Mazyar Kanani, MRCS, Antoon F. M. Moorman, PhD, Andrew C

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Development of the Atrioventricular Valves: Clinicomorphological Correlations Mazyar Kanani, MRCS, Antoon F.M. Moorman, PhD, Andrew C. Cook, PhD, Sandra Webb, PhD, Nigel A. Brown, PhD, Wouter H. Lamers, MD, PhD, Robert H. Anderson, MD, FRCPath The Annals of Thoracic Surgery Volume 79, Issue 5, Pages 1797-1804 (May 2005) DOI: 10.1016/j.athoracsur.2004.06.122 Copyright © 2005 The Society of Thoracic Surgeons Terms and Conditions

Fig 1 This section comes from a human embryo at Carnegie stage 14, just subsequent to looping and ”ballooning“ to form the apical ventricular components. The atrioventricular canal (curly bracket) is aligned predominantly with the developing left ventricle (large white arrow), albeit that there is already a direct communication from the right atrium to the developing right ventricle (small white arrow). The atrioventricular canal musculature will be sequestrated on the atrial side of the atrioventricular junctions, which form at the site of the small black arrows. Note that the right atrioventricular junction (double black arrows) is also the inner heart curvature, and forms the roof of the primary ventricular foramen. The crest of the muscular ventricular septum is noted (black star). (LV = left ventricle.) The Annals of Thoracic Surgery 2005 79, 1797-1804DOI: (10.1016/j.athoracsur.2004.06.122) Copyright © 2005 The Society of Thoracic Surgeons Terms and Conditions

Fig 2 This illustration, modified from the reconstruction of a human heart at Carnegie stage 14, illustrates the location of the ring of musculature of the primary heart tube delineated by reaction to an antibody to the nodose ganglion of the chick [10]. This is the myocardium of the so-called “primary ring.” (AV = atrioventricular; GIN2 = antigen to chick nodose ganglion.) The Annals of Thoracic Surgery 2005 79, 1797-1804DOI: (10.1016/j.athoracsur.2004.06.122) Copyright © 2005 The Society of Thoracic Surgeons Terms and Conditions

Fig 3 The first step in remoulding of the primary ring occurs concomitant with appearance of the primary ventricular septum. As the apical parts of the ventricle balloon form the primary tube, the inferior part of the primary foramen deepens to form the right ventricular inlet component between the right atrium and the dorsal part of the developing right ventricle. At the same time, the cushions within the atrioventricular canal become draped across the inferior part of the forming ventricular septum. (GIN2 = antigen to chick nodose ganglion.) The Annals of Thoracic Surgery 2005 79, 1797-1804DOI: (10.1016/j.athoracsur.2004.06.122) Copyright © 2005 The Society of Thoracic Surgeons Terms and Conditions

Fig 4 This scanning electron micrograph demonstrates the arrangement of the atrioventricular cushions at 7 weeks of development. The short-axis view of the heart from beneath depicts that the larger parts of the cushions, still unfused, are located within the left ventricle. Note also the beginning of delamination of the leaflets of the tricuspid valve from the parietal ventricular wall (dotted white line). At this stage the primary orifice of the developing tricuspid valve (double-headed arrow) is parallel to the developing ventricular septum. The Annals of Thoracic Surgery 2005 79, 1797-1804DOI: (10.1016/j.athoracsur.2004.06.122) Copyright © 2005 The Society of Thoracic Surgeons Terms and Conditions

Fig 5 These illustrations, both taken from the apex of the left ventricle looking toward the ventricular outflow tract, contrast the morphologic arrangement of the zone of apposition (black arrow outlined in white) between the bridging leaflets in a heart with atrioventricular septal defect and common atrioventricular junction (upper panel) and the so-called “isolated cleft” (lower panel, black arrow outlined in white) in the otherwise normal mitral valve. Tendinous cords attach the edges of the “cleft” to the crest of the ventricular septum (small black arrows). The arrangement in the upper panel is comparable with the situation seen in the developing heart at 7 weeks, before formation of the discrete left atrioventricular junction. The Annals of Thoracic Surgery 2005 79, 1797-1804DOI: (10.1016/j.athoracsur.2004.06.122) Copyright © 2005 The Society of Thoracic Surgeons Terms and Conditions

Fig 6 This section of the cardiac short axis, from a normal heart, illustrates the orientation of the definitive orifices of the mitral and tricuspid valves. Note that the septal leaflet of the tricuspid valve “hugs” the septum, while the subaortic outflow tract interposes between the septum and the aortic leaflet of the mitral valve. (TV = tricuspid valve.) The Annals of Thoracic Surgery 2005 79, 1797-1804DOI: (10.1016/j.athoracsur.2004.06.122) Copyright © 2005 The Society of Thoracic Surgeons Terms and Conditions

Fig 7 (A) A longitudinal section of the developing left ventricle after the aorta has been walled into the ventricle. Note that the musculature of the inner heart curvature continues to separate the developing leaflets of the aortic and mitral valves (bracket). This muscular fold will not disappear until after the completion of septation. The contributions from both superior and inferior atrioventricular cushions to the developing aortic leaflet of the mitral valve are clearly seen, albeit that the tips have yet to fuse (star). (B) A scanning electron micrograph illustrating the comparable arrangement, and also revealing how the papillary muscles are formed by compaction of the trabecular layer of myocardium. The unfused tip of the endocardial cushions is noted (star). (LSCV = left superior caval vein.) The Annals of Thoracic Surgery 2005 79, 1797-1804DOI: (10.1016/j.athoracsur.2004.06.122) Copyright © 2005 The Society of Thoracic Surgeons Terms and Conditions

Fig 8 These diagrams, redrawn from the study of Kim and colleagues [9], indicate the change in shape and orientation of the atrioventricular cushions in the developing human heart that occurs concomitant with expansion and separation of the initially common atrioventricular junction. Initially the orifice (left) of the developing mitral valve has a trifoliate configuration (white y), which becomes bifoliate (right) subsequent to expansion of the left atrioventricular junction. The star marks the expansion of the right atrioventricular junction (dotted black line) that occurs in combination with formation of the tricuspid gully. The Annals of Thoracic Surgery 2005 79, 1797-1804DOI: (10.1016/j.athoracsur.2004.06.122) Copyright © 2005 The Society of Thoracic Surgeons Terms and Conditions

Fig 9 This section, from a 6-week-old human heart, illustrates how the right ventricular inlet component (dotted line) is lined on the one side by the lateral cushion, which gives rise to the inferior leaflet of the valve, and on the other side by the septal leaflet, which is delaminating from the surface of the ventricular septum. Note the compaction of the papillary muscles of the mitral valve in the left ventricle (stars). The Annals of Thoracic Surgery 2005 79, 1797-1804DOI: (10.1016/j.athoracsur.2004.06.122) Copyright © 2005 The Society of Thoracic Surgeons Terms and Conditions

Fig 10 These scanning electron micrographs depict the developing tricuspid valve at 7 weeks (left) and 8 weeks (right). Both are dissected by removing the anterior wall of the developing right ventricle. Note that the orifice of the valve initially points towards the subpulmonary infundibulum (left). Only subsequent to liberation of the anterosuperior and inferior leaflets does the valvar orifice open directly into the apical part of the right ventricle. (RV = right ventricle; Ant-sup = anterosuperior.) The Annals of Thoracic Surgery 2005 79, 1797-1804DOI: (10.1016/j.athoracsur.2004.06.122) Copyright © 2005 The Society of Thoracic Surgeons Terms and Conditions

Fig 11 A heart with the Ebstein malformation of the tricuspid valve, from the atrial and ventricular aspects. There is failure of delamination of the inferior and septal leaflets from the walls of the right ventricular inlet component. The black arrows represent the so-called keyhole orifice arising from the conjoint nature of the inferior and septal leaflets. (Left) Atrial aspect. (Right) Ventricular aspect. The Annals of Thoracic Surgery 2005 79, 1797-1804DOI: (10.1016/j.athoracsur.2004.06.122) Copyright © 2005 The Society of Thoracic Surgeons Terms and Conditions