the liver. Its somewhat arched umbilico­ spaces, which soon join with each other and with the preformed upper hepatic free caudal border carries the left umbilical vein. As the ventral part of the lesser sac; the newly formed epithelia join the coelomic body wall develops, this falciform ligament, which initially attaches to epithelium. In sequence, the initial loci occur in the compound poste­ the early cranial intestinal portal, is drawn to the diminishing cranial rior gastric mesenchyme nearer the lesser curvature and along its zone rim of the umbilicus. It may be considered the final ventral part of the of blending with the primitive dorsal mesogastrium; in the dorsal meso­ ventral mesogastrium, although its free border has a ventral mesoduo­ duodenum; and independently, in the caudal rim, where greater curva­ denal origin. Its passage to the ventral body wall becomes increasingly ture mesenchyme and dorsal mesogastrium blend. As these cavities oblique, curved and falciform (sickle­shaped) as the umbilicus becomes become confluent and their ‘reniform’ expansion follows, matches and more defined. then exceeds that of the gastric greater curvature, there are several major In the early embryo, the connection between one pericardioperito­ sequelae. The primitive dorsal mesogastrium increases in area by intrin­ neal canal and the other was directly across the ventral surface of the sic growth, and, as cavitation proceeds, by incorporating substantial cranial midgut, immediately caudal to the developing primitive ventral contributions from the dorsal lamella separated by cleavage of the mesogastrium. By stage 14, the passage from one side of the falciform posterior gastric mesenchyme; it is now called the secondary dorsal ligament to the other necessitates passing below the greatly enlarged mesogastrium (see Fig. 60.7A(ii)). The gastric attachment of the second­ liver, or the curved lower edge of the falciform ligament, or the lesser ary dorsal mesogastrium changes progressively. It may be regarded as a omentum. The position of the falciform ligament is of clinical interest set of somewhat spiral lines, longitudinally disposed, that move with in the neonate in diagnosing pneumoperitoneum because it is silhouet­ time to the left, from near the lesser curvature, towards and finally ted by air on abdominal X­rays. reaching the definitive greater curvature. The parietal mesogastrial and (cleaving) mesoduodenal attachment remains in the dorsal midline for Caval fold a time, but it later undergoes profound changes. With the confluence The caval fold is a linear eminence, with divergent cranial and caudal of the cavities that collectively form the lower part of the lesser sac, its ends, which passes from the upper abdominal to the lower thoracic communication with the upper part (which corresponds to the lesser region and protrudes from the dorsal wall of the pleuroperitoneal canal. gastric curvature and right and left gastropancreatic folds) becomes Cranially, it becomes continuous, lateromedially, with the root of the better defined. Ventral to the lower part of the cavity, post­cleavage pulmonary anlage and pleural coelom, the uppermost portion of the splanchnopleure covers the posteroinferior surface of the stomach and septum transversum mesenchyme, and the retrocardiac mediastinal a short proximal segment of the duodenum. This ventral wall is con­ mesenchyme. Caudally, it forms an arch with dorsal and ventral horns. tinued beyond the greater curvature and duodenum as the splanchno­ The dorsal horn merges with the primitive dorsal mesentery and the pleuric strip of visceral attachment of the secondary dorsal mesogastrium mesonephric ridge and associated gonad and suprarenal (adrenal) and mesoduodenum. The radial width of the strip is relatively short gland. The ventral horn is confluent with the dorsal surface of the septal cranially (gastric fundus) and gradually increases along the descending mesenchyme. left part of the greater curvature. It is longest throughout the remaining Thus, the caval fold is a zone where intestinal, mesenteric, intermedi­ perimeter of the greater curvature as far as the duodenum; this promi­ ate, hepatic, pericardial, pulmonary and mediastinal mesenchymes nent part shows continued marginal (caudoventral and lateral) growth
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DEvEloPmEnT of THE PERiTonEAl CAviTy, gAsTRoinTEsTinAl TRACT AnD iTs ADnExAE 1062 8 noiTCEs with extended internal cavitation (its walls constitute the expanding vein, portal vein, left renal vessels, the caudal pole of the left suprar­ greater omentum; see Fig. 60.6H). The margins of the cavity of the enal gland, a broad ventral band on the left kidney and various inferior part of the lesser sac are limited by the reflexed edges of the muscles). The intervening peritoneal mesothelia fuse and atrophy, and ventrally placed strata derived from the secondary dorsal mesogastrium the mesenchymal cores form fascial sheaths and septa. The pancreas is just described. These converge to form the splanchnopleuric dorsal wall, now sessile. The peritoneum covering the upper left part of its head, which is initially ‘free’ throughout, except at its midline dorsal root. At neck and the anterosuperior part of its body forms the central part of roughly mid­gastric levels, the pancreatic rudiment grows obliquely the dorsal wall of the lesser sac. The pancreatic tail remains perito­ encased in this dorsal wall; its tail ultimately reaches the left limit of nealized by a persisting part of the secondary dorsal mesogastrium as the lesser sac at the level of the junction between gastric fundus and it curves from the ventral aspect of the left kidney towards the hilum body (see Fig. 60.7C(ii)). of the spleen. The infracolic parts of the pancreas are covered with greater sac peritoneum. In the greater omental subregion of the lower Greater omentum part of the lesser sac, two contrasting forms of mesenteric adhesion The greater omentum continues to grow, both laterally and, particularly, occur. The posterior ‘returning’ bilaminar stratum of the omentum caudoventrally. It covers and is closely applied to the transverse meso­ undergoes partial fusion with the peritoneum of the transverse colon colon, transverse colon and inframesocolic and infracolic coils of small at the taenia omentalis and with its mesocolon. The layers remain intestine (see Fig. 60.6D–G). At this stage, the quadrilaminar nature of surgically separable; no anastomosis occurs between omental and the dependent part of the greater omentum is most easily appreciated. colic vessels. ‘Simple’ mesenteries are bilaminar: they possess two mesothelial sur­ The original dorsal midline attachment to the parietes of the faces derived from splanchnopleuric coelomic epithelium, which foregut dorsal mesentery is profoundly altered during the develop­ enclose a connective tissue core derived from splanchnopleuric mesen­ ment of the lesser sac and its associated viscera. However, despite the chyme. In the greater omentum, the gastric serosa covering its postero­ extensive areas of fusion, virtually the whole of the gastric greater cur­ inferior surface (single mesothelium) and the anterosuperior serosa vature (other than a small suboesophageal area) and its topographical (single mesothelium) converge to meet at the greater curvature and continuation (the inferior border of the first 2–3 cm of the duode­ initial segment of the duodenum. The resulting bilaminar mesentery num) retain true mesenteric derivatives of the secondary dorsal mes­ continues caudoventrally as the ‘descending’ stratum of the omentum. ogastrium and its continuation, the dorsal mesoduodenum. Although This, on reaching the omental margins, is reflexed and now passes regional names are used to assist identification and description, it is cranio dorsally to its parietal root as the ‘ascending’ posterior bilaminar important to emphasize that they are all merely subregions of one stratum. The two bilaminar strata are, initially, in fairly close contact continuous sheet. caudally, but are separated by a fine, fluid­containing, cleft­like exten­ The upper (oesophagophrenic) part of the lesser omentum arches sion of the lower part of the lesser sac. The posterior mesothelium of across the diaphragm. As this bilaminar mesentery approaches the the posterior stratum makes equally close contact with the anterosupe­ oesophageal hiatus, its laminae diverge, skirting the margins of the rior surface of the transverse colon, starting at the taenia omentalis, and hiatus. They then descend for a limited distance and with variable with its transverse mesocolon. inclination, to enclose reciprocally shaped areas on the dorsum of the gastric fundus and diaphragm. The area may be roughly triangular to quadrangular; it contains areolar tissue and constitutes the bare area Maturation of the lesser sac of the stomach or, when large, the left extraperitoneal space. Its right lower angle is the base of the left gastropancreatic fold, and its left At this stage, and subsequently, it is convenient to designate the lower lower angle reconstitutes the bilaminar mesentery. The root of the part of the lesser sac as consisting of three subregions: retrogastric, peri­ latter arches downwards and to the left across the diaphragm and gastric and greater omental (Fig. 60.7C(ii)). The names are self­ suprarenal gland, and gives the gastrophrenic ligament to the gastric explanatory but their confines are all modified by various factors. Two fundus. It continues to arch across the ventral surface of the upper phenomena are particularly prominent: namely, gastric ‘descent’ rela­ part of the left kidney, and its layers part to receive the pancreatic tail; tive to the liver, and fusion of peritoneal layers with altered lines of they initially extend to the hilum of the spleen as the splenorenal liga­ reflection, adhesion of surfaces and loss of parts of cavities. ment (see Figs 60.6C, 60.7D). The left half of this bilaminar ‘liga­ After the third month, hepatic growth, particularly of the left lobe, ment’ provides an almost complete peritoneal tunic for the spleen. It diminishes and the whole organ recedes into the upper abdomen. then reunites with its fellow at the opposite rim of the splenic hilum, Meanwhile, the stomach elongates and some descent occurs, despite and continues to the next part of the gastric greater curvature as the its relatively fixed cranial and caudal ends. This produces the angular gastrosplenic ligament. The remaining part (perhaps two­thirds) of flexure of the stomach, which persists postnatally. The concavity of the the gastric greater curvature and its short duodenal extension provide lesser curvature is now directed more precisely to the right; the lesser attachment for the anterior, ‘descending’, bilaminar stratum of the omentum is more exactly coronal and its free border vertical. Ventral greater omentum. Its returning, posterior, bilaminar stratum continues to the liver, the free border of the falciform ligament passes steeply to its parietal root (which extends from the inferior limit assigned to craniodorsally from umbilicus to liver (see disposition in the neonate the splenorenal ligament), and curves caudally and to the right along in Figs 14.6–14.7). The mesenchymal dorsal wall of the lower part of the anterior border of the body of the pancreas, immediately cranial the lesser sac, which is crossed obliquely by the growing pancreas, has, to the line of attachment of the transverse mesocolon. Crossing the up to this point, remained free and retained its original dorsal midline neck of the pancreas, the same curve is followed for a few centimetres root. Substantial areas now fuse with adjacent peritonealized surfaces on to its head; the omental root then sharply recurves cranially and to of retroperitoneal viscera, the parietes, or another mesenteric sheet or the left, to reach the inferior border of the duodenum. Thus, it reaches fold. Where sheets fuse, there is a variable loss of apposed mesothelia that part of the lesser sac provided by cleavage of the dorsal mesoduo­ and some continuity of their mesenchymal cores, but they remain denum from the greater sac. It enters the epiploic foramen, traverses surgically separable and no vascular anastomosis develops across the the epiploic canal between the caudate hepatic process and proximal interzone. Above the pancreas, the posterior secondary dorsomesogas­ duodenum, then crosses the right gastropancreatic fold, and descends trial wall of the sac becomes closely applied to the peritoneum behind the proximal duodenum to enter the right marginal strip covering the posterior abdominal wall and its sessile organs, the dia­ enclosed by the greater omentum. The definitive origins of the perito­ phragm, much of the left suprarenal gland, the ventromedial part of neum from the posterior abdominal wall are shown in the adult in the upper pole of the left kidney, the initial part of the abdominal Figures 63.1, 68.5, 63.6B. aorta, the coeliac trunk and its branches, and other vessels, nerves and lymphatics. Their peritoneal surfaces fuse. However, albeit with Peritoneum associated with the some tissue loss, a single mesothelium remains covering these struc­ mid- and hindgut tures, intercalated as a new secondary dorsal wall for this part of the lesser sac. The pancreas grows from the duodenal loop, penetrating the sub­ It is convenient to consider the mesenteries of the small and large stance of the dorsal mesoduodenum and secondary dorsal mesogas­ intestine after rotation and the principal growth patterns have been trium; their mesenchymes and mesothelia initially clothe its whole achieved, and the developing pancreas is becoming retroperitoneal. surface, except where peritoneal lines of reflection exist. Its posterior Small intestine peritoneum becomes closely applied to that covering all the posterior abdominal wall structures it crosses (the inferior vena cava, abdomi­ Most of the duodenal loop encircles the head of the pancreas and is nal aorta, splenic vein, superior mesenteric vessels, inferior mesenteric retroperitoneal. The peritoneum principally covers its ventral and
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Peritoneal cavity 1063 06 RETPAHC convex aspects. Areas not covered are a short initial segment of the eleventh ribs by a phrenicocolic ligament. The latter sometimes superior (first) part, which is more completely peritonealized because blends with a presplenic fold that radiates from the gastrosplenic liga­ it gives attachment to the right margins of the greater and lesser omenta; ment. The descending colon becomes sessile. The process of fusion and the sites where the transverse colon is closely apposed to the descending obliteration of both ascending and descending mesocolons starts later­ (second) part, or where the latter is crossed by the root of the transverse ally and progresses medially. mesocolon; and the sites where the mesentery crosses the transverse (third) part, and descends across the ascending (fourth) part from its Sigmoid colon upper extremity at the duodenojejunal flexure. These regions are illus­ The sigmoid colon is most variable in its length and disposition. It trated in the adult in Figure 63.2. In addition, one or more of up to six retains its dorsal mesocolon, but the initial midline dorsal attachment different duodenal recesses may develop (p. 1108). of its root is considerably modified in its definitive state. From a mesenteric standpoint, the succeeding small intestine, from the duodenojejunal flexure to the ileocaecal junction, undergoes less Rectum modification of its embryonic form than other gut regions. Its early The rectum continues from the ventral aspect of the third sacral vertebra dorsal mesentery is a continuous, single (but structurally bilaminar) to its anorectal (perineal) flexure anteroinferior to the tip of the coccyx; sheet, with a midline parietal attachment (line of reflection, or ‘root’). the distance changes with age. All aspects of the rectum are encased by The attachment of the root becomes an oblique narrow band from the mesenchyme, and the early, dorsally placed, mass is named, by some left aspect of the second lumbar vertebra to the cranial aspect of the authorities, the dorsal mesorectum. However, the latter does not form right sacroiliac joint (see Figs 60.6H, 63.2). a true mesentery; with progressive skeletal development, it is reduced to a woven fibroareolar sheet that displays patterned variations in thick­ Ascending colon ness and fibre orientation. The sheet is closely applied to the ventral The caecum and vermiform appendix arise as a diverticulum from the concavity of the sacrum and coccyx, and encloses numerous fibromus­ antimesenteric border of the caudal limb of the midgut loop; conse­ cular and neurovascular elements. The rectum, therefore, becomes quently, the caecum does not possess a primitive mesocaecum. These sessile, and visceral peritoneum is restricted to its lateral and ventral regions of the gut undergo long periods of growth, often asymmetrical, surfaces (see Fig. 72.4). and their final positions, dimensions and general topography show With the disappearance of the postanal gut by the end of the fifth considerable variation. The vermiform appendix is almost wholly week, the ventrolateral peritoneum reaches the superior surface of the clothed with visceral peritoneum, derived from the diverging layers of pelvic floor musculature; this condition persists until late in the fourth its rather diminutive mesoappendix. The latter should perhaps be month. In the male, the ventral rectal peritoneum is reflected over the regarded as a direct derivative of the primitive dorsal mesentery, and posterior surface of the prostate, bladder trigone and associated struc­ perhaps a similar status for the vascular fold of the caecum should be tures. In the female, the ventral peritoneum initially receives a reflection considered. that covers almost the whole posterior aspect of the vagina, and is The colonic gut retains its primitive dorsal mesentery, the mesoco­ continued over the uterus. Subsequently, the closely apposed walls of lon, until the differential growth, rotation and circumabdominal dis­ these deep peritoneal pouches fuse over much of their caudal extent, placement of this part of the gut tube near completion. Its original their mesothelia are lost, and the viscera are separated by an interven­ root is still vertical in the dorsal midline, although the mesocolon ing, bilaminar (surgically separable), fibrous stratum. In the male, this diverges from it widely as an incomplete, flattened pyramid, to reach becomes the rectovesical fascia and posterior wall of the prostatic its colonic border at the future taenia mesocolica. During the fourth sheath (see Fig. 72.10). In the female, it becomes the rectovaginal and fifth months, substantial areas of the primitive mesocolon adhere septum between the lower part of the vagina and the rectum (see Fig. to, then fuse with, the parietal peritoneum. In this way, some colonic 72.9). The proximal third of the rectum is covered by peritoneum ven­ segments become sessile while others have a shorter mesocolon with trolaterally; the lateral extensions of this tunic are triangular and deep an often profoundly altered parietal line of attachment. The mesoco­ proximally, but taper to an acute angle by the middle third of the lon of the transverse and sigmoid segments normally persists, while rectum. The middle third of the rectum is covered by peritoneum only the ascending colon, right (hepatic) flexure and descending colon on its ventral surface, where it forms the posterior wall of the shallower become sessile; the ascending or descending, or both, colonic seg­ rectovesical or rectovagino­uterine pouch. The remaining rectum and ments may also retain a mesocolon, which varies from a localized anal canal are extraperitoneal. ‘fold’ to a complete mesocolon. When sessile, the ventral, medial and lateral aspects of the ascending or descending colon are clothed with NEONATAL PERITONEAL CAVITY peritoneum, and the protrusion of the viscus produces medial and lateral peritoneal paracolic gutters on each side. This form of apposi­ The fully formed peritoneal cavity, although complex topographically, tion to underlying structures (zygosis) proceeds from the ascending remains a single cavity with numerous intercommunicating regions, colon to include the right colic (hepatic) flexure; from there, it contin­ pouches and recesses (see Fig. 14.7). The only small peritoneal sacs to ues anteroinferiorly to the left, so involving the right­sided initial separate completely from the main cavity are the infracardiac bursa and segment of the transverse colon. the tunica vaginalis testis (see Fig. 72.17). In fetal life, the greater omental cavity extends to the internal Transverse colon aspect of the lateral and caudal edges of the omentum. Postnatally, a The right extremity of the transverse colon is sessile, and is separated slow but progressive fusion of the internal surfaces occurs, with oblit­ by fibroareolar tissue from the anterior aspect of the descending eration of the most dependent part of the cavity; this proceeds ros­ (second) part of the duodenum and the corresponding aspect of most trally and, when mature, the cavity does not usually extend appreciably of the head of the pancreas. The remainder of the transverse colon, up beyond the transverse colon. Transverse mesocolon–greater omentum to and including the left (splenic) colic flexure, is almost completely fusion begins early while the umbilical hernia of the midgut has not peritonealized by the diverging layers of the transverse mesocolon. returned. It starts between the right margin of the early greater The root of the latter reaches the neck and whole extent of the ante­ omentum and near the root of the presumptive mesocolon, and later rior border of the body of the pancreas. The long axis of the definitive spreads to the left. pancreas lies obliquely. The splenic colonic flexure is considerably In the neonate, the peritoneal cavity is ovoid (see Fig. 14.6). It is more rostral than the hepatic flexure and, consequently, the root of fairly shallow from anterior to posterior because the bilateral posterior the mesocolon curves obliquely upwards as it crosses the upper extensions on each side of the vertebral column, which are prominent abdomen from right to left. As it expands, the posteroinferior wall of in the adult, are not present. Two factors lead to the protuberance of the greater omental part of the lesser sac gradually covers, and becomes the anterior abdominal wall in the neonate and infant. The diaphragm closely applied to, the transverse mesocolon and its contained colon, is flatter in the newborn, which produces a caudal displacement of the finally projecting beyond the latter. Craniocaudal adherence now viscera. The pelvic cavity is very small in the neonate, which means that occurs between the omental wall and the pericolonic and mesoco­ organs that are normally pelvic in the adult, i.e. urinary bladder, ovaries lonic layers. and uterus, all extend superiorly into the abdomen (see Figs 14.7, 72.9–72.10). The pelvic cavity is joined to the abdominal cavity at less Descending colon of an acute angle in the neonate because there is no lumbar vertebral The left colic flexure receives much of its peritoneal covering from the curve and only a slight sacral curve. left extremity of the transverse mesocolon. It is also often connected The peritoneal attachments are similar to the adult. However, the to the parietal peritoneum of the diaphragm over the tenth and greater omentum is relatively small; its constituent layers of peritoneum
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DEvEloPmEnT of THE PERiTonEAl CAviTy, gAsTRoinTEsTinAl TRACT AnD iTs ADnExAE 1064 8 noiTCEs may not be completely fused, and it does not extend much below the The most common anomaly of suprarenal gland development is level of the umbilicus. Generally, the length of the mesentery of the congenital hyperplasia, which occurs in 1 : 5000 to 1 : 15,000 births. small intestine and of the transverse and sigmoid mesocolons is greater This condition is caused by a group of autosomal recessive disorders, than in the adult, whereas the area of attachment of the ascending and in which there are deficiencies in enzymes required for the synthesis of descending colons is relatively smaller. The peritoneal mesenteries and cortisol. In 90% of cases, the cause is deficiency of the enzyme omenta contain little fat. 21­hydroxylase, producing an accumulation of 17­hydroxyprogesterone, which is converted to androgens. The levels of androgens increase by several hundred times, causing female embryos and fetuses to undergo SPLEEN external genital masculinization ranging from clitoral hypertrophy to formation of a phallus and scrotum; masculinization of the brain has The spleen appears about the sixth week as a localized thickening of also been suggested. In male embryos, the levels do not cause any the coelomic epithelium of the dorsal mesogastrium near its cranial end changes in external genitalia. Signs of androgen excess may appear in (see Figs 60.6–60.7). The proliferating cells invade the underlying ang­ childhood with precocious masculinization and accelerated growth iogenetic mesenchyme, which becomes condensed and vascularized. (Lewis et al 1999). The process occurs simultaneously in several adjoining areas, which soon fuse to form a lobulated spleen of dual origin (from coelomic epithelium and from mesenchyme of the dorsal mesogastrium). SUPRARENAL GLANDS IN THE NEONATE The vascular reticulum is well developed at 8–9 weeks, and contains immature reticulocytes and numerous closely spaced, thin­walled, vas­ The suprarenal glands are relatively very large at birth (see Figs 14.6C, cular loops. From 11 weeks, the development of the spleen has been 72.8) and constitute 0.2% of the entire body weight, compared with described in four stages: stage 0 has erythrocyte precursors, few macro­ 0.01% in the adult. The left gland is heavier and larger than the right, phages and fewer lymphocytes; at stage I, lymphocytes begin coloniza­ as it is in the adult. At term, each gland usually weighs 4 g; the average tion and arterial vascular lobules are seen; at stage II, T and B weight of the two glands is 9 g (average in the adult is 7–12 g). Estima­ lymphocytes form peri­arteriolar clusters with B cells aggregated around tion of the suprarenal gland volume can provide an estimate of fetal the peripheral branches of splenic arterioles and T cells centrally; at weight; a volume of greater than 420 mm3/kg is relevant in predicting stage III, before birth, the lobular arrangement is no longer discernible preterm birth within 5 days of measurement (Turan et al 2012, Turan (Steiniger et al 2007). et al 2007). Within the first 2 weeks of postnatal life, the glands shrink From week 17, α­SMA­positive reticulum cells are found around to normal infantile size. The average weight of both glands is 5 g by the arterioles. These increase in number and form a reticular framework end of the second week, and 4 g by 3 months; gland birth weight is not from 20 to 23 weeks, when a primitive white pulp can be observed regained until puberty. This rapid involution of the glands occurs around arterioles. By 24 weeks, T and B lymphocytes become segre­ regardless of gestational age. It is thought that parturition is the stimu­ gated, with T cells within the SMA­positive reticular framework, and B lus for suprarenal involution (Ben­David et al 2007). The cortex of the cells aggregating close to the peri­articular lymphoid sheath, where they suprarenal gland is thicker than in the adult and the medulla of the form lymphoid follicles (Satoh et al 2009). gland is small. With normal involution, the fetal zone cells of the post­ Initially, the splenic capsule consists of cuboidal cells bearing cilia natal gland become smaller and they assume the appearance and organ­ and microvilli. The enlarging spleen projects to the left, so that its sur­ ization typical of zona fasciculata. faces are covered by the peritoneum of the mesogastrium on its left aspect, which forms a boundary of the general extrabursal (greater) sac. When fusion occurs between the dorsal wall of the lesser sac and the INFERIOR VENA CAVA, PORTAL CIRCULATION dorsal parietal peritoneum, it does not extend to the left as far as the AND UMBILICAL VESSELS spleen, which remains connected to the dorsal abdominal wall by a short splenorenal ligament. Its original connection with the stomach persists as the gastrosplenic ligament. The earlier lobulated character of INFERIOR VENA CAVA the spleen disappears, but is indicated by the presence of notches on its upper border in the adult. The inferior vena cava of the adult is a composite vessel that develops The spleen displays various developmental anomalies, including on the posterior abdominal wall dorsal to the developing peritoneal complete agenesis, multiple spleens or polysplenia, isolated small addi­ cavity. It forms as a consequence of the temporal remodelling of suc­ tional spleniculi and persistent lobulation. Asplenia and polysplenia cessive venous complexes (see Fig. 13.4). The precise mode of develop­ are associated with other anomalies, especially those involving the ment of its postrenal segment (caudal to the renal vein) is still somewhat cardiac and pulmonary systems. Accessory spleens are very common in uncertain. Its function is initially carried out by the right and left post­ neonates, located in the greater omentum. At birth, the spleen weighs, cardinal veins (Fig. 60.8; see also Fig. 13.4), which receive the venous on average, 13 g (see Fig. 14.6). It doubles its weight in the first post­ drainage of the lower limb buds and pelvis, and run in the dorsal part natal year and triples it by the end of the third year. of the mesonephric ridges, receiving tributaries from the body wall (intersegmental veins) and from the derivatives of the mesonephroi. It should be remembered that descriptions of venous development are SUPRARENAL GLANDS very largely based on studies on animals, where the dimensions and final disposition of visceral organs differ from those found in humans. The suprarenal (adrenal) cortex is formed during the second month by Many of the changes seen in the development of the infrahepatic caval a proliferation of the coelomic epithelium. Cells pass into the underly­ and azygos systems in the human may result from lateral to medial ing mesenchyme between the root of the dorsal mesogastrium and the movement of the vessels as a consequence of the growth of the abdomi­ mesonephros (see Fig. 17.11). The proliferating tissue, which extends nal viscera (Hikspoors et al 2015). from the level of the sixth to the twelfth thoracic segments, is soon The early postcardinal veins communicate across the midline via an disorganized dorsomedially by invasion of neural crest cells from interpostcardinal anastomosis. This remains as an oblique transverse somite levels 18–24, which form the medulla, and also by the develop­ anastomosis between the iliac veins, and becomes the major part of the ment of venous sinusoids. The latter are joined by capillaries, which definitive left common iliac vein. It diverts an increasing volume of arise from adjacent mesonephric arteries and penetrate the cortex in a blood into the right longitudinal veins, which accounts for the ultimate radial manner. When proliferation of the coelomic epithelium stops, disappearance of most of those on the left. the cortex is enveloped ventrally, and later dorsally, by a mesenchymal The supracardinal veins receive the larger venous drainage of the capsule that is derived from the mesonephros. The subcapsular nests of growing body wall. The right supracardinal vein persists and forms cortical cells are the rudiment of the zona glomerulosa; they proliferate the greater part of the postrenal segment of the inferior vena cava. The cords of cells that pass deeply between the capillaries and sinusoids. continuity of the vessel is maintained by the persistence of the anasto­ The cells in these cords degenerate in an erratic fashion as they pass mosis between the right supracardinal and the right subcardinal in the towards the medulla, becoming granular, eosinophilic and, ultimately, renal collar. The left supracardinal disappears, but some of the renal autolysed. These cords of cells constitute the fetal cortex, which under­ collar formed by the left supracardinal–subcardinal anastomosis per­ goes rapid involution during the first 2 years after birth. The fascicular sists in the left renal vein. Both supracardinal veins drain cranially into and reticular zones of the adult cortex are proliferated from the glomer­ the subcardinal veins. On the right side, the subcardinal vein comes ular zone after birth. Serial ultrasound measurements of the length of into intimate relationship with the liver. An extension of the vessel takes fetal suprarenal glands at 4­week intervals from the fifteenth week of place in a cranial direction and meets and establishes continuity with gestation have been published (van Vuuren et al 2012). a corresponding new formation that is growing caudally from the right
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inferior vena cava, portal circulation and umbilical vessels 1065 06 RETPAHC Brachiocephalic veins A B Superior intercostal vein Internal jugular veins Oblique vein Superior and ligament vena cava of left atrium Azygos vein IVC hepatic Postcardinal vein segment IVC subhepatic segment Hemiazygos vein IVC subcardinal Remains of intersubcardinal segment anastomosis (renal collar) Left suprarenal vein Left supracardinal vein Left renal vein Oblique transverse anastomosis Left gonadal vein IVC supracardinal segment Postcardinal vein Supracardinal vein (thoracolumbar line vein) Common iliac veins Azygos line vein (medial sympathetic line vein) Subcardinal vein Hepatic segment of inferior vena cava (and right vitelline vein) Subhepatic segment of IVC Fig. 60.8 The inferior vena cava (IVC) develops within the posterior abdominal wall. It is a composite vessel formed by temporal remodelling of successive somatic venous anastomoses. A, The progressive asymmetry of the developing venous system. B, The definitive venous arrangement. (For early venous development, see Fig. 13.4.) vitelline hepatocardiac (common hepatic) vein. In this way, on the right embryonic arrangement occur with the growth of the foregut, liver and side, a more direct route is established to the heart and the prerenal paired viscera, i.e. kidneys and suprarenal glands. (cranial) segment of the inferior vena. In summary, the inferior vena The early development of the ventral splanchnic arteries is outlined cava is formed from below upwards by the confluence of: the common in Chapter 13. Three main arterial trunks – the coeliac trunk, superior iliac veins, a short segment of the right postcardinal vein, the mesenteric and inferior mesenteric arteries – supply the fore­, mid­ and postcardinal–supracardinal anastomosis, part of the right supracardinal hindgut, respectively. From the gastric terminal segment of the future vein, the right supracardinal–subcardinal anastomosis, right subcardi­ oesophagus to the upper rectum, the developing endodermal epithe­ nal vein, a new anastomotic channel of double origin (the hepatic lium is surrounded by splanchnopleuric mesenchyme permeated by a segment of the inferior vena cava), and the cardiac termination of the capillary plexus that drains into an anastomosing network of veins. This right vitelline hepatocardiac vein (common hepatic vein). plexus is particularly dense ventrally where it is associated with the Only the supracardinal part of the inferior vena cava receives central midgut region; here, for a while, it receives a network of small intersegmental venous drainage. The postrenal (caudal) segment of the veins from the definitive yolk sac. Later, in normal development, these inferior vena cava is on a plane that lies dorsal to the plane of the vessels atrophy as the yolk sac diminishes. More rostrally, the splanch­ prerenal (cranial) segment. Thus, the right phrenic, suprarenal and nopleuric capillaries associated with the foregut and upper portions of renal arteries, which represent persistent mesonephric arteries, pass the yolk sac form longitudinal channels anterolateral to the gut and behind the inferior vena cava, whereas the testicular or ovarian artery, these become increasingly well defined as the embryonic abdominal which has a similar developmental origin, passes anterior to it. vitelline veins. Entering the septum transversum, the right and left vitel­ In some animals, the right postcardinal vein constitutes a large part line veins incline slightly, becoming parallel to the lateral aspects of the of the postrenal segment of the inferior vena cava. In these cases, the gut. They establish connections with capillary plexuses in the septal right ureter, on leaving the kidney, passes medially dorsal to the vessel mesenchyme, and then continue, finally curving to enter the medial and then, curving round its medial side, crosses its ventral aspect. part of the cardiac sinual horn of their corresponding side. The parts of Rarely, a similar condition is found in humans, and indicates the per­ the gut closely related to the presinual segments of the vitelline veins sistence of the right postcardinal vein and failure of the right supracar­ are the future subdiaphragmatic end of the oesophagus, primitive dinal to play its normal part in the development of the inferior vena stomach, the superior (first) and descending (second) regions of the cava. duodenum, and the remainder of the duodenal tube. The principal ascending vitelline veins flanking the sides of the abdominal part of the foregut receive venules from its splanchnopleuric PORTAL CIRCULATION capillaries and those of the septal mesenchyme. Within these venular nets, enlarged (but still plexiform) anastomoses connect the two vitel­ The heart first differentiates in splanchnopleure that, after head­fold line veins (Fig. 60.9; see Fig. 13.1C). A subdiaphragmatic intervitelline formation, forms the dorsal wall of the primitive pericardial cavity anastomosis develops in the rostral septal mesenchyme, lying a little (floor of the rostral foregut) and may, therefore, be considered a highly caudal to the cardiac sinuatrial chamber, connecting the veins near their specialized vitelline vascular derivative. At the caudal extremity of the sinual terminations. (The channel is sometimes termed suprahepatic splanchnopleuric gut tube (the future lower rectum and upper anal because of the position of the hepatic primordium; with expansion of canal), the vitelline venous drainage makes connections with the inter­ the latter, it becomes partly intrahepatic.) The presumptive duodenum nal iliac radicles of the postcardinal complex. is crossed by three transverse duodenal intervitelline anastomoses. Their The development of the gut occurs contemporaneously with changes relation to the gut tube alternates so that the most cranial, the subhe­ to the early symmetrical embryonic circulation (Ch. 13). A symmetrical, patic, is ventral, the intermediate is dorsal and the caudal is ventral (Fig. segmental system of somatic arteries remains and supplies the body 60.9B). It has become customary to describe the paraduodenal vitelline wall of the trunk. The underlying arrangement of these vessels is only veins and their associated anastomoses as forming a figure eight. At this slightly modified by subsequent development. The main changes to the early stage, when left and right embryonic veins are still symmetrical,
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DEvEloPmEnT of THE PERiTonEAl CAviTy, gAsTRoinTEsTinAl TRACT AnD iTs ADnExAE 1066 8 noiTCEs A Common sinuatrial chamber B Parts that persist, expand and modify into main permanent Sinus venosus: right horn channels Right New connections forming further main precardinal vein permanent channels Site of hepatic rudiment, which expands Right common cardinal vein INTERVITELLINE and invades neighbouring anastomoses, ANASTOMOTIC vitelline and umbilical veins Right VEINS postcardinal vein 1 Subdiaphragmatic Oxygenated blood (suprahepatic) Early ductus venosus Deoxygenated blood Right 2 Subhepatic, ventral Right vitelline duodenal umbilical vein vein 3 Intermediate, dorsal Region of future duodenal duodenum 4 Caudal, central duodenal Fig. 60.9 Development of the vitelline, umbilical and terminal cardinal vein complexes: the early symmetrical condition. A, The early symmetrical arrangement of cardinal and umbilical veins entering the sinus venosus; blood from the yolk sac passes, via vitelline veins, through anastomoses forming in the septum transversum mesenchyme (green). B, The developing duodenum is surrounded by transverse duodenal intervitelline anastomoses. Changes in the developing gut and umbilical veins cause shifts in the routes taken by venous blood flowing to the sinus venosus. Right half of subdiaphragmatic anastomosis Progressive inflection of sinuatrial wall Right precardinal and common cardinal veins Left precardinal and common cardinal veins Right postcardinal vein Postcardinal vein Hepatocardiac part of right umbilical vein Hepatocardiac part of left umbilical vein Left venae revehentes Right hepatocardiac vein (termination of Hepatocardiac part of left vitelline vein right vitelline vein – future inferior vena cava) Hepatic terminals of left vitelline vein Left venae advehentes Hepatic terminal right umbilical vein Hepatic terminals of left umbilical vein Vitelline vein segments and ventral anastomosis New venous connections Left umbilical vein Presumptive splenic vein Merge to form root of Presumptive superior mesenteric vein definitive hepatic portal vein Parts that persist, expand and modify into main permanent channels New connections forming further main permanent channels Oxygenated blood Deoxygenated blood Fig. 60.10 Development of the vitelline, umbilical and terminal cardinal vein complexes: a mid-stage of asymmetry has been reached between the early symmetrical condition (see Fig. 60.9) and the definitive late prenatal state. The extent of the liver within the septum transversum mesenchyme is shown in green. the cranial duodenal anastomosis becomes connected with the subdia­ CHANGES IN THE VITELLO-UMBILICAL VEINS phragmatic anastomosis by a median longitudinal channel, the primi­ tive median ductus venosus, which is dorsal to the expanding hepatic Progressive changes in the vitello­umbilical veins are rapid, profound primordium but ventral to the gut. The further development of the and closely linked with regional modifications in shape and position vitelline veins and anastomoses is, as indicated, closely interlocked, of the gut, expansion and invasion of venous channels by hepatic tissue, with rapid hepatic expansion and gut changes, and umbilical vein dis­ asymmetry of the heart and cardiac venous return. The principal events position and modification is closely involved. are summarized in Figures 60.9–60.11.
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inferior vena cava, portal circulation and umbilical vessels 1067 06 RETPAHC Superior vena cava Left atrium Fig. 60.11 The condition of some main upper abdominal and intrathoracic right atrial terminal Coronary sinus veins in the later prenatal months. The rotation of Right atrium Secondary upper left hepatic vein the stomach and movement of the duodenum produce relative changes in the final arrangement Inferior vena cava of the duodenal intervitelline anastomoses that form the hepatic portal vein. Upper right hepatic vein Ductus venosus Lower right hepatic vein Persistent left afferent hepatic veins Left umbilical vein Portal vein formed from the Splenic vein final arrangement of anterior, left and posterior anastomoses around the duodenum Superior mesenteric vein Duodenum Oxygenated blood Deoxygenated blood From the cranial portion of the early hepatic evagination of the fibrous tags attached to the inferior wall of the coronary sinus. The right foregut, interconnected sheets and ‘cords’ of endodermal cells, the pre­ vitelline hepatocardiac vein continues enlarging and, ultimately, forms sumptive hepatocytes, penetrate the septum transversum mesenchyme. the terminal segment of the inferior vena cava. The latter receives the Hepatic mesenchyme is composed of a mixed population of cells with right efferent hepatic veins and new channels draining the territories of endothelial/angiogenic and connective tissue lineages. Capillary plex­ the left efferent hepatic veins. These collectively form the upper and uses develop within this mesenchyme and, possibly under the influence lower groups of right and (secondary) left hepatic veins. The terminal of the endodermal hepatic sheets, the plexuses become more profuse caval segment also shows the orifice of the right half of the intervitelline by further addition of angioblastic septal mesenchyme, which also subdiaphragmatic anastomosis, and a large new connection with the forms masses of perivascular intrahepatic haemopoietic tissue. These right subcardinal vein. processes extend along the plexiform connections of the vitelline, and The hepatic terminals of the right and left duodenal parts of the later the umbilical, veins until their intrahepatic (trans­septal) zones vitelline veins are destined to form the corresponding branches of the themselves become largely plexiform. Initially capillary in nature, they hepatic portal vein, the left branch incorporating the cranial ventral transform into a mass of rather wider, irregular, sinusoidal vessels with intervitelline anastomosis. With rotation of the gut and formation of a discontinuous endothelium containing many phagocytic cells. The the duodenal loop, segments of the original vitelline veins and the lengths of vitelline veins involved in these processes are the intermedi­ caudal transverse anastomosis atrophy (indicated in Figs 60.10–60.11), ate parts of the segments extending from the subhepatic (cranioventral while new splanchnopleuric venous channels – the superior mesenteric duodenal) to the suprahepatic (subdiaphragmatic) transverse intervitel­ and splenic veins – converge and join the left end of the dorsal inter­ line anastomoses, and the corresponding lengths of the umbilical veins. mediate anastomosis. The numerous other radicles of the portal vein Thus, at this early stage, the liver sinusoids are perfused by mixed blood and its principal branches, including the inferior mesenteric vein, are reaching them through a series of branching vessels collectively called later formations. the venae advehentes, or afferent hepatic veins: they are deoxygenated For a period, placental blood returns from the umbilicus via right from the gut splanchnopleure via vitelline vein hepatic terminals, and and left umbilical veins, both discharging through afferent hepatic veins oxygenated from the placenta via hepatic terminals of the umbilical into the hepatic sinusoids, where admixture with vitelline blood occurs. veins (see Fig. 60.10). Blood leaves the liver through four venae reve­ At approximately 7 mm crown–rump length, the right umbilical vein hentes (efferent hepatic veins); two on each side reach and open into retrogresses completely. The left umbilical vein retains some vessels their respective cardiac sinual horns. This full complement of four discharging directly into the sinusoids, but new enlarging connections hepatocardiac veins is only transient and becomes reduced to one with the left half of the subhepatic intervitelline anastomosis emerge. dominant, rapidly enlarging channel. The originally bilaterally sym­ The latter is the start of a bypass channel for the majority of the pla­ metrical cardinal vein complexes, both rostral and caudal, develop cental blood, which continues through the median ductus venosus and, transverse or oblique anastomoses so that the cardiac venous return is finally, the right half of the subdiaphragmatic anastomosis, to reach the ultimately restricted to the definitive right atrium. termination of the inferior vena cava (see Fig. 60.11). These cardiac and concomitant hepatoenteric changes are accompa­ The left and right hepatic portal veins and the ductus venosus are nied by events in supra­, intra­ and subhepatic parts of the vitello­ routinely observed in the second trimester ultrasound scan at the plane umbilical veins. Some vessels enlarge, persisting as definitive vessels to to estimate abdominal circumference (see Fig. 14.4G). maturity; in places, they are joined later by other channels that become defined in already established capillary plexuses. Other vessels retro­ FETAL/NEONATAL UMBILICAL VESSELS gress, either disappearing completely or remaining as vestigial tags and, occasionally, vessels of fine calibre. Some vessels of crucial importance Umbilical arteries in the circulatory patterns of embryonic and fetal life become obliter­ ated postnatally and transformed to substantial fibrous cords. Both right and left umbilical hepatocardiac and the left vitelline hepatocar­ The fetal umbilical arteries are in direct continuation with the internal diac veins continue, for a time, to discharge blood into their sinual iliac arteries. Their lumen is 2–3 mm in diameter at their origin, when horns; however, they begin to retrogress (see Figs 60.9–60.10). The right distended. This narrows as they approach the umbilicus, where there is umbilical channel atrophies completely. The left channels also disap­ a reciprocal thickening of the tunica media, as a result, in particular, of pear, but their cardiac terminals may, on occasion, be found as conical an increase in the number of longitudinal smooth muscle fibres and
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DEvEloPmEnT of THE PERiTonEAl CAviTy, gAsTRoinTEsTinAl TRACT AnD iTs ADnExAE 1068 8 noiTCEs Table 60.1 Key anatomical reference points for umbilical arterial catheterization Umbilical vein Structure Vertebral level The umbilical vein in the neonate is 2–3 cm long and 4–5 mm in Ductus arteriosus T4–5 diameter when distended. It passes from the umbilicus, within the layers Coeliac artery T12 of the falciform ligament, superiorly and to the right, to the porta hepatis. Superior mesenteric artery T12–L1 Here, it gives off several large intrahepatic branches to the liver and then Renal artery L1 joins the left branch of the portal vein and the ductus venosus. The Inferior mesenteric artery L3 umbilical vein is thin­walled; it possesses a definite internal lamina of Aortic bifurcation L4–5 elastic fibres at the umbilical ring but not in its intra­abdominal course. The tunica media contains smooth muscle fibres, collagen and elastic fibres. When the cord is severed, the umbilical vein contracts, but not elastic fibres. Before birth, there is a proliferation of connective tissue so vigorously as the arteries. The rapid decrease in pressure in the umbili­ within the vessel wall. The umbilical vessels constrict in response to cal vein after the cord is clamped means that the elastic tissue at the handling, stretching, cooling and altered tensions of oxygen and carbon umbilical ring is sufficient to arrest any retrograde flow along the vessel. dioxide. Umbilical vessels are muscular, but devoid of a nerve supply Before birth, there is a subintimal proliferation of connective tissue. in their extra­abdominal course. After the cord is severed, the umbilical After birth, the contraction of the collagen fibres in the tunica media arteries contract, preventing significant blood loss; thrombi often form and the increased subintimal connective tissue contribute to the trans­ in the distal ends of the arteries. The arteries obliterate from their distal formation of the vessel into the ligamentum teres. Obliteration occurs ends until, by the end of the second or third postnatal month, involu­ from the umbilical ring towards the hepatic end. No thrombi are formed tion has occurred at the level of the superior vesical arteries. The proxi­ in the obliteration process. For up to 48 hours after birth, the intra­ mal parts of the obliterated vessels remain as the medial umbilical abdominal portion of the umbilical vein can be easily dilated. In most ligaments. adults, the original lumen of the vein persists through the ligamentum teres and can be dilated to 5–6 mm in diameter. Umbilical arterial catheterization Insertion of an umbilical catheter is undertaken to provide direct access Ductus venosus to the arterial circulation. Arterial blood can be withdrawn repeatedly The ductus venosus is a direct continuation of the umbilical vein and for measurement of oxygen and carbon dioxide partial pressures, pH, arises from the left branch of the portal vein, directly opposite the base excess and many other parameters of blood biochemistry and termination of the umbilical vein. It passes for 2–3 cm within the layers haematology. The indwelling catheter also enables the continuous of the lesser omentum, in a groove between the left lobe and caudate measurement of arterial blood pressure. lobe of the liver, before terminating in either the inferior vena cava, or The catheter is inserted directly into either the cut end or the side of in the left hepatic vein immediately before it joins the inferior vena one of the two umbilical arteries in the umbilical cord stump that cava. The tunica media of the ductus venosus contains circularly remains attached to the baby after transection of the umbilical cord at arranged smooth muscle fibres, an abundant amount of elastic fibres the time of delivery. The catheter tip is then advanced along the length and some connective tissue. of the umbilical artery, through the internal iliac artery, into the The ductus venosus is already closed in about one­third of newborn common iliac artery and, from there, into the aorta. In order to keep infants. It shuts down by an unknown mechanism. Obliteration begins the catheter patent, a small volume of fluid is continuously infused at the portal vein end in the second postnatal week and progresses to through it. It is important for the tip of the catheter to be located well the vena cava; the lumen has been completely obliterated by the second away from arteries branching from the aorta, to avoid potentially or third month after birth. The fibrous remnant of the ductus venosus harmful perfusion of these arteries with the catheter fluid. Thus, umbili­ is the ligamentum venosum. cal arterial catheter tips are placed in the descending aorta either in a Umbilical vein catheterization ‘high’ position, above the coeliac artery but well below the ductus arte­ riosus, or in a ‘low’ position, below the renal and inferior mesenteric The umbilical vein may be catheterized in the neonate to enable arteries but above the point where the aorta bifurcates into the two exchange and transfusion of blood, for central venous pressure meas­ common iliac arteries. The length of catheter to be inserted can be urement and, usually in an emergency, for vascular access. The catheter estimated from charts relating the required catheter length to external is inserted into the cut end of the umbilical vein and is advanced along body measurements, or from birth weight. Positioning of the catheter the length of the vein, through the ductus venosus and into the inferior is assessed by means of radiographs of the abdomen or chest: a ‘high’ vena cava; the tip is placed between the ductus venosus and the right catheter tip should be located in the descending aorta somewhere atrium. Positioning of the catheter tip is confirmed radiologically and between the levels of the sixth and ninth thoracic vertebrae (T6–9), it should be located just above the diaphragm at a point that is level while a ‘low’ catheter tip should be at a level between the third and with the ninth or tenth thoracic vertebra (T9/T10). As with umbilical fourth lumbar vertebrae (L3–4). Relevant anatomical reference points arterial catheters, estimation of the required catheter length can be are given in Table 60.1. determined from standard charts. KEY REFERENCES Collins P 2002a Embryology of the pancreas. In: Howard ER, Stringer MD, Lebenthal E 1989 Concepts in gastrointestinal development. In: Lebenthal Colombani PM (eds) Surgery of the Liver, Bile Ducts and Pancreas in E (ed) Human Gastrointestinal Development. New York: Raven Press; Children, Part 8. London: Arnold, pp. 479–92. Ch. 1. Covers pancreatic morphogenesis, the timescale of development, the origin of This chapter is the first in a volume dedicated to the development of pancreatic cell lines and factors that regulate pancreatic development. structure and function of the gut, liver and pancreas. It includes the development of the immunological surveillance mechanisms and Collins P 2002b Embryology of the liver and bile ducts. In: Howard ER, gastrointestinal flora. Stringer MD, Colombani PM (eds) Surgery of the Liver, Bile Ducts and Pancreas in Children, Part 3. London: Arnold, pp. 91–102. Neu J (ed) 2012 Gastroenterology and Nutrition: Neonatology Questions Covers morphogenesis of the liver and early hepatic circulation, the origin of and Controversies, 2nd ed. Philadelphia: Elsevier, Saunders. hepatic cell lines and the development of the extra- and intrahepatic biliary Contains a comprehensive range of articles on the development and systems. maturation of the gut. Gershon MD 2010 Developmental determinants of the independence and O’Rahilly R, Müller F 1987 Developmental Stages in Human Embryos. complexity of the enteric nervous system. Trends Neurosci 33:446–56. Washington: Carnegie Institution. This paper reviews the molecular basis of normal and defective enteric Streeter GL 1942 Developmental horizons in human embryos. Descriptions nervous system development. of age group XI, 13 to 20 somites, and age group XII, 21 to 29 somites. Contrib Embryol Carnegie Inst Wash 30:211–45. Howard ER 2002 Biliary atresia: aetiology, management and complications. In: Howard ER, Stringer MD, Colombani PM (eds) Surgery of the Liver, Whittle MJ 1999 Gastrointestinal abnormalities. In: Rodeck CH, Whittle MJ Bile Ducts and Pancreas in Children, Part 3. London: Arnold, (eds) Fetal Medicine: Basic Sciences and Clinical Practice. Edinburgh: pp. 103–32. Elsevier, Churchill Livingstone; Ch. 54, pp. 703–14. Reviews the aetiology and clinical presentation of biliary atresia, including the Reviews the diagnosis and treatment of anomalies of the gastrointestinal tract. congenital, infective and anatomical factors that are related to the condition.
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Development of the peritoneal cavity, gastrointestinal tract and its adnexae 1068.e1 06 RETPAHC REFERENCES Bäckhed F, Roswall J, Peng Y et al 2015 Dynamics and stabilization of the Lemaigre FP 2009 Mechanisms of liver development: concepts for under­ human gut microbiome during the first year of life. Cell Host Microbe standing liver disorders and design of novel therapies. Gastroenterology 17:690–703. 137:62–71. Ben­David S, Zuckerman­Levin N, Epelman M et al 2007 Parturition itself Lewis P, Yaron Y, Evans MI 1999 Fetal endocrine disorders. In: Rodeck CH, is the basis for fetal adrenal involution. J Clin Endocrinol Metab 92: Whittle MJ (eds) Fetal Medicine: Basic Sciences and Clinical Practice. 93–7. Edinburgh: Elsevier, Churchill Livingstone; Ch. 62, pp. 829–34. Burns AJ, Roberts RR, Bornstein JC et al 2009 Development of the enteric Martin CR, Caicedo Ra, Walker WA 2012 Development of the intestinal nervous system and its role in intestinal motility during fetal and early mucosal barrier. In: Neu J (ed) Gastroenterology and Nutrition: Neona­ postnatal stages. Semin Pediatr Surg 18:196–205. tology Questions and Controversies, 2nd ed. Philadelphia: Elsevier, Butzner JD, Befus AD 1989 Interactions among intraepithelial leucocytes Saunders; Ch. 4, pp. 39–58. and other epithelial cells in intestinal development and function. In: McLin VA, Henning SJ, Jamrich M 2009 The role of the visceral mesoderm Lebenthal E (ed) Human Gastrointestinal Development. New York: in the development of the gastrointestinal tract. Gastroenterology Raven Press; Ch. 37. 136:2074–91. Collins P 2002a Embryology of the pancreas. In: Howard ER, Stringer MD, Neu J (ed) 2012 Gastroenterology and Nutrition: Neonatology Questions Colombani PM (eds) Surgery of the Liver, Bile Ducts and Pancreas in and Controversies, 2nd ed. Philadelphia: Elsevier, Saunders. Children, Part 8. London: Arnold, pp. 479–92. Contains a comprehensive range of articles on the development and Covers pancreatic morphogenesis, the timescale of development, the origin of maturation of the gut. pancreatic cell lines and factors that regulate pancreatic development. Neu J, Mai V 2012 The developing intestinal microbiome and its relation­ Collins P 2002b Embryology of the liver and bile ducts. In: Howard ER, ship to health and disease. In: Neu J (ed) Gastroenterology and Nutri­ Stringer MD, Colombani PM (eds) Surgery of the Liver, Bile Ducts and tion: Neonatology Questions and Controversies, 2nd ed. Philadelphia: Pancreas in Children, Part 3. London: Arnold, pp. 91–102. Elsevier, Saunders; Ch. 5, pp. 59–65. Covers morphogenesis of the liver and early hepatic circulation, the origin of O’Rahilly R, Müller F 1987 Developmental Stages in Human Embryos. hepatic cell lines and the development of the extra- and intrahepatic biliary Washington: Carnegie Institution. systems. Patel RM, Neish As, Lin P 2012 The developing intestine as an immune Gershon MD 2010 Developmental determinants of the independence and organ. In: Neu J (ed) Gastroenterology and Nutrition: Neonatology complexity of the enteric nervous system. Trends Neurosci 33: 446–56. Questions and Controversies, 2nd ed. Philadelphia: Elsevier, Saunders; This paper reviews the molecular basis of normal and defective enteric Ch. 6, pp. 67–89. nervous system development. Rodríguez JM, Murphy K, Stanton C et al 2015 The composition of the gut Gritz EC, Bhandari V 2015 The human neonatal gut microbiome: a brief microbiota throughout life, with an emphasis on early life. Microb Ecol review. Front Pediatr 3:17. Health Dis 2015;26 26050 doi: 10.3402/mehd.v26.26050. Hikspoors JP, Soffers JH, Mekonen HK et al 2015 Development of the Satoh T, Sakurai E, Tada H et al 2009 Ontogeny of reticular framework of human infrahepatic inferior caval and azygos venous systems. J Anat white pulp and marginal zone in human spleen: immunohistochemical 226:113–25. studies of fetal spleens from the 17th to 40th week of gestation. Cell Tissue Res 336:287–97. Hitchcock RJI, Pemble MJ, Bishop AE et al 1992 Quantitative study of the development and maturation of human oesophageal innervation. Steiniger B, Ulfig N, Risse M et al 2007 Fetal and early post­natal develop­ J Anat 180:175–83. ment of the human spleen: from primordial arterial B cell lobules to a non­segmented organ. Histochem Cell Biol 128:205–15. Howard ER 2002 Biliary atresia: aetiology, management and complications. In: Howard ER, Stringer MD, Colombani PM (eds) Surgery of the Liver, Streeter GL 1942 Developmental horizons in human embryos. Descriptions Bile Ducts and Pancreas in Children, Part 3. London: Arnold, of age group XI, 13 to 20 somites, and age group XII, 21 to 29 somites. pp. 103–32. Contrib Embryol Carnegie Inst Wash 30:211–45. Reviews the aetiology and clinical presentation of biliary atresia, including Turan OM, Turan S, Funai EF et al 2007 Fetal adrenal gland volume: a novel the congenital, infective and anatomical factors that are related to the method to identify women at risk for impending preterm birth. Obstet condition. Gynecol 109:855–62. Ionescu S, Mocanu M, Andrei B et al 2014 Differential diagnosis of abdomi­ Turan OM, Turan S, Buhimschi IA et al 2012 Comparative analysis of 2­D nal wall defects – omphalocele versus gastroschisis. Chirurgia (Bucur) versus 3­D ultrasound estimation of the fetal adrenal gland volume and 109:7–14. prediction of preterm birth. Am J Perinatol 29:673–80. Kabouridis PS, Lasrado R, McCallum S 2015 Microbiota controls the Vaarala O 2012 The developing gastrointestinal tract in relation to autoim­ homeostasis of glial cells in the gut lamina propria. Neuron 85: mune disease, allergy, and atopy. In: Neu J (ed) Gastroenterology and 289–95. Nutrition: Neonatology Questions and Controversies, 2nd ed. Philadel­ phia: Elsevier, Saunders; Ch. 7, pp. 91–9. Kim WK, Kim H, Ahn DH et al 2003 Timetable for intestinal rotation in staged human embryos and fetuses. Birth Defects Res A Clin Mol Teratol van Vuuren SH, Damen­Elias HA, Stigter RH et al 2012 Size and volume 67:941–5. charts of fetal kidney, renal pelvis and adrenal gland. Ultrasound Obstet Gynecol 40:659–64. Kolterud A, Grosse AS, Zacharias WJ et al 2009 Paracrine hedgehog signal­ ling in stomach and intestine: new roles for hedgehog in gastrointestinal Whittle MJ 1999 Gastrointestinal abnormalities. In: Rodeck CH, Whittle MJ patterning. Gastroenterology 137:618–28. (eds) Fetal Medicine: Basic Sciences and Clinical Practice. Edinburgh: Elsevier, Churchill Livingstone; Ch. 54, pp. 703–14. Lebenthal E 1989 Concepts in gastrointestinal development. In: Lebenthal Reviews the diagnosis and treatment of anomalies of the gastrointestinal E (ed) Human Gastrointestinal Development. New York: Raven Press; tract. Ch. 1. This chapter is the first in a volume dedicated to the development of Wynn JL, Neu J 2012 The neonatal gastrointestinal tract as a conduit to structure and function of the gut, liver and pancreas. It includes the systemic inflammation and developmental delays. In: Neu J (ed) Gas­ development of the immunological surveillance mechanisms and troenterology and Nutrition: Neonatology Questions and Controver­ gastrointestinal flora. sies, 2nd ed. Philadelphia: Saunders; Ch. 19, pp. 293–304.
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CHAPTER 61 Anterior abdominal wall The anterior abdominal wall constitutes a hexagonal area defined supe- adherent to the linea alba and pubic symphysis. Inferiorly, it fuses riorly by the costal margins and xiphoid process, laterally by the mid- with the iliac crest, extends superficial to the inguinal ligament and axillary line, and inferiorly by the iliac crests, pubis and pubic symphysis. fuses with the fascia lata at the inguinal flexure or skin crease of the It is continuous with the posterior abdominal wall and paravertebral thigh. In the male, it extends on to the dorsum of the penis, forming tissues, forming a flexible sheet of skin, muscle and connective tissue part of the superficial ligament of the penis, and on to the scrotum, across the anterior and lateral aspects of the abdomen. These tissues where it becomes continuous with the membranous layer of superfi- also form the umbilicus and the inguinal canal, which connects the cial fascia of the perineum (Colles’ fascia). In the female, it continues abdominal cavity to the scrotum in men or to the labia majora in into the labia majora and is continuous with the fascia of the women. The anterior abdominal wall maintains the shape of the perineum. abdomen and aids numerous physiological functions. However, its In boys, the testis can frequently be retracted out of the scrotum into dysfunction is equally notable because hernia repair is the single most the loose areolar tissue between the membranous layer of superficial common operation performed by general surgeons. fascia over the inguinal canal and the external oblique aponeurosis. This ‘space’ is sometimes called the superficial inguinal pouch. Deep adipose layer SKIN AND SOFT TISSUE The thickness of the deep adipose layer is more variable than the super- ficial fatty layer. It is thin or absent where the membranous layer fuses The integument of the anterior abdominal wall comprises skin, soft with bony prominences and the linea alba, and becomes markedly tissues, and lymphatic and vascular structures, as well as segmental thick in the morbidly obese. Its adipocytes show different metabolic nerves. The outer layer is formed from the skin and subcutaneous fat. activities to those in the superficial adipose layer (Chopra et al 2011). The skin is non-specialized and variably hirsute, depending on sex and Liposuction preferentially removes this layer of fat with relative preser- race. All postpubertal individuals have some extension of the pubic hair vation of the superficial adipose layer in order to avoid skin dimpling on to the anterior abdominal wall skin, although this is commonly and other skin contour irregularities (Markman and Barton 1987). most pronounced in males, in whom the hair may extend almost up to the umbilicus in a triangular pattern. The subcutaneous fat of the abdominal wall is highly variable in thickness, depending in part on Transversalis fascia gender and adiposity. The transversalis fascia is a thin layer of connective tissue lying between the deep surface of transversus abdominis and the extraperitoneal fat. SOFT TISSUE It is part of the general layer of thin fascia between the peritoneum and the abdominal wall. Posteriorly, it fuses with the anterior layer of the Superficial fascia thoracolumbar fascia (p. 1083), and anteriorly, it forms a continuous sheet. Superiorly, it blends with the fascia covering the inferior surface The ‘superficial fascia’ of the abdominal wall lies between the dermis of the diaphragm. Inferiorly, it is continuous with the iliac and pelvic and the muscles, and is conventionally divided into a superficial fatty parietal fasciae, and is attached to the iliac crest between the origins layer (Camper’s fascia) and a deep membranous layer (Scarpa’s fascia). of transversus abdominis and iliacus, and to the posterior margin of In reality, there are three layers, with a further layer of adipose tissue the inguinal ligament between the anterior superior iliac spine and the deep to the membranous layer (Lancerotto et al 2011). These three femoral sheath. Medial to the femoral sheath it is thin and fused to the layers are particularly well defined in the child. Lying within the super- pubis behind the conjoint tendon. An inferior extension of the trans- ficial fascia are blood vessels, lymphatics, nerves and, in the region of versalis fascia forms the anterior part of the femoral sheath. The fascia the groin, superficial inguinal lymph nodes. displays a discrete thickening known as the iliopubic tract (also called the deep crural arch), which runs parallel to the inguinal ligament Superficial adipose layer (Teoh et al 1999); it consists of transverse fibres that fan out laterally The superficial layer contains a variable amount of fat that is partitioned towards the anterior superior iliac spine to blend with the iliopsoas by fibrous septa connecting the dermis with the deeper membranous fascia and run medially behind the conjoint tendon to the pubic bone. layer. Inferiorly, it is continuous with the superficial fascia of the thigh, The iliopubic tract is recognized as an important structure during open and medially, it is continuous over the linea alba. In the male, this layer and laparoscopic inguinal hernia repair. A further thickening of the continues over the external genitalia, where it becomes thin and pale transversalis fascia, the interfoveolar ligament, runs inferior to the red, and contains very little adipose tissue. In the scrotum it also con- inguinal ligament at the medial margin of the deep inguinal ring; it tains the smooth muscle fibres of the dartos muscle. In the female, it may contain muscle fibres. continues from the suprapubic region of the abdomen into the labia The transversalis fascia is prolonged as the internal spermatic fascia majora and perineum. over the structures that pass through the deep inguinal ring (the testicu- lar vessels and vas (ductus) deferens in the male and the round ligament Membranous layer of the uterus in the female). The membranous layer is a variably developed entity composed of connective tissue and elastic fibres. In the adult, its thickness varies Extraperitoneal connective tissue over the anterior abdominal wall, becoming thinner in the upper abdomen (Lancerotto et al 2011). Measured histologically, it is between 0.5 and 1 mm thick but it appears thicker on computed tomography The extraperitoneal connective tissue lying between the peritoneum and (CT) scans (Lancerotto et al 2011, Chopra et al 2011). It is loosely con- the fasciae lining the abdominal and pelvic cavities contains a variable nected to the underlying external oblique aponeurosis and rectus amount of fat. The fat is especially abundant on the posterior wall of sheath by oblique fibrous septa. Superiorly, it is continuous with the the abdomen around the kidneys (particularly in obese men) and superficial fascia over the remainder of the trunk. In the midline, it is scanty above the iliac crest and in much of the pelvis. 1069
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Anterior AbdominAl wAll 1070 8 noitCeS Superficial vessels Deep vessels Subclavian artery and vein Internal thoracic artery and vein Intercostal artery and vein Axillary vein Lateral thoracic vein Musculophrenic artery and vein Superior epigastric artery and vein Thoracoepigastric vein Subcostal artery and vein Inferior epigastric artery and vein Superficial epigastric artery and vein Deep circumflex iliac artery and vein Superficial circumflex iliac artery and vein External iliac artery and vein Superficial external pudendal artery and vein Femoral artery and vein Long (great) saphenous vein Fig. 61.1 The blood supply of the anterior abdominal wall. VASCULAR SUPPLY AND LYMPHATIC DRAINAGE artery also gives small branches to the anterior part of the diaphragm. On the right, small branches reach the falciform ligament, where they Understanding the blood supply of the abdominal wall is critical when anastomose with branches from the hepatic artery. planning incisions, raising myocutaneous flaps and reconstructing the abdominal wall during ventral hernia repair (Fig. 61.1). Inferior epigastric artery and veins Superior epigastric artery and veins The inferior epigastric artery (often referred to as the deep inferior The superior epigastric artery is a terminal branch of the internal tho- epigastric artery in clinical practice in order to distinguish it from the racic artery. It arises at the level of the sixth costal cartilage and descends superficial (inferior) epigastric artery) originates from the medial aspect between the costal and xiphoid slips of the diaphragm, accompanied of the external iliac artery just proximal to the inguinal ligament (see by two or more veins that drain to the internal thoracic vein (see Figs 61.1–61.2; Fig. 61.3). Its accompanying veins, usually two, unite Fig. 61.1; Fig. 61.2). The vessels pass anterior to the lower fibres of to form a single vein that drains into the external iliac vein (Rozen et al transversus thoracis and the upper fibres of transversus abdominis 2009). It curves forwards in the anterior extraperitoneal tissue and before entering the rectus sheath, where they run inferiorly behind ascends obliquely along the medial margin of the deep inguinal ring. rectus abdominis. They anastomose with the inferior epigastric arteries, It lies posterior to the spermatic cord, separated from it by the transver- usually above the level of the umbilicus, in one of several potential salis fascia. It pierces the transversalis fascia and enters the rectus sheath branching patterns (Rozen et al 2008). by passing anterior to the arcuate line. In this part of its course, it is Branches supply rectus abdominis and perforate the anterior lamina visible through the parietal peritoneum of the anterior abdominal wall of the rectus sheath to supply the abdominal skin. A branch given off and forms the lateral umbilical fold. Disruption of the artery at this site in the upper rectus sheath passes anterior to the xiphoid process of the by surgical incisions (e.g. insertion of laparoscopic ports or abdominal sternum and anastomoses with a corresponding contralateral branch. drains) may result in a haematoma that can expand to considerable size This vessel may give rise to bleeding during surgical incisions that because of the absence of adjacent tissue against which the bleeding extend up to and alongside the xiphoid process. The superior epigastric can be tamponaded.
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Anterior abdominal wall 1070.e1 16 retPAHC The vascular supply to the anterior abdominal wall can be divided into three zones. Zone I represents the epigastrium and central anterior abdominal wall within the region of rectus abdominis, and is supplied by the superior and inferior epigastric vessels. Zone II consists of the lower anterior abdominal wall below zone I and is predominantly supplied by the superficial epigastric, superficial external pudendal, and superficial circumflex iliac arteries. Zone III is lateral to zone I and is supplied by the musculophrenic, lower intercostal, subcostal and lumbar arteries. The distance of the vertically running superior and deep inferior epigastric vessels from the midline is relevant to siting surgical incisions (Table 61.1). Table 61.1 Distances of superior and deep inferior epigastric arteries from midline Level Left Right Xiphoid cartilage 4.5 ± 0.1 cm 4.4 ± 0.1 cm Between xiphoid and umbilicus 5.4 ± 0.2 cm 5.5 ± 0.2 cm Umbilicus 5.6 ± 0.1 cm 5.9 ± 0.1 cm Between umbilicus and pubic symphysis 5.3 ± 0.1 cm 5.3 ± 0.1 cm Pubic symphysis 7.5 ± 0.1 cm 7.5 ± 0.1 cm Adapted from Saber AA, Meslemani AM, Davis R, Pimentel R 2004 Safety zones for anterior abdominal wall entry during laparoscopy: a CT scan mapping of epigastric vessels. Ann Surg 239:182–5.
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Skin and soft tissue 1071 16 retPAHC Fig. 61.2 The deep muscles and arterial supply of the anterolateral abdominal wall. The greater part of Internal thoracic artery and vein Serratus anterior the left rectus abdominis has been removed to show the superior and inferior epigastric vessels. Latissimus dorsi Superior epigastric artery and vein Intercostal artery Innermost intercostal Linea alba Musculophrenic artery Rectus abdominis (cut) External oblique (cut) Cut edge of aponeurosis Internal oblique (cut) of internal oblique Transversus abdominis Arcuate line Deep circumflex iliac artery Transversalis fascia Inferior epigastric artery and vein Inguinal ligament Superficial epigastric artery and vein External iliac artery and vein Rectus abdominis (cut) Deep circumflex iliac artery Inferior epigastric artery and vein Pyramidalis Superficial epigastric artery and vein Spermatic cord Femoral artery and vein The inferior epigastric arteries ascend and anastomose with their laparoscopic inguinal hernia repair or with pelvic fractures. Muscular superior counterpart without branching in about 30% of cases branches supply the abdominal muscles and peritoneum, and anasto- (El-Mrakby and Milner 2002). Branching into two vessels before anas- mose with the circumflex iliac and lumbar arteries. Cutaneous branches tomosis is the most common pattern, accounting for almost 60% of perforate the aponeurosis of external oblique, supply the skin and cases, with a trifurcation being present in the remainder. The inferior anastomose with branches of the superficial epigastric artery. These epigastric arteries have an average diameter of approximately 3 mm musculocutaneous perforators have been mapped in detail because they at their origin, compared to an average diameter of 1.6 mm at the are particularly important to plastic surgeons undertaking reconstruc- origin of the superior epigastric arteries, presumably explaining why the tive surgery with (myo)cutaneous flaps (Rozen et al 2008). inferior epigastric arteries provide the ‘dominant’ supply to rectus Occasionally, the inferior epigastric artery arises from the femoral abdominis. Preliminary ligation of the inferior epigastric artery is often artery. It then ascends anterior to the femoral vein to follow its usual performed when preparing a myocutaneous flap using the mid or lower abdominal course. Rarely, it arises from the external iliac artery in rectus abdominis based on the superior epigastric artery; this encour- common with an aberrant obturator artery or from the obturator artery. ages the augmentation of the superior epigastric arterial supply. The superior and inferior epigastric arteries are important sources of Branches of the inferior epigastric artery anastomose with branches collateral blood flow between the internal thoracic artery and the exter- of the superior epigastric artery within the rectus sheath posterior to nal iliac artery when aortic blood flow is compromised. Small tributar- rectus abdominis at a variable level above the umbilicus (Rozen et al ies of the inferior epigastric vein draining the skin around the umbilicus 2008). Other branches anastomose with terminal branches of the lower anastomose with terminal branches of the umbilical vein draining the five posterior intercostal, subcostal and lumbar arteries at the lateral umbilical region via the falciform ligament. These portosystemic anas- border of the rectus sheath. Inferolaterally, branches anastomose with tomoses may open widely in cases of portal hypertension, when portal the deep circumflex iliac artery. The inferior epigastric artery ascends venous blood may drain into the systemic circulation via the inferior along the medial margin of the deep inguinal ring. The vas deferens in epigastric veins. The pattern of dilated superficial veins radiating from the male, or the round ligament in the female, passes medially after the umbilicus is referred to as the ‘caput medusae’. hooking around the artery at the deep inguinal ring. The artery forms the lateral border of Hesselbach’s inguinal triangle, an important land- Posterior intercostal, subcostal mark in laparoscopic inguinal hernia repair; the inferior border of the and lumbar arteries triangle is formed by the inguinal ligament, and the medial border is formed by the lateral margin of rectus abdominis. The inferior epigastric artery also gives off the cremasteric artery, a The tenth and eleventh posterior intercostal arteries, the subcostal pubic branch, and muscular and cutaneous branches. The cremasteric artery, and the lumbar arteries pierce the posterior aponeurosis of trans- artery accompanies the spermatic cord in males, supplies cremaster and versus abdominis to enter the neurovascular plane of the abdominal the other coverings of the cord and anastomoses with the testicular wall deep to internal oblique (Fig. 61.4). The location of these arteries artery. In females, the artery is small and accompanies the round liga- and their accompanying segmental nerves is of clinical importance ment. A pubic branch, near the femoral ring, descends posterior to the when creating myofascial flaps during abdominal wall reconstruction. pubis and anastomoses with the pubic branch of the obturator artery. The arteries on either side run forwards, giving off muscular branches The pubic branch of the inferior epigastric artery may be larger than the to the overlying internal and external oblique, before anastomosing obturator artery and supply most of the obturator artery territory in the with the lateral branches of the superior and inferior epigastric arteries thigh, in which case it is referred to as the aberrant obturator artery (Pai at the lateral border of the rectus sheath (see Fig. 61.4). Perforating et al 2009). It lies close to the medial border of the femoral ring and cutaneous vessels run vertically through the muscles to supply the may be damaged in medial dissection of the ring during femoral or overlying skin and subcutaneous tissue. A small contribution to the
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Anterior AbdominAl wAll 1072 8 noitCeS A lower abdominal wall run with the deep circumflex iliac and inferior epigastric arteries to external iliac nodes. Inguinal ligament Testicular vessels Rectus SEGMENTAL NERVES abdominis The ventral rami of the sixth to eleventh intercostal nerves, the subcostal nerve (twelfth thoracic) and first lumbar nerve (iliohypogastric and Deep ilioinguinal nerves) supply the muscles and skin of the anterior abdom- inguinal ring inal wall (Rozen et al 2008). The seventh to the twelfth thoracic ventral rami continue anteriorly from the intercostal and subcostal spaces into Iliopsoas the abdominal wall (Fig. 61.5). Approaching the costal margin, the Femoral seventh to tenth nerves curve medially across the deep surface of nerve the costal cartilages between the digitations of the diaphragm and Inferior transversus abdominis. The subcostal nerve gives a branch to the first External epigastric iliac lumbar ventral ramus (dorsolumbar nerve) that contributes to the vessels vessels lumbar plexus (Ch. 62). It accompanies the subcostal vessels along the Femoral ring inferior border of the twelfth rib, passing behind the lateral arcuate liga- ment and kidney, and anterior to the upper part of the quadratus lumborum. Vas All these segmental nerves run anteriorly within a thin layer of fascia deferens Obturator in the neurovascular plane between transversus abdominis and internal nerve and oblique, where they branch and interconnect with adjacent nerves artery (Rozen et al 2008). Muscular branches innervate transversus abdominis and internal and external oblique. Cutaneous branches supply the skin of the lateral and anterior abdominal walls. The thoracic nerves enter the rectus sheath at its lateral margin and pass posterior to rectus abdominis, where they again intercommunicate. Each nerve then II pierces rectus abdominis from its posterior aspect and gives off muscu- H lar branches to this muscle (and a branch to pyramidalis from the subcostal nerve), and cutaneous branches that pierce the anterior rectus sheath to supply overlying skin. The ninth intercostal nerve supplies skin above the umbilicus, the tenth supplies skin that consistently includes the umbilicus, and the eleventh supplies skin below the umbilicus (see Fig. 16.10; Fig. 61.5). The subcostal nerve supplies the anterior gluteal skin just below the iliac crest, and the skin of the lower abdomen and inguinal region (overlapping with the L1 dermatome in this region) (Lee et al 2008). A typical dermatome map of the anterior abdominal wall is shown in TT DD Figure 16.10. The ventral rami of the lower intercostal and subcostal EE nerves also provide sensory fibres to the costal parts of the diaphragm and parietal peritoneum. The transversus abdominis plane (TAP) block is a regional anaes- B thetic technique for abdominal surgery. Using ultrasound imaging guid- ance, local anaesthetic is injected into the neurovascular plane between Fig. 61.3 A, The deep aspect of the lower part of the anterior abdominal internal oblique and transversus abdominis, targeting the segmental wall of the left side. The femoral and deep inguinal rings are displayed, nerves of the anterolateral abdominal wall. together with the vessels and other structures in relation to them and also the opening into the obturator canal. B, A laparoscopic view showing the Lesions of the intercostal nerves parietal peritoneum covering the area. Abbreviations: D, vas (ductus) deferens; E, external iliac vessels; H, orifice of direct inguinal hernia; I, inferior epigastric vessels; T, testicular vessels. (B, With permission from The anterolateral abdominal wall muscles are innervated by several Drake RL, Vogl AW, Mitchell A (eds), Gray’s Anatomy for Students, 2nd segmental nerves and injury to a single nerve does not produce a clini- ed, Elsevier, Churchill Livingstone. Copyright 2010.) cally detectable loss of muscle tone. The overlap between sequential dermatomes means that significant cutaneous anaesthesia is appreci- ated only after sectioning at least two sequential nerves. supply of the lower abdominal muscles comes from branches of the MUSCLES deep circumflex iliac arteries. The anterior abdominal wall is also supplied by branches of the ANTEROLATERAL MUSCLES OF THE ABDOMEN femoral artery: namely, the superficial epigastric, superficial circumflex iliac, and superficial external pudendal arteries, and by the deep circum- Rectus abdominis, pyramidalis, external oblique, internal oblique and flex iliac artery arising from external iliac artery (see Fig. 78.7A). transversus abdominis constitute the anterolateral muscles of the abdomen. They act together to perform a range of functions, some of Lymphatic drainage which involve the generation of a positive pressure within one or more body cavity. Although many of these activities may occur with no Superficial lymphatic vessels accompany the subcutaneous blood ‘forced assistance’, expiration, defecation and micturition may be aided vessels immediately below the dermis (Tourani et al 2013). Vessels from by the generation of a positive intra-abdominal pressure. Parturition, the lumbar and gluteal regions run with the superficial circumflex iliac coughing and vomiting always require such a positive pressure. Under vessels, and those from the infra-umbilical skin run with the superficial resting conditions, the tone developed within the muscles provides epigastric vessels. Both drain into superficial inguinal nodes. The supra- support for the abdominal viscera and retains the normal contour of umbilical region is drained by vessels draining to axillary and paraster- the abdomen. The consequences of diminished muscular support can nal nodes. be seen in patients who have massive ventral hernias or conditions like The deep lymphatic vessels accompany the deeper arteries. Laterally, ‘prune belly syndrome’, where there is congenital deficiency or absence they run either with the lumbar arteries to drain into the lateral aortic of these muscles. nodes, or with the intercostal and subcostal arteries to posterior media- Active contraction of the muscles provides an important role in the stinal nodes. Lymphatics in the upper anterior abdominal wall run with maintenance of abdominal wall tone. The compression of the abdomi- the superior epigastric vessels to parasternal nodes while those in the nal cavity required to increase intra-abdominal pressure is brought
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1073 16 retPAHC muscles Muscular terminal branch RA Cutaneous artery Intercostal artery Inferior epigastric artery PPF IOA SCF PP TF EOA Perforating cutaneous artery Subcostal artery TF IO SCF PPF TA EO Lumbar artery RPF EO SCF TLF LD EO External oblique PP Parietal peritoneum SCF Subcutaneous fat EOA External oblique aponeurosis PPF Preperitoneal fat TA Transversus abdominis IO Internal oblique RA Rectus abdominis TF Transversalis fascia IOA Internal oblique aponeurosis RPF Retroperitoneal fat TLF Thoracolumbar fascia LD Latissimus dorsi Fig. 61.4 The arrangement of the anterolateral abdominal wall vessels at the level of the mid-abdomen. about mainly by contraction of the diaphragm. The bony pelvis, spine muscle, fusing with the fibres of the anterior lamina of the rectus sheath. and lower thoracic cage provide rigidity to part of the abdominal wall. Occasionally, one or two incomplete intersections are present below the During the generation of positive intra-abdominal pressure, the abdom- umbilicus. The intersections may represent the myosepta delineating inal muscles act to hold the abdominal wall in a relatively fixed posi- the myotomes that form the muscle. tion, rather than to generate pressure directly; because the majority of The medial border of each rectus abdominis abuts the linea alba. Its the abdominal wall is muscular, the anterolateral abdominal wall lateral border may be visible on the surface of the anterior abdominal muscles must be synchronously contracted to prevent displacement of wall as a gently curved groove, the linea semilunaris, which extends the viscera and the resultant loss of pressure. The oblique muscles, from the tip of the ninth costal cartilage to the pubic tubercle. In a acting through their anterior aponeuroses and the rectus sheath, provide muscular individual it is readily visible, even when the muscle is not the majority of this tension, although transversus abdominis and rectus actively contracting, but in many normal and obese individuals it may abdominis contribute. be completely obscured. The anterolateral abdominal muscles contribute little to the move- ments of the trunk during normal sitting and standing; these move- Attachments Rectus abdominis arises by two tendons. The larger, ments are controlled predominantly by the paravertebral and spinal lateral tendon is attached to the pubic crest and may extend beyond the muscles. However, movements of the trunk against resistance or when pubic tubercle to the pectineal line. The medial tendon interlaces with the individual is supine require the anterolateral abdominal muscles. the contralateral muscle and blends with ligamentous fibres covering Rectus abdominis is the most important in these situations, producing the front of the pubic symphysis. Additional fibres may arise from the anterior flexion of the trunk. If the pelvic girdle is fixed, flexion of the lower part of the linea alba. The pubic attachment of the tendon of thoracic girdle occurs. With a fixed thoracic cage, contraction of rectus rectus abdominis and its anterior sheath run over the anterior surface abdominis causes the pelvis to tilt and lift. Lateral flexion and rotation of the pubic symphysis and become continuous with the attachments of the trunk against resistance is provided by unilateral contraction of of gracilis and adductor longus (Norton-Old et al 2013). Superiorly, the oblique muscles. rectus abdominis is attached by three slips of muscle to the fifth, sixth and seventh costal cartilages. The most lateral fibres are usually attached Rectus abdominis to the anterior end of the fifth rib; occasionally, this slip is absent or it Rectus abdominis is a paired, long, strap-like muscle that extends along extends to the fourth and third ribs. The most medial fibres are occa- the entire length of the anterior abdominal wall on either side of the sionally connected to the costoxiphoid ligaments and the side of the linea alba (Fig. 61.6). It is widest in the upper abdomen. The muscle xiphoid process. fibres of rectus abdominis are partially interrupted by three fibrous bands or tendinous intersections, which pass transversely or obliquely Vascular supply Rectus abdominis is supplied principally by the across the muscle. One is usually situated at the level of the umbilicus, superior and inferior epigastric arteries, the latter being the dominant another opposite the free end of the xiphoid process and a third about supply. Small terminal branches from the lower three posterior inter- midway between the other two. They are rarely full-thickness and costal arteries, the subcostal artery, the lumbar arteries and the deep usually extend only half-way through the anterior thickness of the circumflex iliac artery may contribute, particularly at the lateral edges
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Anterior AbdominAl wAll 1074 8 noitCeS Fig. 61.5 The cutaneous branches of the lower intercostal and lumbar Serratus anterior nerves. Portions of the muscles of the anterior abdominal wall have been removed, including most of the Latissimus dorsi anterior layer of the rectus sheath and parts of rectus abdominis. Sixth intercostal nerve Lateral cutaneous branches of intercostal nerve Innermost intercostal Lateral cutaneous branches Tenth intercostal nerve Rectus abdominis (cut) External oblique (cut) Transversus abdominis Eleventh intercostal nerve Anterior cutaneous branch Subcostal nerve Arcuate line Iliohypogastric nerve Ilioinguinal nerve Transversalis fascia Rectus abdominis (cut) Internal oblique (cut) Anterior lamina of Inguinal ligament rectus sheath Spermatic cord and the lower parts of the muscle, where they anastomose with small from all three anterior leaves run obliquely upwards, whereas the pos- lateral branches of the epigastric arteries. Rectus abdominis provides a terior leaves run obliquely downwards at right angles to the anterior reliable and versatile myocutaneous flap, either pedicled or free, because leaves. Above the arcuate line, the anterior rectus sheath is composed of the excellent vascularity provided by the epigastric vessels and of both leaves of the aponeurosis of external oblique and the anterior because the muscle belly can be separated relatively easily from its leaf of the aponeurosis of internal oblique fused together. The poste- surrounding sheath. The upper half of the muscle may be used for rior rectus sheath is composed of the posterior leaf of the aponeurosis breast reconstruction, and the lower half may be transposed to the of internal oblique and both leaves of the aponeurosis of transversus groin and upper thigh or rotated on its lower attachments and delivered abdominis. Thus, both the anterior and posterior layers of the rectus into the perineum for reconstruction after radical pelvic and perineal sheath consist of three layers of fibres with the middle layer running resections. at right angles to the other two. At the midline, the anterior and pos- terior layers are closely approximated. Fibres from each layer decussate Innervation Rectus abdominis is innervated segmentally by the ter- to the opposite side of the sheath, forming a continuous aponeurosis minal branches of the ventral rami of the lower six or seven thoracic with the contralateral muscles. Fibres also decussate anteroposteriorly, spinal nerves. It may also receive a branch from the ilioinguinal nerve crossing from the anterior sheath to the posterior sheath. The dense (Rozen et al 2008). fibrous line caused by this decussation is called the linea alba. The external oblique, internal oblique and transversus abdominis muscles Actions The recti contribute to flexion of the trunk and the mainte- can therefore be regarded as digastric muscles with a central tendon nance of abdominal wall tone required during straining. comprising the linea alba (Rizk 1980). The decussating fibres at the linea alba can be used to identify the midline during surgical incisions. rectus sheath Below the arcuate line, all three aponeuroses from the oblique and Rectus abdominis on each side is enclosed by a fibrous sheath (Figs transversus abdominis muscles pass into the anterior rectus sheath (see 61.7–61.10). The anterior portion of this sheath extends the entire Fig. 61.7). length of the muscle and fuses with periosteum and ligaments at sites of the muscle’s attachments. The posterior part of the sheath is complete linea alba and umbilicus behind the upper two-thirds of the muscle but absent below this level, The linea alba is a tendinous raphe extending from the xiphoid process which corresponds to approximately one-third of the distance between to the pubic symphysis and pubic crest. It lies between the two recti and the umbilicus and the pubis (Loukas et al 2008). The termination of is formed by the interlacing and decussating aponeurotic fibres of exter- the posterior rectus sheath is usually gradual but may be abrupt and nal oblique, internal oblique and transversus abdominis. At its lower marked by a clearly visible curved horizontal line known as the arcuate end, the linea alba has two attachments to the pubis: superficial fibres line (of Douglas). Below this level, rectus abdominis lies on the trans- are attached to the pubic symphysis, and deeper fibres form a triangular versalis fascia and extraperitoneal connective tissue. lamella that is attached behind rectus abdominis to the posterior The rectus sheath is formed from the aponeuroses of all three surface of both pubic crests (adminiculum lineae albae). The fundiform lateral abdominal muscles: namely, external oblique, internal oblique ligament of the penis and pyramidalis are attached to the suprapubic and transversus abdominis. Each aponeurosis is bilaminar; the fibres part of the linea alba. The linea alba is visible externally in those who
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1075 16 retPAHC muscles Fig. 61.6 Muscles of the left side of the trunk. External oblique has been Pectoralis major (cut) removed to show internal oblique, but its digitations from the ribs have been preserved. The sheath of rectus abdominis has been opened and its anterior layer removed. Latissimus dorsi Linea alba Digitations of external oblique Internal intercostal muscle of tenth intercostal space Tendinous intersections Internal oblique Aponeurosis of internal oblique Rectus abdominis Cut edge of aponeurosis of external oblique Anterior superior iliac spine Gluteus medius Inguinal ligament Gluteus maximus Pyramidalis Spermatic cord Tensor fasciae latae Sartorius Rectus femoris A Rectus abdominis Linea alba External oblique Fig. 61.7 Transverse sections through the anterior abdominal wall. A, Immediately above the umbilicus. B, Below the arcuate line. The bilaminar nature of each muscular aponeurosis is difficult to illustrate in cross-section. Peritoneum Transversalis fascia Internal oblique The fibres appear to fuse into a single sheet during Preperitoneal fat Transversus abdominis formation of the rectus B Rectus abdominis Linea alba External oblique sheath. Note that rectus is supported directly by the transversalis fascia below the arcuate line. Peritoneum Transversalis fascia Internal oblique Preperitoneal fat Transversus abdominis are lean and muscular, as a shallow midline groove in the anterior consists of skin, a fibrous layer (representing the area of fusion between abdominal wall. Its width varies along its length: it is wider above the the round ligament of the liver, the median umbilical ligament, and umbilicus than below, and widest at the level of the umbilicus (Rath two medial umbilical ligaments), the transversalis fascia, the umbilical et al 1996). It is wider and thinner in women, in adults aged over fascia surrounding the urachal remnant, and peritoneum (Fathi et al 50 years, and in the obese and multiparous (Naraynsingh et al 2012). 2012). Its appearance and position are variable (Fathi et al 2012). In Its tensile strength is proportional to its thickness and density (Kore- adults, it tends to lie at a relatively lower position with advancing age, nkov et al 2001). The linea alba is relatively bloodless but it is crossed in men, and in individuals with a higher body mass index. superficially from side to side by a few small blood vessels. In the fetus, the umbilicus transmits the umbilical vessels, urachus The umbilicus is a fibrous cicatrix that lies a little below the mid- and, up to the third month of gestation, the vitelline or yolk stalk. It point of the linea alba, and is covered by an adherent area of skin. It closes a few days after birth, but the vestiges of the vessels and urachus
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Anterior AbdominAl wAll 1076 8 noitCeS A A B Fused aponeuroses B Aponeurosis of external and of external oblique internal oblique Linea alba Linea alba Aponeurosis of External oblique transversus Rectus abdominis Internal oblique Rectus abdominis abdominis Internal oblique Transversus Fused aponeuroses of internal oblique and abdominis Transversalis Transversus transversus abdominis fascia abdominis Left renal vein Aorta Fig. 61.8 The rectus sheath. Computed tomography scan (A) and Fig. 61.9 The rectus sheath. Computed tomography scan (A) and diagram (B) of the anterior abdominal wall, demonstrating the formation of diagram (B) of the anterior abdominal wall, demonstrating the formation of the rectus sheath above the umbilicus. The anterior rectus sheath is the rectus sheath below the umbilicus. The posterior rectus sheath is composed of both leaves of the aponeurosis of external oblique and the replaced by the transversalis fascia and extraperitoneal connective tissue. anterior leaf of the aponeurosis of internal oblique, fused together. The posterior rectus sheath is composed of the posterior leaf of the aponeurosis of internal oblique and both leaves of the aponeurosis of transversus abdominis. Posterior rectus sheath Fig. 61.10 The concept of bilaminar aponeuroses of the oblique and transversus abdominis muscles. Note that Laminae of Posterior lamina of the fibres of the superficial and deep laminae are transversus abdominis internal oblique approximately at right angles; decussations occur as part Posterior Anterior of the linea alba. Transversus abdominis Internal oblique Rectus abdominis External oblique Anterior lamina of Posterior Anterior internal oblique Laminae of external oblique Anterior rectus sheath
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