The ophidian paramyxoviruses (OPMV) were first described in 1972 in a venom production laboratory in Zurich, Switzerland, affecting specimens of fer-de-lance (Bothrops moojeni) originating from Brazil.1 Since then, many outbreaks have been reported in the United States and Europe.3,5 The major clinical signs associated with OPMV infection are respiratory disease, abnormal posturing, head tremors, regurgitation, anorexia, mucoid feces, and death. Secondary invaders including Pseudomonas sp., Aeromonas sp., Salmonella sp., Morganella sp., Providencia sp., and other pathogens, may facilitate the primary viral infection. The major histopathologic findings of infection include proliferative pneumonia and necrotizing pancreatitis. Encephalitis and pancreatic hyperplasia may also be observed.3
OPMV has been reported in Brazilian snakes in the United States and Europe and was identified in the venom gland of a jararaca viper (Bothrops jararaca) in Brazil.4 Here we report the presence of OPMV in an epizootic outbreak of respiratory and central nervous system disease in neonatal urutus (Bothrops alternatus) in Brazil.
In December 2000, a female urutu housed in the Laboratory of Herpetology, Butantan Institute, São Paulo, Brazil, gave birth to 27 offspring. The animals were measured, weighed, and transferred to another room where snakes of different species were maintained. Forty days after the transfer, three of the neonates died without manifesting clinical signs of illness. Postmortem examination revealed mild pulmonary congestion. At that time, four other snakes (animal numbers 1, 2, 3, and 4) from the same litter developed clinical signs of respiratory and central nervous system disease. These four animals were euthanatized according to protocols recommended by Butantan Institute, followed by a complete gross postmortem examination. Tissue samples from major organs were collected, fixed in 10% buffered formalin, and routinely processed for light microscopy. Additional sections were obtained and processed for immunohistochemical assays as previously described.2
No significant postmortem findings were observed during gross examination of all four snakes. Histopathologic examination revealed proliferative pneumonia in animals 1, 2, and 4. One snake demonstrated giant cell pneumonia (animal 4), and another demonstrated giant cell pancreatitis (animal 1). No microscopic changes were detected in animal 3. No lesions were identified in the brain of the four animals. Immunohistochemical assays for OPMV antigen were strongly positive in pulmonary epithelial cells of animals 1, 2, and 4, and in the giant cell pancreatitis of animal 1. Bacteriologic cultures isolated Citrobacter braakii from the blood of animals 1 and 2, Enterobacter cloacae from the blood, lung, and liver of animal 3, and Salmonella arizonae from the lung and liver of animal 4.
OPMV is considered to be an important infectious agent of snakes. Death often occurs within 1 day following the onset of signs of illness. In many cases, clinical signs are subtle and may go unrecognized until death. In the present report, three snakes were found dead without prior clinical signs, and four presented with respiratory distress and opisthotonos before euthanasia. Using light microscopy, three of the four euthanatized snakes were found to have proliferative pneumonia. Although clinical central nervous system distress was identified prior to death, microscopic brain lesions were not observed in any of the animals examined. Immunohistochemical assays demonstrated the presence of OPMV antigen in pulmonary tissue from three of the snakes evaluated.
Postmortem microbiological cultures isolated gram-negative bacteria from the tissues of several snakes. Secondary bacterial infections have been reported with OPMV infections in snakes.3 OPMV may function as an immunosuppressive pathogen, allowing secondary bacterial organisms to become invasive and contribute to the severity of the disease.
The presence of OPMV in Brazil has been previously documented as an incidental finding in the venom gland of a jararaca viper (Bothrops jararaca).4 However, no illness was observed in this snake. The current study confirms the presence of OPMV in captive snakes in Brazil manifesting clinical signs of respiratory and central nervous system disease.
Additional studies are currently underway to isolate and partially sequence the virus and to determine the serological status of the snakes from the Laboratory of Herpetology, Butantan Institute.
This work was supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP grants #99/09459-7 and 00/02924-5) and the Conselho Nacional para o Desenvolvimento Científico e Tecnológico (CNPq).
1. Foelsch, D.W., and P. Leloup. 1976. Fatale endemische infektion in einem serpentarium. Tierarzt Praxis. 4:527–536.
2. Homer, B.L., J.P. Sundberg, J.M. Gaskin, J. Schumacher, and E.R. Jacobson. 1995. Immunoperoxidase detection of ophidian paramyxovirus in snake lung using a polyclonal antibody. J Vet Diag Invest. 7:72–77.
3. Jacobson, E.R., J.M. Gaskin, S. Wells, B.S. Bowler, and J. Schumacher. 1992. Epizootic of ophidian paramyxovirus in a zoological collection: pathological, microbiological and serological findings. J Zoo Wildl Med. 23:318–327.
4. Junqueira de Azevedo, I.L.M., A.R.B. Prieto e Silva, E. Carmona, and P. Lee Ho. 2001. Characterization of a paramyxovirus from a fer de lance viper: partial nucleotide sequence of putative fusion protein. Arch Virol. 156:51–57.
5. Oros, J., A. Torrent, P. Castro, S. Deniz, A. Arencibia, E.R. Jacobson, and B.L. Homer. 2001. Immunohistochemical detection of ophidian paramyxovirus in snakes in the Canary Islands. Vet Rec. 149:21–23.