Drury Reavill, DVM, DABVP (Avian and Reptile/Amphibian Practice), DACVP; Ethan Biswell, DVM, DACVP
Abstract
This paper will cover the diseases of the cardiovascular system in reptiles and amphibians. It is not intended as a comprehensive review. In-depth disease descriptions can be found in the references cited. The paper is divided by etiologic disease categories involving the cardiovascular system. A short discussion of the disease conditions occurring in reptiles and amphibians is found in each section.
Introduction
Poikilotherms have been considered to have few primary cardiovascular disorders.1 Clinical cardiovascular disorders may be primary or secondary and are associated with infection, parasitism, nutritional imbalances, and poor husbandry practices.2 This section will present a limited review of reptile cardiovascular pathology.
Developmental Anomalies
Developmental anomalies are reported to be common in reptiles3 and are usually associated with deaths of juveniles.1 Incomplete development of the atrioventricular valves has been described, leading to incomplete valve closure.4 A secundum atrial septal defect was described in a Komodo dragon (Varanus komodoensis).5 The lesion was on the craniodorsal portion of the septum. It led to chronic congestion of several organs. Two juvenile ball pythons (Python regius) with bifid ventricles were reported.6 All cardiac chambers were enlarged; the lesion disrupted the ability to separate pressures within the ventricles. An interventricular septal defect was also reported in an alligator (Alligator mississippiensis).7
Noninfectious Diseases
Aortic aneurysm rupture leading to cardiopulmonary arrest was described in a Burmese python (Python molurus bivittatus), and the exact cause was not determined.1 Dissecting aortic aneurysm in a bearded dragon presented with acute listlessness, weakness, and general pallor. A pericardial hemorrhagic effusion produced an enlarged cardiac silhouette on radiographs.8 Arteriosclerosis has been documented in green iguanas (Iguana iguana),9 and dystrophic mineralization of arteries is seen in various lizards.4 Mineralization of arteries is most likely due to secondary nutritional hyperparathyroidism from a calcium deficiency. A mole king snake (Lampropeltis calligaster rhombomaculata)10 and a Deckert’s rat snake (Elaphe obsoleta deckerti)11 were diagnosed with cardiomyopathy of undetermined cause. The lesions in the king snake were primarily collagen proliferation and osteoid-like material, while the rat snake had degeneration and necrosis of myocardial fibers. Aortic stenosis with associated dilatation of the right atrium and the ventricle were found in an iguana.12 Histologically, both aortic arches had narrow lumens with thickened intimae, and the myocardial fibers were attenuated. Although the cause was not determined, the authors considered a chronic congenital lesion as one possibility.
A bearded dragon with severe atherosclerosis was also associated with hypertensive heart disease. The adult animal had bradyarrhythmia and balance abnormalities. Cardiac function was evaluated with electrocardiography (ECG) and echocardiography, which identified an AV block. Atherosclerosis is uncommon in reptiles.13
Myocardial degeneration due to vitamin E deficiency has been seen in several reptile species.14 Grossly and microscopically, the lesion is similar to that described in mammals. The heart will have mottled white to grey myocardium, and histologically there will be multifocal to coalescing loss of myocytes replaced with dense fibrous stroma. Visceral gout can lead to severe pericardial lesions,15 as well as changes in the myocardium. These can include thickening of the pericardial sac with a deposition of the urate crystals as well as crystals forming within the myocardium. Primary disease can be nutritional or toxic.16
Infectious Diseases
Infectious agents affecting the heart are usually secondary to systemic illness.2 West Nile virus infection led to myocardial degeneration and necrosis in a farmed American alligator.17 Arenavirus (inclusion body disease of boids) inclusions have been identified in cardiac myocytes; however, they do not appear to be associated with any clinical changes.18
Iridovirus has been recognized as systemic infections in both salamanders and frogs. Infections in frogs are characterized by increased tadpole mortality and are best described in the tadpoles of the American bullfrog. There will be hemorrhage identified in the skin and muscle, as well as stomach. Necrotic foci are recognized in the liver, kidney, and intestines. A viral epizootic has been recognized in larval and adult tiger salamanders. The primary lesion was a skin lesion with cutaneous ulcers and erosions. These epithelial cells contain large cytoplasmic inclusions. Systemic effects were noted; however, no specific lesions were associated with the direct viral infection. Intracytoplasmic viral inclusions were in the heart sections.19,20
Mycoplasma infection was seen in American alligators (Alligator mississippiensis).21 Rapidly growing mycoplasmas were identified by culture and polymerase chain reaction. The alligator isolate is a novel species in the Mycoplasma family.
Bacterial disease has been reported in conjunction with endocardial thrombosis,22 endocarditis,23 endocarditis valvularis,24,25 and myocarditis.26 A bacterial infection resulting in a necrotizing myocarditis and multiple granulomas in the kidney was suspected in a boa constrictor. The lesion was suspected to have been due to a bite wound on the ventrum, and that may have penetrated the underlying heart.27 A severe bacterial pneumonia (Salmonella enterica ssp. IV, Enterobacter cloacae, and Klebsiella pneumoniae) in a Burmese python was associated with endocarditis of the pulmonic valve and a dilated truncus pulmonalis. An additional lesion of arteriosclerosis of the pulmonary trunk was present. Grossly, the lesion on the pulmonic valve was a cauliflower-like mass lesion.25 Valvular endocarditis is described in an Argentine boa (Boa constrictor occidentalis) with a concurrent arenavirus infection. A vegetative lesion was present on the right atrioventricular valve with valvular insufficiency and a mildly dilated right atrium. The granuloma on the cardiac valve contained gram-positive cocci. In addition, there was a subacute bronchopneumonia and air sacculitis with edema.24 Mycobacterial infections, although uncommon in reptiles, have involved the heart.28
Systemic gram-negative bacterial septicemias commonly involve the cardiovascular system in amphibians. The frequent clinical presentation is of generalized ascites or localized edema. The best-known bacteria in these cases include Aeromonas hydrophila, Flavobacterium spp., Klebsiella pneumoniae, Proteus mirabilis, and Chlamydophila species.29,30 Mycobacterial infections are common in some species of amphibians. These are also generally systemic infections, involving the heart.28
Chlamydophila sp. infection is a cause of heart disease in reptiles. Granulomatous pericarditis and myocarditis were found in puff adders (Bitis arietans)31 and necrotizing myocarditis in green turtles (Chelonia mydas).32 Organisms could be demonstrated in macrophages in sections of paraffin-embedded heart. In emerald tree boas (Corallus caninus), there were histiocytic granulomas in the heart as well as in other organs. Small, basophilic organisms were seen on hematoxylin and eosin-stained sections. Transmission electron microscopy of an intestinal granuloma demonstrated developmental stages of the chlamydial organisms.33 A combined infection of Chlamydia species and Aeromonas sobria resulted in a systemic infection including the liver, spleen, kidneys, heart, and the respiratory tract in farmed juvenile Siamese crocodiles (Crocodylus siamensis). The inflammation was a severe necrotizing lymphohistiocytic and heterophilic response.34
Systemic fungal infections commonly involve the heart in various amphibians.35 The most commonly reported systemic fungus in amphibians is Chromomycosis. The lesion is associated with pigmented fungal organisms from the genera Cladosporium, Fonsecaea, Phialophora, Rhinocladiella, Hormodendrum, Curvularia, and Drechslera, among others. These fungi are saprophytes that live in soil and decaying vegetable matter, and they are potentially zoonotic. In tissue, they produce characteristic amber-brown, thick-walled septate structures known as sclerotic bodies. Chromomycosis generally presents first as an ulcerated or granulomatous skin lesion. These lesions can be nodules, grey-black papules, and/or irregularly shaped grey-black ulcers. The most common sites for external lesions are the dorsal and ventral skin surfaces. Over a period of time (which can be >6 months), the animal succumbs to disseminated disease. On gross examination, multiple organs may contain multiple coalescing grey-black nodules. These granulomas are commonly described in the liver and kidney, but they also occur in the spleen, lung, heart, adrenal, gastrointestinal tract (serosal and mucosal surfaces), bone, and central nervous system.36 Exfoliative cytology of the cutaneous lesions may have mononuclear cells surrounding pigmented, septate fungal hyphae. These organisms are zoonotic with human infection resulting from the contaminated environment.
Encephalitozoon pogonae can result in a systemic infection in bearded dragons. The infection has occurred in the great vessels in the heart, resulting in a granulomatous arteritis. An acute and severe hemopericardium developed in two cases.37
Spirorchid fluke (Digenea: Spirorchidae) infections have been recognized in a variety of marine turtles. From necropsies of 96 stranded green turtles, cardiovascular lesions included mural endocarditis, arteritis, and thrombosis—frequently accompanied by aneurysm formation.38 Spirorchiid trematode eggs were noted in the heart and other organs in black turtles (Chelonia mydas agassizii).39 Seventy-five adult Learedius learedi were recovered from the heart of one of the turtles.39 Loggerhead turtles (Caretta caretta L.) supported lesions from two spirorchiids, Hapalotrema mistroides and Neospirorchis species. The lesions were mild with no obvious clinical signs. Rarely vasculitis was observed in the heart and great vessels.40
During a 5-year period, 16 freshwater turtles (Trachemys scripta elegans and Chrysemys picta) died spontaneously.41 Necropsy lesions included subcutaneous edema, hepatic necrosis, pancreatic necrosis, splenic necrosis, and intestinal parasites. Histologically, trematode eggs were seen within the myocardium and in other tissues, associated with granulomatous lesions. The size and distribution of the eggs were consistent with Spirorchis sp. infection. Fluke infections can result in parasites within the three chambers of the heart and in major vessels (right aortic arch and brachiocephalic artery), attached to the walls, or free in the lumen.42
Whiptail lizards (Cnemidophorus spp.) from Texas and Colorado (USA) were examined for Mesocestoides sp. tetrathyridia, and 11 (5%) were infected. Free tetrathyridia were found in the body cavity of lizards, and encapsulated tetrathyridia were observed in the heart, liver, and stomach.43
The invasive coqui frogs (Eleutherodactylus coqui), as well as Cuban greenhouse frogs (Eleutherodactylus planirostris) and cane toads (Rhinella marina) serve as paratenic hosts for the lungworm (Angiostrongylus cantonensis), an important human health concern in Hawaii. Larval migration was identified through the stomach, intestines, muscle, liver, heart, and brain.44
Neoplastic Diseases
Primary tumors of the reptile cardiovascular system are not common. Among those reported are a rhabdomyosarcoma in a boa constrictor (Boa constrictor), a hemangiosarcoma in the heart of a Madagascar giant hognose snake (Leioheterodon madagascariensis; family Colubridae),45 and a fibrosarcoma in a Gaboon viper (Bitis gabonica).46 Other tumors that may be primary or part of a disseminated process include lymphoblastic malignant lymphoma in several species of reptiles46 and malignant chromatophoromas in bearded dragons.47 Thirty-nine percent of green turtles with fibropapillomatosis (FP) had disseminated internal tumors, most of them in the lung, kidney, and heart.48 A disseminated mast cell tumor diagnosed in an eastern kingsnake (Lampropeltis getulus getulus) involved the heart and numerous other organs.49 A disseminated chondrosarcoma involved the heart in a corn snake (Elaphe guttata).50 Large areas of myocardium had been replaced by neoplastic tissue. A metastatic oviductal adenocarcinoma has also been reported in the heart of a corn snake.51
Vascular tumors include hemangiosarcomas and hemangiomas. These are uncommon tumors in reptiles. A corn snake developed a mid-body swelling, and the extraluminal mass was a splenic hemangiosarcoma.52 A similar case has been reported in a lizard.53 Hemangiomas are also very rare, with two cases reported: a corn snake with an atrial cardiac tumor and an esophageal tumor in a red-eared slider.54,55 Some tumors that have been tested were positive for factor VIII-related antigen, by immunohistochemistry.45
Spontaneous and primary cardiac tumors of amphibians are not reported in the literature (VIN and PubMed search, April 2020).
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