Anatomy of the heart and coronary blood supply of the white-eared opossum (Didelphis albiventris)

[Anatomia do coração e do suprimento sanguíneo coronariano no gambá-de-orelha-branca (Didelphis albiventris)]

ABSTRACT

Although the white-eared opossum is frequently observed in both rural and urban environments, there is little anatomical knowledge about this marsupial species. To our knowledge, there are no descriptions of its heart anatomy. Thus, the aim of this study was to describe the anatomy of the heart and its coronary blood supply in the white-eared opossums. Eight adult white-eared opossums (Didelphis albiventris) were used. Heart anatomical features and the coronary blood supply were examined using gross dissection and latex cast preparations. The heart of the white-eared opossum was located between the second and fifth intercostal spaces. Pectinate muscles were observed inside the atria, while papillary muscles and chordae tendineae inside the ventricles. Left and right coronary arteries emerged from the ascending aorta. The main branches of the left coronary artery were the paraconal interventricular and circumflex branches, whereas the subsinuous interventricular branch was the main branch of the right coronary artery. The findings of this study suggest that it is likely that the white-eared opossum presents a balanced pattern without dominance by the coronary arteries, since each coronary artery has an interventricular branch. Furthermore, cardiac morphology in white-eared opossums did not differ from that reported for other domestic and wild mammals.

Keywords:
coronary arteries; heart; marsupial; white-eared opossum; wildlife

RESUMO

Embora o gambá-de-orelha-branca seja frequentemente observado tanto em ambientes rurais quanto urbanos, há pouco conhecimento anatômico sobre essa espécie de marsupial. Até onde se sabe, não há descrições de sua anatomia cardíaca. Assim, o objetivo deste estudo foi descrever a anatomia do coração e de seu suprimento sanguíneo coronariano em gambás-de-orelha-branca. Oito gambás-de-orelha-branca (Didelphis albiventris) adultos foram utilizados neste estudo. As características anatômicas do coração e do suprimento sanguíneo coronariano foram examinadas usando-se dissecção macroscópica e preparações de molde de látex. O coração do gambá-de-orelha-branca estava localizado entre o segundo e o quinto espaços intercostais. Músculos pectinados foram observados no interior dos átrios, enquanto músculos papilares e cordas tendíneas no interior dos ventrículos. As artérias coronárias esquerda e direita emergiram da aorta ascendente. Os principais ramos da artéria coronária esquerda eram os ramos interventriculares paraconais e circunflexos, enquanto o ramo interventricular subsinuoso era o ramo principal da artéria coronária direita. Os achados deste estudo sugerem que é provável que o gambá-de-orelha-branca apresente um padrão equilibrado, sem dominância das artérias coronárias, uma vez que cada artéria coronária possui um ramo interventricular. Além disso, a morfologia cardíaca em gambás-de-orelha-branca não diferiu daquela relatada para outros mamíferos domésticos e selvagens.

Palavras-chave:
artérias coronárias; coração; gambá-de-orelha-branca; marsupial; animais selvagens

INTRODUCTION

Marsupials represent an important subclass of mammals, which appear in Australia and the Americas, and include several species such as kangaroos, koalas, Tasmanian devil, sugar glider, and opossums (Nowak, 2005). Brazilian marsupials belong to the Order Didelphimorphia and Family Didelphidae. There are about 56 species of marsupials represented especially by opossums in Brazil, all belonging to the family Didelphidae, the family with the largest number of species of Neotropical marsupials (Cáceres, 2012; Rossi et al., 2012). These species are distributed in the Brazilian biomes, from the Amazon Forest to the Pampa in Rio Grande do Sul, with the greatest diversity of species found in the Atlantic and Amazon Forests (Melo and Sponchiado, 2012). The massive presence of these marsupials in the Atlantic and Amazon Forests is due to the adaptation of most species to the arboreal habit, being common for these animals to have a prehensile tail and an opposable digit (Melo and Sponchiado, 2012). However, not all Brazilian marsupials are arboreal, such as marsupials belonging to the genus Monodelphis, which are strictly terrestrial and have a short, non-prehensile tail (Melo and Sponchiado, 2012).

The Didelphis genus has six species, most of which have a wide geographic distribution. Of these six species, five appear in South America, and four are found in Brazil (Cáceres, 2012). Marsupials of the species Didelphis virginiana appear exclusively from the United States to Costa Rica (Flórez-Oliveros and Vivas-Serna, 2020) and Didelphis pernigra is not found in Brazilian territory, although it appears in some countries in South America. Brazilian didelphids comprise the species Didelphis albiventris, D. aurita, D. marsupialis and D. imperfecta (Cáceres, 2012).

One of the most common didelphids in the Brazilian territory is the species Didelphis albiventris, which is known as white-eared opossum, which is a small to medium-sized animal, weighing about one to two pounds as an adult. Its body coat is grayish-black, black on the tail and white on the ears and face, with a black stripe on the head, in addition to black spots around the eyes (Cáceres, 2002). The head has a triangular shape with an elongated snout with long vibrissae. The ears, except for their base which is black, are light in color. The distal end of the limbs is completely black. The tail is fully prehensile and covered with abundant hair at the base and scales to its tip (Flórez-Oliveros and Vivas-Serna, 2020).

The white-eared opossums have crepuscular and nocturnal habits. They are opportunistic and omnivorous animals, which have increasingly adapted to urban habits. Their diet is omnivorous and includes fruits, seeds, leaves, insects, molluscs and vertebrates of different sizes, and they often attack chicken coops and feed on bird eggs and chicks (Flórez-Oliveros and Vivas-Serna, 2020).

Although the white-eared opossum is frequently observed in rural and urban environments, there is little anatomical knowledge about this marsupial species. To our knowledge there are no descriptions of the heart anatomy in the Didelphis albiventris. Massari et al. (2019) stated that opossums can represent a great model for studying the anatomy of wild animals. Due to the fact that Didelphis albiventris is an important seed disseminating agent helping the recovery of degraded environments (Cáceres, 2002; Cáceres and Monteiro-Filho, 2007), in addition to the fact that it can be a wild reservoir of pathological agents, it is noteworthy that the white-eared opossum is a species of environmental and public health interest, so the objective of this study is to describe the anatomy of the heart and coronary blood supply of the white-eared opossum in order to fill a gap about the anatomy of these marsupials and contribute to subsidize veterinary clinical care.

MATERIALS AND METHODS

Eight adult white-eared opossums (Didelphis albiventris) of both sexes (5 males, 3 females) were donated by the Center for Medicine and Research in Wild Animals (CEMPAS), School of Veterinary Medicine and Animal Sciences, UNESP, Botucatu, São Paulo. The marsupial corpses were taken to the Laboratory of Wildlife Anatomy, Institute of Biosciences of Botucatu, to study the morphology and topography of the heart and coronary blood supply as authorized by the Committee on the Use of Animals of School of Veterinary Medicine and Animals Science, UNESP (CEUA 7380270922).

The specimens were divided into Groups A (n=5) and B (n=3). Group A was used to study heart morphology and Group B used to study coronary vasculature. Group A specimens were fixed with 10% formaldehyde solution injected into muscles, abdominal cavity and thoracic cavity, then submerged in the solution for 7 days (Pinheiro et al., 2014). After fixation, the skin, subcutis, thoracic limb and trunk muscles were removed. Finally, the intercostal muscles were opened, the left wall removed, and the topography of the heart was observed. Next the hearts were removed from the thoracic cavity and the exterior examined. The aorta and its divisions and branches were identified. The hearts were opened longitudinally to observe the interior of the heart. One heart was opened along the coronary groove and the atria separated from the ventricles to study the A-V ostia.

The Group B hearts were removed to study the coronary blood supply. The left thoracic wall was opened through the sternum and the heart removed. The major blood vessels were identified and isolated. Aortas from two marsupials were cannulated and perfused with red latex in the retrograde direction to identify the coronary arteries. Hearts were static for 24 hours to allow the latex to solidify (Cury et al., 2013). Subsequently, they were submerged in 10% formalin for 7 days (Pinheiro et al., 2014). The aorta of one animal of the Group B was cannulated and perfused with G4 rigid epoxy resin (Polipox^®) colored with red silkscreen paint, until the coronary arteries were filled. Resin polymerization occurs within 72 hours (Santos et al., 2021) therefore, the heart was not handled during this time. After this period, the heart was submerged in hydrochloric acid P.A. The immersed heart was examined daily until the cardiac tissues corroded and the injected coronary arteries became evident, in about three weeks. Afterwards, the heart was removed from the acid bath and rinsed in tap water to remove the remaining tissue. The casts were photographed using a digital camera (Canon G7 X Mark II). Nomina Anatomica Veterinaria (2017) terms were used to name the identified structures.

RESULTS

The heart of the white-eared opossum (Didelphis albiventris) was located in the middle mediastinum lying on the sternum, between the right and left lungs, in an oblique disposition with its base directed dorsocranially and its apex ventrocaudally and to the left. The heart was located between the second and fifth intercostal spaces (Figure 1) within the pericardium. The cardiac notch was present between the cranial and middle lobes of the right lung and allowed exposure to part of the atrial surface of the opossum heart. The phrenicopericardiac ligament extended from the apical pericardium to the ventral part of the diaphragm (Figure 1).

The heart base was bulging and wide craniodorsally which tapered caudoventrally into the apex. The classic four chambers were noted with the two classic surfaces: atrial and auricular. On the atrial surface all four chambers were observed with the subsinuosal interventricular groove indicating the division between the ventricles and carrying the middle cardiac vein from the coronary groove to the apex (Figure 2). On the auricular surface, the demarcation between the ventricles was determined by the paraconal interventricular groove, which delimited the ventricles more sharply than the subsinuosal interventricular groove on the atrial surface. Right and left auricles were proeminent on the auricular surface, in addition to the pulmonary trunk and the aorta (Figure 2). The coronary groove appeared at the boundary between the atria and ventricles, demarcating the caudal margin of the cardiac base, which is formed by the right and left atria.

The pulmonary trunk continued from the right ventricle and conus arteriosus or right ventricular outflow track (Figure 2) and bifurcated into the right and left pulmonary arteries. The ascending aorta emerged from the left ventricle (just to the left of the pulmonary trunk) and moved cranially and curved dorsally, to give rise to the aortic arch. The brachiocephalic trunk and left subclavian artery emerged from the aortic arch. The brachiocephalic trunk was the first branch of the arch and gave origin to the right subclavian artery and bicarotid trunk, which, in turn, bifurcated into the right and left common carotid arteries (Figures 2 and 3).

Figure 1
Topographical location of the opossum heart through opened intercostal spaces (A) and ventral view of the heart in situ (B) of the white-eared opossum. 1, cranial lobe of the right lung; 2, middle lobe of the right lung; 3, caudal lobe of the right lung; 4, cranial lobe of the left lung; 5, caudal lobe of left lung; 6, accessory lobe of right lung; 7, caudal vena cava; 8, pericardium; 9, phrenicopericardiac ligament; r1, first rib; r13, last rib (13^th rib); is2nd, second intercostal space; is3rd, third intercostal space; is4th, fourth intercostal space; is5th, fifth intercostal space. Bar=1 cm.

Figure 2
Auricular (A) and atrial (B) surfaces of the white-eared opossum heart. 1, right auricle; 2, right ventricle; 3, left auricle; 4, left ventricle; 5, paraconal interventricular groove; 6, conus arteriosus; 7, pulmonary trunk; 8, aortic arch; 9, thoracic aorta; 10, brachiocephalic trunk; 11, right subclavian artery; 12, bicarotid trunk; 13, left subclavian artery; 14, right common carotid artery; 15, left common carotid artery; 16, left atrium; 17, right atrium; 18, cranial vena cava; 19, caudal vena cava; 20, subsinuosal interventricular groove. Bar=1 cm.

Figure 3
Cranioventral view of isolated white-eared opossum heart and lungs. 1, right atrium; 2, right ventricle; 3, left ventricle; 4, conus arteriosus; 5, pulmonary trunk; 6, ascending aorta; 7, left phrenic nerve; 8, brachiocephalic trunk; 9, right subclavian artery; 10, bicarotid trunk; 11, right subclavian artery; 12, left common carotid artery; 13, right common carotid artery; 14, right phrenic nerve; 15, trachea; 16, cranial vena cava; 17, cranial lobe of right lung; 18, middle lobe of right lung; 19, caudal lobe of right lung; 20, accessory lobe of right lung; 21, caudal vena cava; 22, cranial lobe of left lung; 23, caudal lobe of left lung. Bar=1cm.

The abundance of pectinate muscle (Figure 4), in the auricles of the white-eared opossum was most striking. The ostia of the cranial and caudal vena cavae with the intravenous tubercle separating then, were observed in the right atrium. In addition, the fossa ovalis was visualized on the interatrial septum of the right atrium, caudal to the intravenous tubercle (Figure 4).

The ventricles were separated by the interventricular septum (Figure 5). There were conical papillary muscles (3 - right & 2 - left) in the ventricles. These finger-like projections gave the chordae tendineae (Figure 5). A right septomarginal trabecula was also observed, crossing the right ventricle, connecting the interventricular septum with the external/free cardiac wall (Figure 5).

Figure 4
Internal view of the dorsum of the opened right atrium (A and B). Internal view of the dorsum of the opened right and left atria (C). 1, pectinate muscles; 2, ostium of the caudal vena cava; 3, ostium of the cranial vena cava; 4, cavity of the right auricle; 5, intervenous tubercle; 6, oval fossa; 7, interatrial septum; 8, pulmonary trunk; 9, aorta; LA, left atrium; RA, right atrium. Bar=1cm.

Figure 5
Internal view of the right (A) ventricle and right and left cardiac ventricles (B) in the white-eared opossum heart. 1, papillary muscles; 2, right septomarginal trabecula; 3, chordae tendineae; 4, free wall of left ventricle (myocardium); 5, right ventricle; 6, interventricular septum. Bar=1cm.

When the atria were removed, it was observed that both the atrioventricular ostia and the pulmonary trunk ostia were oval, the latter being slightly more rounded. When comparing the atrioventricular orifices, a greater diameter was noted for the right orifice, which contained the right atrioventricular (tricuspid) valve, formed by three cusps anchored by chordae tendineae. The left atrioventricular ostium, housed the left atrioventricular (bicuspid) valve, composed of two cusps. The valve of the pulmonary trunk formed by three valvulae was also observed in the pulmonary ostium. Axially to the atrioventricular and pulmonary ostia, the aortic ostium was observed, in which the aortic valve was formed by three valvulae (Figure 6).

Figure 6
Dorsal view of white-eared opossum heart with atria removed. 1, left atrioventricular ostium; 2, pulmonary trunk ostium; 3, right atrioventricular ostium with right coronary artery; 4, right atrioventricular valve (septal cusp); 5, aortic ostium; 6, aortic valve. Bar=1cm.

The coronary arteries arose from the ascending aorta out of their respective semilunar sinus. The left coronary artery was short and bifurcated into the paraconal interventricular and circumflex branches (Figure 7). The paraconal interventricular branch coursed in the paraconal interventricular groove and gave off several septal and muscular branches. It terminated near the apex (Figures 7 and 9). The circumflex branch followed the coronary groove caudally and gave off atrial branches (Figure 7).

The right coronary artery emerged cranially from the right sinus of the semilunar valve and followed the coronary groove past the right atrium dispatching the right marginal, muscular and atrial branches. Near the caudal aspect of the right atrium, it deviated caudally into the subsinuosal interventricular groove and terminated near the apex (Figures. 8 and 9). No anastomoses were observed between the circumflex branch and the subsinuosal interventricular branch.

Figure 7
Auricular surface (A) and left ventricular margin of the auricular surface (B) of the white-eared opossum heart with latex injected into coronary vessels. 1, paraconal interventricular branch; 2, ventricular branches; 3, left auricle; 4, right auricle; 5, ascending aorta; 6, pulmonary trunk; 7, circumflex branch; 8, atrial branch; 9, ventricular branch. Bar=1cm.

Figure 8
Atrial surface of the white-eared opossum heart with latex injected into coronary vessels: right atrium and auricle retracted with forceps. 1, right coronary artery; 2, ventricular branches; 3, right marginal branch; 4, subsinuosal interventricular branch; 5, conus arteriosus; 6, ascending aorta; 7, right atrium (retracted with forceps); 8, atrial branch; 9, right lung. Bar=1cm.

Figure 9
Atrial view of white-eared opossum heart with epoxy injected into coronary vessels and microvasculature (A,B,C). 1, subsinuosal interventricular branch; 2, ventricular branches; 3, right coronary artery; 4, right coronary artery arising from the aortic bulb; 5, ascending aorta; 6, right marginal branch; 7, paraconal interventricular branch. Bar=1cm.

DISCUSSION

The topography and morphology of the heart and coronary blood vessels of the white-eared opossum (Didelphis albiventris) was observed and recorded. The white-eared opossum heart is similar to that described in other mammals. These findings are compared with non-didelphid mammals, as there were no reports found in the literature on the cardiac anatomy of the genus Didelphis. The anatomy of this Brazilian marsupial is important for the biological knowledge of the species, in addition to supporting the medical care of these animals.

The conical shape and location of the heart in the opossum in the middle part of the mediastinum are similar to descriptions for other wild animals such as paca (Ávila et al., 2010), lesser anteater (Pinheiro et al., 2014), capuchin monkey (Furtado et al., 2017), common marmoset (Falcão et al., 2020) and giant anteater (Santos et al., 2021).

The hearts of the animals in this study were found between the second and fifth intercostal spaces. It seems that this topography varies according to the species of animal studied, since in non-human primates such as capuchin monkeys and white-tufted marmosets, their hearts occupy the third to fifth intercostal space (Falcão et al., 2020; Rocha Neto et al., 2015). According to Ávila et al. (2010), the heart of the paca is found between the first and fifth intercostal spaces.

In this study, a phrenicopericardiac ligament was observed. Singh (2019) suggested that the ligament appears in species with an oblique cardiac axis. The ligament restricts cardiac mobility but allows small movements to occur in each respiratory excursion. The findings of this study corroborate the previous statements, as the opossum's heart has an oblique disposition. It is noteworthy that other species such as pacas do not have this ligament, having only the sternopericardiac ligament, although the paca heart is also obliquely oriented (Ávila et al., 2010).

Branching of the aortic arch first gave rise to the brachiocephalic trunk and then the left subclavian artery. The brachiocephalic trunk gave rise to the bicarotid trunk and right subclavian artery. The bicarotid trunk, in turn, bifurcated into the right and left common carotid arteries. These findings are similar to the pattern most found in a previous study in the white-eared opossums (Schimming et al., 2016).

The hearts studied showed most of the structures routinely found in wild mammals such as the paca (Ávila et al., 2010), capuchin monkey (Furtado et al., 2017), common marmoset (Falcão et al., 2020) and giant anteater (Santos et al., 2021) had similarities. The right septomarginal trabecula extending across the lumen of the right ventricle was similar to the paca (Ávila et al., 2010).

The aorta emitted the right and left coronary arteries from their respective aortic semilunar sinuses. Each coronary artery dispatched an interventricular branch, characterizing a balanced pattern without dominance by either coronary artery. The left coronary artery originated the paraconal interventricular branch, while the right coronary artery continued as the subsinuosal interventricular branch much like the domestic pig and horse (Singh, 2019). This branching pattern was similar to that described for paca (Ávila et al., 2009), lesser anteater (Pinheiro et al., 2014), puma (Viotto-Souza et al., 2017) and giant anteater (Santos et al., 2021). On the other hand, these findings differed from those reported for the domestic cat, dog, ruminants (Singh, 2019), and brown brocket deer (Zaniboni et al., 2021), where the subsinuosal interventricular branch originates from the circumflex branch of the left coronary artery, which represents a pattern of left coronary dominance.

Ventricular, atrial, and right and left marginal branches arising from the coronary arteries directly or from their branches have also been reported in other wild mammals such as the puma (Viotto-Souza et al., 2017), brown brocket deer (Zaniboni et al., 2021) and giant anteater (Santos et al., 2021). Accessory elements such as the right accessory coronary artery and the accessory subsinuosal interventricular branch described for the giant anteater (Santos et al., 2021) were not found in the hearts of the white-eared opossum.

The heart of the white-eared opossum (Didelphis albiventris) is anatomically and topographically similar to that reported for domestic and wild mammals, differing by being located in a more cranial or caudal intercostal space depending on the animal with which we compare it. The knowledge of this cardiac topography is important for the clinical examination of the white-eared opossum. In addition, the coronary blood supply is carried out through both the right and left coronary arteries and characterizes a balanced pattern without dominance on the part of the coronary arteries, since each one emits an interventricular branch. The description of the heart of the white-eared opossum has not yet been described and this information could add to a better understanding of this species especially during a clinical examination of this marsupial.

ACKNOWLEDGMENTS

The authors would like to thank Center of Medicine and Research in Wild Animals (CEMPAS), School of Veterinary Medicine and Animal Science, UNESP, for providing the animals used in this study, and to The São Paulo Research Foundation (FAPESP), São Paulo, Brazil, for LCO scholarship (process 2022/03940-3).

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Publication Dates

• Publication in this collection
  14 July 2025
• Date of issue
  Jul-Aug 2025

History

• Received
  21 Jan 2024
• Accepted
  21 Jan 2025