2003, 111 Cases of Ophidian Gastritis Were Coded at Northwest Zoopath, Indicating That Gastritis Was a Significant Factor in the Animal’S Demise

A RETROSPECTIVE STUDY OF GASTRITIS IN SNAKES

Michael M. Garner, DVM, Dipl ACVP* and James T. Raymond, DVM, MS, Dipl ACVP

Northwest ZooPath, Snohomish, WA 98296 USA

ABSTRACT

Gastritis in snakes is most often reported as being caused by Cryptosporidium serpentis infection.4,5 There is a single report of salmonellosis caused by Salmonella arizonae.6 Although the agent and lesions associated with cryptosporidiosis have been well described,1,2 other causes of gastritis appear to be important in snakes. Idiopathic gastritis is an inclusive term for one or more forms of gastritis, for which the pathogenesis is currently not well understood. A thorough review of the common morphologic alterations is in progress; basically, these snakes have varying degrees of chronic mucosal erosion, ulceration and fibrosis, and mucosal mucous cell metaplasia. More acute lesions include mucosal glandular distention and necrosis, mixed inflammation, and mucosal edema. Lesions lack the proliferative mucosal changes and hypertrophy of muscular tunics typically seen with gastric cryptosporidiosis. No retrospective studies of gastritis in snakes have been published. This report documents the occurrence of gastritis in snakes submitted to Northwest ZooPath pathology service and provides preliminary evidence that other forms of gastritis are also important in snakes.

Table 1 summarizes the total numbers for the four major snake families and the identifiable causes of gastritis as determined by histologic examination. From 1994-2003, 111 cases of ophidian gastritis were coded at Northwest ZooPath, indicating that gastritis was a significant factor in the animal’s demise. Boids were the most frequent submissions, followed by colubrids, viperids and crotalids. Most cases of gastritis were idiopathic, followed by cryptosporidiosis, bacterial infection and other forms of parasitic gastritis. Idiopathic gastritis was most commonly diagnosed in boids and viperids, while cryptosporidiosis was most common in colubrids and crotalids.

Table 2 summarizes the species affected and causes of gastritis in boids. A trend was clearly apparent for idiopathic gastritis, particularly in annulated boas submitted from a single facility. Nearly half of the boids with idiopathic gastritis had concurrent inclusion body disease.

Table 3 summarizes the species affected and causes of gastritis in colubrids. Cryptosporidiosis was by far the most common cause of gastritis in this family. It is interesting to note that three cases diagnosed as cryptosporidiosis by immunofluorescent antibody testing (IFA) testing of fecal samples,3 two in boids and one in a colubrid, had no histologic evidence of cryptosporidiosis or abnormalities in the alimentary tract, suggesting the possibility of false positive test results for these animals.

2003 Proceedings Association of Reptilian and Amphibian Veterinarians 61 Table 4 summarizes the species affected and causes of gastritis in crotalids. Cryptosporidiosis was the most common cause of gastritis. Several cases of flagellate-associated gastritis and bacterial gastritis were also seen in this group, as were several cases of mixed bacterial and protozoan gastritis. Several cases of idiopathic gastritis were also seen in this group.

Table 5 summarizes the species affected and causes of gastritis in viperids. Most cases of gastritis in this family were idiopathic, although several cases of cryptosporidiosis and bacterial gastritis were also seen.

Our preliminary findings suggest that cryptosporidiosis is an important pathogen in snakes, and that incidence may vary among different families. We also provide evidence that other poorly understood forms of gastritis exist and cause significant disease in snakes.

LITERATURE CITED

1. Carmel B.P. and V. Groves. 1993. Chronic cryptosporidiosis in Australian elapid snakes: control of an outbreak in a captive colony. Aust. Vet. J. 70:293-295. 2. Brownstein, D.G., J.D. Strandberg, R.J. Montali, M. Bush, and J. Fortner. 1977. Cryptosporidium in snakes with hypertrophic gastritis. Vet. Pathol. 14:606-617. 3. Graczyk T.K., M.R. Cranfield, and R. Fayer. 1996. Evaluation of commercial enzyme immunoassay (EIA) and immunofluorescent antibody (FA) test kits for detection of Cryptosporidium oocysts of species other than Cryptosporidium parvum. Am. J. Trop. Med. Hyg. 54:274-279. 4. Kimbell L.M. 3rd, D.L. Miller, W. Chavez, and N. Altman. 1999. Molecular analysis of the 18S rRNA gene of Cryptosporidium serpentis in a wild-caught corn snake (Elaphe guttata guttata) and a five-species restriction fragment length polymorphism- based assay that can additionally discern C. parvum from C. wrairi. Appl. Environ. Microbiol. 65:5345-5349. 5. Morgan U.M., L. Xiao, R. Fayer, T.K. Graczyk, A.A. Lal, P. Deplazes, and R.C. Thompson. 1999. Phylogenetic analysis of Cryptosporidium isolates from captive reptiles using 18S rDNA sequence data and random amplified polymorphic DNA analysis. J. Parasitol. 85:525- 530. 6. Oros J., J. L. Rodriguez, P. Herraez, P. Santana, and A. Fernandez. 1996. Respiratory and digestive lesions caused by Salmonella arizonae in two snakes. J. Comp. Pathol. 115:185- 189.

2003 Proceedings Association of Reptilian and Amphibian Veterinarians 62 Table 1. Ophidian gastritis: total numbers by family and etiology. Family Total # Cryptosporidiosis Other Bacterial Idiopathic Parasites Boidae 46 10a (17%) 0 3 (6%) 33 (76%) Colubridae 34 26b (76%) 0 2 (6%) 6 (18%) Crotalidae 15 6 (40%) 3c (20%) 6 (40%) 4 (27%) Viperidae 16 3 (19%) 0 1 (6%) 12 (75%) Total 111 45 (41 %) 3 (3%) 12 (11%) 55 (50%) aMadagascar tree boa and Boelen’s python were Cryptosporidium positive by IFA, no parasites or related lesions seen histologically (normal gut). bBaja gopher snake was Cryptosporidium positive by IFA, no parasites or related lesions seen histologically (normal gut). cTwo cases of unidentified flagellates, one case of unidentified nematodes.

Table 2. Boid snakes: species and classifications of gastritis. Species # Cryptosporidiosis Other parasites Bacterial Idiopathic Annulated boa 25 0 1 (4%) 24 (96%)d Rosy boa 4 4 (100%) 0 0 0 Emerald tree boa 2 0 0 0 2 (100%) Misc. boa speciesb 63a (50%) 0 0 3 (50%) Ball python 2 1 (50%) 0 1 (50%) 0 Misc. python speciesc 72a (29%) 0 1 (14%) 4 (57%) Total 46 10 (22%) 0 3 (7%) 33 (73%) aMadagascar tree boa and Boelen’s python were Cryptosporidium positive by IFA, no parasites or related lesions seen histologically (normal gut). bOne each of Madagascar, Madagascar ground, Madagascar tree, Argentine, common, and unspecified boa species. cOne each of Burmese, Boelen’s, blood, coastal carpet, Mexican burrowing, Angolan pythons, and an unspecified Morelia sp. dTwelve annulated boas and one common boa also had inclusion body disease.

2003 Proceedings Association of Reptilian and Amphibian Veterinarians 63 Table 3. Colubrid snakes: species and classifications of gastritis. Species # Cryptosporidiosis Other parasitesBacterial Idiopathic Tentacled 6 5 (83%) 0 0 1 (17%) Leaf nosed 5 5 (100%) 0 0 0 King 5 2 (40 %) 0 2 (40%) 1 (20%) Rat 3 3 (100%) 0 0 0 Racer 2 2 (100%) 0 0 0 Garter 2 1 (50%) 0 0 1 (50%) Corn 2 2 (100%) 0 0 0 Indigo 2 2 (100%) 0 0 0 Milk 2 0 0 0 2 (100%) Misc. speciesa 54b (80%) 0 0 1 (20%) Total 34 26 (76%) 0 2 (6%) 6 (18%) aOne each of Baja gopher, Northern pine, Eastern ribbon, Eastern fox, Eastern hognosed, and twig mimic snake. bBaja gopher snake was Cryptosporidium positive by IFA, no parasites or related lesions seen histologically (normal gut).

Table 4. Crotalid snakes (all rattlesnakes): species and classification of gastritis. Species # Cryptosporidiosis Other parasites Bacterial Idiopathic Prairie 3 3 (100%) 0 2 (67%) 0 Aruba Island 2 2 (100%) 0 1 (50%) 0 Banded rock 2 0 1a (50%) 2 (100%) 0 Eastern D. back 2 0 1b (50%) 0 1 (50%) Misc. speciesc 6 1 (20%) 1a (20%) 1 (20%) 3 (60%) Total 15 6 (40%) 3 (20%) 6 (40%) 4 (27%) aUnidentified flagellate. bUnidentified nematode. cOne each of massasauga, pygmy, Western diamondback, dusky, neotropical and Mexican green rattlesnakes.

Table 5. Viperid snakes: species and classification of gastritis. Species # Cryptosporidiosis Other parasites Bacterial Idiopathic Gaboon 3 0 0 0 3 (100%) Rhinoceros 2 0 0 2 (100%) Wagler’s 2 0 0 0 2 (100%) Misc. speciesa 9 3 (33%) 0 1 (11%) 5 (56%) Total 16 3 (19%) 0 1 (6%) 12 (75%) aOne each of West African bush, white lipped tree, caucasian, desert, leaf nosed, speckled forest, and temple vipers, bushmaster, Eastern coral snake.

2003 Proceedings Association of Reptilian and Amphibian Veterinarians 64