Sequential segmental analysis of the crocodilian heart

Abstract

Differences between hearts of crocodilians and those of mammals and birds are only partly understood because there is no standardised approach and terminology for describing cardiac structure. Whereas most reptiles have an undivided ventricle, crocodilians have a fully septated ventricle. Their hearts, therefore, are more readily comparable with the hearts of mammals and birds. Here, we describe the heart of a crocodile (Crocodylus noliticus). We use the versatile sequential segmental approach to analysis, juxtaposing several key views of the crocodilian heart to the comparable views of human hearts. In crocodiles, the atrial and ventricular septums are complete but, unlike in placental mammals, the atrial septum is without an oval fossa. The myocardial component of the crocodilian ventricular septum dominates, but the membranous septum likely makes up a greater proportion than in any mammal. In the crocodile, the aortic trunk takes its origin from the left ventricle and is not wedged between the atrioventricular junctions. Consequently, there is a common atrioventricular junction, albeit with separate right and left atrioventricular valvar orifices. As in mammals, nonetheless, the crocodilian left atrioventricular valvar orifice is cranial to the right atrioventricular valvar orifice. By applying a method of analysis and terminology usually restricted to the human heart, we build from the considerable existing literature to show neglected and overlooked shared features, such as the offset between the left and right atrioventricular valvar orifices. Such commonalities are surprising given the substantial evolutionary divergence of the archosaur and synapsid lineages, and likely reflect evolutionarily shared morphogenetic programmes.

Keywords: arterial trunks; atrioventricular junction; crocodile; foramen of Panizza; heart development.

Figure 1

External view of a 2‐year‐old crocodile heart showing the relative position of the chambers as they would be seen during life. There is a common arterial trunk arising from the ventricular mass, which is divided internally into two aortic and one pulmonary channel. The proximal extent of the muscular sub‐pulmonary infundibulum, which forms part of the pulmonary outflow tract, is marked by a deep recess carrying within it coronary arteries, (blue arrow). LA, left atrium, LV, left ventricle, RA, right atrium, RV, right ventricle.

Figure 2

View of the dorso‐caudal aspect of the atriums, showing the relationship between the venous channels and the pulmonary veins. The left superior caval vein runs along the left atrial wall between the left atrial appendage and the two pulmonary veins. It is some distance from the left atrioventricular groove, and the coronary veins within it. The three caval veins join together into the venous sinus and enter the right atrium via the venous valves. ICV, inferior caval vein, SCV, superior caval vein.

Figure 3

Opened morphologically, the right atrium and right atrioventricular valve of the crocodile (a) and human (b) heart. (a) The right atrium of the adult crocodile contains similar components as the human heart, specifically an extensive, trabeculated appendage, an atrial septum (AS), a smooth‐walled vestibule (blue asterisks), and a venous sinus, the entrance to which is marked by two prominent venous valves. The right atrioventricular valve consists of a large fibrous septal (S) and smaller muscular mural leaflet (M) and is supported by two papillary muscle groups (red triangles). In the crocodilian heart, coronary veins become confluent with the caval veins in the venous sinus dorsal to the venous valves, whereas in the human heart the coronary sinus opens into the venous component of the right atrium. The crocodilian heart, furthermore, is without an oval fossa.

Figure 4

Opened morphologically, the right ventricle and its outflow of the crocodile (a) and human (b) heart. (a) The outflow from the morphologically right ventricle of crocodiles leads both to the right ventricular aorta and to the pulmonary trunk. The right ventricular aorta is walled from the morphologically left ventricle by the interventricular component of the membranous septum. The two right ventricular outflows are separated by a small muscular outlet septum (blue asterisk). Below the base of the pulmonary valve is the ‘cog‐tooth’ valve. Also shown are the coarse apical trabeculations, the septomarginal trabeculation (SMT), the septal (S) and mural (M) leaflets of the right atrioventricular valve, and the supporting papillary muscles (red triangles). The human right ventricle has more defined papillary muscles, with the margins of the leaflets being anchored to these by more numerous tendinous cords than in the crocodilian heart. The valve in the human heart also displays three leaflets, all of which are fibrous. AS, anterior‐superior leaflet of the tricuspid valve; RV, right ventricular.

Figure 5

Corresponding view of the left atrium and left atrioventricular valve of the crocodile (a) and human (b) heart, opened morphologically. Again, the crocodilian left atrium can be divided into components that are similar to the human heart. There is a septal component, a pulmonary venous component, a smooth‐walled vestibule (blue asterisks), and an appendage, which is much more extensive in the crocodile than in human. In the left atrium of both species, there is also an extensive smooth‐walled body. The crocodilian atrial septum is without a secondary foramen. The left atrioventricular valve in both species again possesses two leaflets, with both being fibrous. The aortic leaflet (a) in the crocodilian heart occupies a greater proportion of the left atrioventricular junction than does the mural leaflet (M), but these proportions are reversed in the human heart. The left ventricle of the crocodilian heart, which is extensively trabeculated morphologically, can also be seen in the image, together with a prominent muscle which extends across the mid part of the cavity (yellow arrow).

Figure 6

Views from the left atrium in a fetal crocodile specimen showing that the structure of the flap valve is similar to that reported in the chick. (a) The flap valve is distended to show its pocket‐like shape. The cranial margin (green arrow) is intact and is attached towards the left atrial appendage (deviated leftwards). The asterisk marks the site of a prominent muscular strand for orientation purposes. (b) The caudal margin of the flap valve has been distended to show multiple small fenestrations present within the body of the flap valve below the level of the muscular strand (*). LAA, left atrial appendage.

Figure 7

Short axis section across the ventricular base of the crocodile (a) and human (b) heart. (a) Arterial roots at the level of the sub‐pulmonary infundibulum and two aortic valves, and below the level of the pulmonary valve. The cog‐teeth can be seen partially closing the sub‐pulmonary outflow tract. They are supported by a myocardial sleeve, which is in continuity with the walls of the two aortas. The relationship between the five cardiac valves can also be seen, with the left ventricular aortic valve sitting on top of the two atrioventricular valves (LAVV and RAVV) and below the two arterial valves leaving the morphologically right ventricle. The green asterisk marks the site of the foramen of Panizza. The aortic roots of the crocodilian heart are positioned less leftwards than in the human heart, and there is no wedging of the left ventricular aorta between the atrioventricular junctions. In consequence, the atrioventricular valvar orifices are less separated in the crocodilian heart, being supported by a common atrioventricular junction. LAVV, left atrioventricular valve; LV, left ventricular; MV, mitral valve; RAVV, right atrioventricular valve; RV, right ventricular; TV, tricuspid valve.

Figure 8

Four‐chamber sections of crocodile (a–b) and human heart (c–d) in attitudinally correct positions. The heart of a 2‐year‐old crocodile showing the inferior aspect (a) and the superior half (b). The section cuts across the inferior aspect of the fibrous leaflet of the right atrioventricular valve. In the inferior part of the heart (a), the two septally positioned leaflets of the atrioventricular valves are seen to insert at similar levels (circled). There is no evidence of an atrioventricular septal ‘sandwich’ as seen in the human heart. The fold of tissue between the right pulmonary vein and the right atrium is also evident (red arrow), as are the right (R) and left (L) venous valves. In the superior half of the heart (B), there is a greater degree of offsetting of the atrioventricular valves. This is due to the right atrioventricular valve hinging from the mid‐point of the extensive membranous septum (green arrow). LA, left atrium; LV, left ventricle; PV, pulmonary veins; RA, right atrium; RV, right ventricle; SS, spurious septum; TC, terminal crest.

Figure 9

Trans‐illumination of the membranous septum of the crocodile (a–b) and human heart (c–d). (a–b) In this heart from an adult crocodile, the septum has been trans‐illuminated to the show the extensive nature of the membranous septum as seen from the morphologically right (a) and left ventricle (b). The atrioventricular component, above the hinge line of the septal leaflet of the right atrioventricular valve, is outlined in red. On the morphologically right side of the human heart (c), the tendon of Todaro (T) and hinge point (h) of the tricuspid valve converge on the atrioventricular node (the position is approximated by the black circle). AV, atrioventricular; h, hinge point of the tricuspid valve; LA, left atrium; LV, left ventricle/left ventricular; R, right venous valve (crocodile) or Eustachian valve (human); RA, right atrium; RV, right ventricle; SMT, septomarginal trabeculation; T, tendon of Todaro.

Figure 10

The section reveals the detailed anatomy of the right ventricular outflows. A common party wall separates the right ventricular aorta from the pulmonary trunk. Within the heart, a small myocardial outlet septum (red asterisk) creates a degree of offsetting between the leaflets of the pulmonary and right ventricular aortic valves. The foramen of Panizza (yellow asterisk) can be seen just behind one of the leaflets of the right ventricular aorta. The foramen itself is surrounded by an arc of cartilage (C) which carries on its leading edge a crescent of smooth muscle. Also shown is the septal leaflet of the right atrioventricular valve (S). Pulm., pulmonary; RV, right ventricular.

Figure 11

Computerised tomographic images of the great vessels viewed from the left: (a) cross‐sectional slice, no contrast; (b) thin maximum intensity projection, post‐contrast, and (c) anatomic correlate. 1) Right ventricle, 2) left ventricle, 3) LV aorta, 4) pulmonary trunk, Asterisk=RV Aorta, white arrowhead, position of cog‐wheel apparatus, and red arrow, foramen of Panizza.

Figure 12

Volume‐rendered, post‐contrast computerised tomographical images of the great vessels and ventricles viewed from: (a) left, (b) ventrally, and (c) right. 1) right ventricle, 2) left ventricle, 3) LV aorta, 4) pulmonary trunk, *RV aorta, white arrowhead, position of cog‐wheel apparatus, and yellow arrow, foramen of Panizza.

Figure 13

Anatomic cross‐section (a) and comparable cross‐sectional image obtained with computerised tomography (b) through the ascending arterial trunks, showing that the three arterial pathways are encased in a common arterial wall. LV, left ventricular; Pulm., pulmonary; RV, right ventricular.

Figure 14

The pulmonary outflow tract has been opened in this specimen from a young crocodile to show the rudimentary nature of the cog‐teeth compared with the adult (see Fig. 10). The location of the myocardial outlet septum is marked by the red asterisk and the septal leaflet of the right atrioventricular valve is seen in the background (S). Pulm., pulmonary; RV, right ventricular.

Figure 15

These schematic diagrams show the location of the cartilaginous component of the crocodile heart as seen in our examinations, and compared with our interpretation of the initial description by White (1956) (inset). Our studies show that the cartilage consists of two components, one lateral and one medial. The medial component has prongs running in the base of the aortic sinuses facing the pulmonary trunk and is anchored to the crest of the ventricular septum via a caudal prong. It also encircles the foramen of Panizza cranially (yellow asterisk). This cranial crescent is lined by an arc of smooth muscle (blue arc). The lateral component occupies the base of the non‐facing sinuses, and runs into the fold of tissue between the right atrioventricular valve and the left ventricular aorta. The extensive membranous septum is shown in green. LAVV, left atrioventricular valve; RAVV, right atrioventricular valve.

Figure 16

These images show the left ventricular aorta as viewed from the right (a) and left (b) sides in an adult specimen. There is a single coronary arising from this aorta which gives rise to a right coronary artery (RCA), an infundibular branch (Inf CA), and also passes behind the arterial trunks as a left coronary artery branch (LCA) which then divides into circumflex (Cx) and ventral branches. The coronary arteries thus encircle the arterial pedicle, as can also be seen in Fig. 1. LV, left ventricular; RA, right atrium; RV, right ventricle.