Review
From Anatomy to Angioscopy: 164 Years of Crocodilian Cardiovascular Research, Recent Advances, and Speculations

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Abstract

This paper present a synthesis of current research on the crocodilian cardiovascular system with a view to encourage discussion and debate about the intricacies of this unique system and to provide ideas and suggestions for future studies. Innovative experimental approaches combined with new technologies have helped to resolve the complex flow and pressure patterns observed during non-shunting conditions that predominate in resting instrumented animals and during pulmonary to systemic shunting, which has been observed to occur spontaneously and during diving. The mechanisms and structures that may induce and regulate shunting are presented and the functional significance of a pulmonary to systemic shunt is discussed.

Introduction

Ever since the first description of the crocodilian cardiovascular system 164 years ago [32], the complexity and intricacies of this system have intrigued anatomists and physiologists. In the past 5 years, with the development of new technologies and experimental approaches, some significant advances have been made in our understanding of crocodilian haemodynamics. We feel that it is an appropriate time to review our current knowledge, to indicate the gaps in our knowledge, and to provide suggestions for future research. This review is a synthesis of the more recent papers and of current on-going investigations. Readers are directed to the reviews of Grigg 18, 19 which surveys earlier work on the crocodilian heart in a chronological manner, but more importantly poses questions and hypotheses about the functional significance of the crocodilian cardiovascular system. Several of these questions and hypotheses have since been examined, tested and elaborated upon.

In comparative physiology, it is, as the name suggests, of interest to compare the physiology between species or groups of animals in order to find similarities and differences, thus ultimately providing an insight into the evolution of physiological systems and processes [13]. An underlying tenet of this discipline is an understanding of the phylogenetic relationships between the animals we are comparing. Crocodilians are grouped with lizards, snakes, turtles, and the tuatara (Sphenodon) as reptiles and in doing so, comparisons between the crocodilians and “non-crocodilian” reptiles are common 8, 9, 37. However, by examining the phylogeny of these groups it becomes clear that it is impossible to define the Reptilia, except as amniotes that are not birds or mammals. The non-mammalian amniotes can be divided into two major groups, turtles and an entirety including crocodiles, birds, and lepidosaurs 5, 10. The Lepidosauria include the lizards, snakes, and Sphenodon, while the Archosauria include the birds, crocodilians, and the extinct dinosaurs. With this in mind we have to be careful when making comparisons since, from a strict phylogenetic point of view, crocodilians are more closely related to birds than to the lepidosaurs or turtles.

The extant crocodilians can be classified into three families (Alligatoridae, Crocodylidae, and Gavialidae) and encompass 22 species [for extensive information on the various species see URL a [44]]. These three families have been separated for at least 65 million years, thus providing the possibility for evolutionary change within each group.

The first comprehensive description of the crocodilian cardiovascular system was published in 1833 by an Italian scientist, Bartolomeo Panizza [32]. He gave a general description of the heart and circulatory system of Crocodilus lucius (subsequently classified as the American alligator, Alligator mississipiensis) and noted that a foramen existed between the right and left aortas (foramen of Panizza). Later studies in other species have confirmed these early findings and shown that the morphology of the crocodilian heart is uniform across the Alligatoridae and Crocodylidae 16, 37, 38, 39.

The crocodilian heart is four chambered, having two atria and a complete septum between the left and right ventricles. This feature separates the crocodilians from the rest of the reptilians which have a single ventricle subdivided into three anatomically interconnected chambers [see 8, 24, 37, 42, 47]. This complete division of the atria and ventricles excludes the possibility of intra-cardiac shunting and, in line with the adult avian and mammalian hearts, the crocodilian heart is capable of generating different pressures in the systemic and lung circulations (see Fig. 1, Fig. 5A and B). The extra-cardiac anatomy is one feature that makes the crocodilian cardiovascular system unique and, from a physiological perspective, complicated. As in amphibians and the non-crocodilian reptiles, crocodilians have retained two aortic arches, the left aortic arch leaves the right ventricle alongside the pulmonary artery and the right aortic arch emerges from the left ventricle and runs posteriorly as the dorsal aorta (Fig. 1). The left and right aortic arches communicate at two locations: the foramen of Panizza, and the “anastomosis” (see Fig. 1). The foramen of Panizza is an aperture in the common wall between the right and left aortae just at the base of the aortic arches. In describing the close association of the valves of the right and left aortic arches with the foramen of Panizza, Sabatier [33] noted that the interaction of the valves with the foramen could have a crucial effect on haemodynamics. Indeed, the occlusion of the foramen of Panizza by the aortic valves during systole has been the subject of much debate (see Physiology section). White [38] described the presence of cartilaginous struts which partly encircles the distal and lateral margins of the foramen [see Fig. 8 in Grigg [18]]. At present, nothing is known about the function of these cartilaginous struts, but Grigg [18] speculated that they may somehow be involved in the control of the diameter of the foramen. It should be noted that a foramen between the left and right aortae is not unique to the crocodilians. An interaortic foramen is also found in snakes. The anatomical arrangements of the aortic valves in relation to the foramen are complex and variable among species and so far no quantitative analysis has been made to explain the function of the foramen in this group [46].

The second communication point between the two aortic arches occurs just caudal and dorsal to the heart and consists of a vessel simply called the anastomosis (see Fig. 1, Fig. 2A and B). Although when viewed in situ, this vessel appears to be insignificant (small in diameter), corrosion vascular casts reveal that the internal diameter of the anastomosis is around 50% of the right aortic internal diameter (Fig. 2A) indicating that the anastomosis is capable of supporting high blood flows, a characteristic which has been substantiated by recent physiological studies (see Physiology section) [27].

The anatomical arrangements of the cardiac valves and the foramen of Panizza were recently investigated using high resolution angioscopy in an in situ perfused heart preparation [Fig. 3A, B, and C; see also URL b [45]] [3]. In the past and traditionally, our understanding of the anatomy and morphology of the crocodilian cardiovascular system has been based on measurements taken from freshly dissected material or preserved specimens. Such measurements are liable to suffer from artifacts associated with fixation shrinkage or trauma associated with dissection. In the in situ perfused heart, angioscopy allowed the inside of the heart to be viewed intact and performing physiologically, permitting the actual dynamics of cardiac valves to be analysed [3]. Of particular interest was the location of the foramen of Panizza with respect to the right aortic and left aortic valves. Anatomical descriptions based on dead material established that the foramen was tucked down into pockets formed by the aortic valve cusps 18, 37; i.e., both the left and right aortic valves covered the foramen when opened at peak systole and that only during diastole when the aortic valves are closed is there free communication between the two aortae. Angioscopy revealed, however, that only the medial cusp of the right aortic valve was capable of completely covering the foramen during peak systole [Fig. 4A; see also URL b [45] for quicktime sequences of the interaction between the aortic valves and foramen of Panizza]. Thus, during shunting when blood is leaving the right side of the heart via the left aorta, the medial left aortic valve does not occlude the foramen of Panizza even during a maximal shunt [Fig. 4A; [45]]. This anatomical arrangement has significant consequences as blood is able to flow from the left to the right aorta during the entire cardiac cycle (see Physiology section).

The use of angioscopy also allowed another unique morphological feature of the crocodilian heart to be observed, the cog-teeth-like valves [connective tissue protrusions as described by Rathke [34], Webb [37], and van Mierop and Kutsche [29]] which project from the walls of the subpulmonary conus a separate chamber in the right ventricle. These cog-teeth-like valves are positioned just proximal to the leaf-type pulmonary valves [Fig. 1 and Fig. 3C; URL b [45]] and during systole come together, resulting in an increase in the pulmonary outflow tract resistance. These protrusions may represent an actively controlled cardiac valve and evidence for their role in regulating shunting and producing the characteristic pressure pulse in the right ventricle is detailed in the following Physiology section.

Immunocytochemical methods have been employed to elucidate the innervation of some key sites in the cardiovascular system of Crocodylus porosus [27]. Not surprisingly and in line with other vertebrates, a rich innervation of the heart and major vessels was found. Of particular interest was the extent of innervation of some of the intriguing anatomical elements of the crocodilian heart including the foramen of Panizza and the anastomosis. A band of smooth muscle was found around the circumference of the foramen in a sphincter-like arrangement. This area has nerves showing immunoreactivities to tyrosine hydroxylase (indicator of adrenergic fibres), NPY, somatostatin, VIP, bombesin, and substance P [27]. Such a rich concentration and variety of nerve fibres and transmitters indicates that the foramen of Panizza is an important site for cardiovascular regulation and warrants a detailed investigation of the “variable calibre foramen hypothesis” proposed by Grigg and Johansen [21]. This hypothesis proposes that the diameter of the foramen may be actively controlled which would affect the resistance to flow through the aperture. Variations in the size of the foramen spike recorded from the same animals lends support to this hypothesis [see Grigg and Johansen [21]].

The anastomosis also was found to be richly innervated, the vessel walls having a well-developed adventitia and media (Fig. 2B). Nerves showing immunoreactivities to substance P, somatostatin, tyrosine hydroxylase, NPY, galanin, calcitonin gene-related peptide, VIP, and bombesin were demonstrated histochemically [27].

Section snippets

Pressure and Flow Haemodynamics

Since Greenfield and Morrow [17] first recorded the cardiovascular haemodynamics of the alligator, A. mississipiensis, the timing and characteristics of pressure and flow profiles in crocodilians have been the subject of many investigations. As for the morphology, all published work thus far indicates that the central haemodynamics of crocodilians are similar for species in both the Alligatoridae and the Crocodylidae [Spectacled caiman, Caiman crocodylus sp. [1]; American alligator, Alligator

Summary

In the review from 1989, Gordon Grigg speculated about the possible function of the shunt and put forward the theory about the reversed foramen flow. Today we have some evidence to substantiate this theory. In contrast to the right aortic valves, the anatomical arrangement of the left aortic valves has been shown to permit a continuous blood flow from the left aorta to the right via the foramen [3]. Moreover, in the pressurized system, the size of the foramen is around 30–40% of the right

Future directions

Although there has been marked increase in the number of investigations (more than 12 papers) on the cardiovascular system of crocodilians since Gordon Grigg's 1989 review, there still remain many unanswered questions, with many of those questions being formulated as a consequence of the recent research. The underlying goal is of course to be able to understand the functional significance of such an intriguingly complex cardiovascular system. To date, much of the emphasis has clearly been on

Acknowledgements

This review stems from the culmination of some very exciting, stimulating and enjoyable research periods, often in association with a team of colleagues, all of whom we thank. We thank Gordon Grigg and Stefan Nilsson for providing feedback on earlier drafts of this review.

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