Paramyxoviruses

PARAMYXOVIRUS IN REPTILES

Paramyxoviruses have been detected worldwide and are considered important pathogens in private and zoological collections (Folsch et al., 1976; Jacobson el al., 1992; Essbauer et al., 2001; Kolesnikovas et al., 2006).

These are medium sized encapsulated monocaternary RNA viruses that belong to the Paramyxoviridae family, which is divided in to two subfamilies: Paramyxoviridae and Pneumovirinae. Paramyxovirinae is composed of the following genres: Rubulavirus, Avulavirus, Respiravirus, Henpavirus and Morillivirus. The subfamily Paramyxovirinae is divided in to Pneumovirus and Metapneumovirus. Although these are all related, they seem to form two large groups (Ahne et al., 1999; Franke et al., 2001).  

The Fer-de-Lance virus (FDLV) was the first isolated virus in snakes and it is considered the type species or virus with the complete genome having already been sequenced and analysed. All related Paramyxoviruses have hemoglutinating, neuramidase activity (similar to receptor destroying enzyme present in Vibrio cholera) and are fusogenic like Reovirus. Research classified this virus within Paramyxovirinae and in the newly proposed genre: Ferlavirus (Kurath et al., 2004). Currently, two groups are present (A and B) and also a third group C (Abbas et al., 2011).

The first case isolated in reptiles was in a serpentaurium in Switzerland in 1976 (Fölsch et al., 1976). The virus isolated is considered the current type virus (Clark et al., 1979). This has been described in eight speceis of lizards (Gravendyck et al., 1998; Marschang et al., 2002; Jacobson et al., 2001) and numerous species of snakes (Ahne et al., 1999; Franke et al., 2001; Foelsch & Leloup, 1976). Koch's postulates were proved in the species Crotallus unicolor (Jacobson et al., 1997)

Transmission is considered direct contact through excretions (oral and cloacal) and possibly vectors (water, mites, aerosols and fomites), although the virus has not been isolated nor detected by PCR from mites or fomites  at time of writing (Hyndman et al., 2013). Vertical transmission has not been proven either (Pasmans et al., 2008).

Incubation period is unclear but could be as soon as 21 days (Hernandez-Divers, 2006) and generally exceed 90 days (Hernandez-Divers, 2006; Ritchie, 2006), although these are not supported by control studies (Hyndman et al., 2013).

Snakes typically present with respiratory signs, although central nervous signs may also be evident. Clinical signs may include head tremors, opisthotonos, respiratory difficulty, regurgitation, anorexia or sudden death. Infections have been described in Boidae, Elapidae, Colubridae and Crotalide (Jacobson et al., 2007). Infections in lizards are less frequent and antibodies have been found in captive and wild lizards (Gravendyck et al., 1998); Marschang et al., 2002; Ahne et al., 1991; Lloyd et al., 2005).Infections are rare in chelonia and clinical signs observed include dermatitis (Zangger et al., 1991) and pneumonia (Marschang et al., 2009; Papp et al., 2011) although it was unclear if the virus was the causative agent as it was not isolated from the lung.

Post-mortem findings may include exudtive pneumonia, hepatomegaly, enlarged pancreas, fluid in the coelomic cavity and pale kidneys. Microscopically, snae lungs often appear congested with hemorrhages, pulmonary  proliferative interstitial disease with intracytoplasmatic inclusions that may appear in small numbers (Jacobson et al., 1992, 1997, 2001), pancreatitis, nephritis and encephalitis.

Diagnosis in live animals is by antibody detection through hemoglutination inhibition or viral detection via PCR (RT-PCR) with cloacal and oral swabs. Viral isolation is also possible but less sensitive. There are numerous laboratories where the tests can be run. In dead animals, histopathology (detection of intranuclear inclusionsor sometimes intracytoplasmatic inclusions from the liver, lung, pancreas, kideny and brain), PCR and viral isolation are possible. Immunohistochemistry and in-situ hibridation have also been described.

Laboratory samples: 
Dead animals: lung or intestine in formaline (histology) and fresh or frozen (PCR or viral isolation).
Live animals: Cloacal and oral swabs in plain tube (PCR), and plasma or serum (antibody detection).

Antiviral drugs have been used in mammalian paramyxoviral infection and may be used to treat reptilian patients (Chong et al., 2009).

Prevention should be through 60-90 days of strict quarantine. Cloacal and oral swabs are also beneficial, as are necropsies of dead animals, parasitology testing and treatment as necessary, serological testing before and after quarantine and disinfections (EAZA - Ophidian paramyxovirus infection, 2009).


References and Advanced Reading

Ahne W, Batts WN, Kurath G, et al. Comparative sequence analyses of sixteen reptilian paramyxoviruses. Virus Res 1999;63:65–74.

Ahne W., Neubert W.J. Isolation of paramyxovirus-like agents from teju (Callopistes maculatus) and python (Python regius). Proceedings of the Second International Symposium on Viruses of Lower Vertebrates; Corvallis, OR, USA. 29–31 July 1991.

Chong HT, Kamarulzaman A, Tan CT, et al. Treatment of acute Nipah encephalitis with ribavirin. Ann Neurol 2001;49:810–3.

EAZA - Ophidian Paramyxovirus Infection, 2009

Essbauer S., Ahne W. Viruses of lower vertebrates. J. Vet. Med. B. 2001;48:403–475.

Fölsch D.W., Leloup P. Fatale endemische Infektion in einem Serpentarium. Tierärztl. Praxis. 1976;4:527–536.

Franke J, Essbauer S, Ahne W, et al. Identification and molecular characterization of 18 paramyxoviruses isolated from snakes. Virus Res 2001;80:67–74.

Gravendyck M, Ammermann P, Marschang RE, et al. Paramyxoviral and reoviral infections of iguanas on Honduran Islands. J Wildl Dis 1998;34:33–8.

Hernandez-Divers SJ. Appendix A: Reptile viral diseases – summary table. In: Reptile Medicine and Surgery, Elsevier, St. Louis, 2006:1147–1158. 

Hyndman TH, Shilton CM, Marschang RE. Paramyxoviruses in reptiles: A review. Vet Micro 2013;165:200–213. 

Kolesnikovas C.K.M., Grego K.F., Rameh de Albuquerque L.C., Jacobson E.R., Monezi T.A., Mehnert D.U., Catão-Dias J.L. Ophidian paramyxovirus in Brazilian vipers (Bothrops alternatus) Vet. Rec. 2006;159:390–392.

Kurath G, Batts WN, Ahne W, et al. Complete genome sequence of Fer-de-Lance virus reveals a novel gene in reptilian paramyxoviruses. J Virol 2004;78:2045–56.

Kurath G. Create new genus Ferlavirus (type species: Fer-de-Lance paramyxovirus), in the subfamily Paramyxovirinae, familyParamyxoviridae, order Mononegaviales. Available online: http://talk.ictvonline.org/files/proposals/taxonomy_proposals_vertebrate1/m/vert04/3859.aspx

Jacobson E.R., Gaskin J.M., Wells S., Bowler K., Schumacher J. Epizootic of ophidian paramyxovirus in a zoological collection: Pathological, microbiological, and serological findings. J. Zoo Wildl. Med. 1992;23:318–327.

Jacobson ER, Adams HP, Geisbert TW, et al. Pulmonary lesions in experimental ophidian paramyxovirus pneumonia of Aruba Island rattlesnakes, Crotalus unicolor. Vet Pathol 1997;34(5):450–9.

Jacobson ER, Origgi F, Pessier AP, et al. Paramyxovirus infection in caiman lizards (Draecena guianensis). J Vet Diagn Invest 2001;13:143–51.

Jacobson E.R. Viruses and viral diseases of reptiles. In: Jacobson E.R., editor. Infectious Diseases and Pathology of Reptiles. CRC Press, Taylor and Francis Group; Boca Raton, FL, USA: 2007. pp. 395–460.

Lloyd C., Manvell R., Drury S., Sainsbury A.W. Seroprevalence and significance of paramyxovirus titers in a zoological collection of lizards. Vet. Rec. 2005;156:578–580.

Marschang RE, Donahoe S, Manvell R, et al. Paramyxovirus and reovirus infections in wild-caught Mexican lizards (Xenosaurus and Abronia spp.). J Zoo Wildl Med 2002;33(4):317–21.

Marschang R.E., Papp T., Frost J.W. Comparison of paramyxovirus isolates from snakes, lizards and a tortoise. Virus Res. 2009;144:272–279. 

Marschang RE (2011) Viruses infecting reptiles. Viruses 3: 2087–2126. [PMC free article

Papp T., Seybold J., Marschang R.E. Paramyxovirus infection in a leopard tortoise (Geochelone pardalis babcocki) with respiratory disease. J. Herpetol. Med. Surg. 2011

Pasmans F, Blahak S, Martel A., Pantchev N.. Introducing reptiles into a captive collection: the role of the veterinarian. Vet J 2008;175:53–68. 

Ritchie B. Virology. In: Medicine and Surgery of Reptiles. Elsevier, St. Louis, 2006:391–417. 

Clark H.F., Lief F.S., Lunger P.D., Waters D., Leloup P., Foelsch D.W., Wyler R.W. Fer de Lance virus (FDLV): a probable paramyxovirus isolated from a reptile. J. Gen. Virol. 1979;44:405–418. 

Zangger N., Müller M., Pagan O. Virale Dermatitis bei der Maurischen (Testudo graeca) und der Griechischen (Testudo hermanni) Landschildkröte in der Schweiz. Proceedings of the Fourth International Colloquium on Pathology and Medicine of Reptiles and Amphibians; Bad Nauheim, Germany. 27–29 September 1991; pp. 25–29.
 
Abbas M.D., Marschang R.E., Schmidt V., Kasper A., Papp T. A unique novel reptilian paramyxovirus, four atadenovirus types and a reovirus identified in a concurrent infection of a corn snake (Pantherophis guttatus) collection in Germany. Vet. Microbiol. 2011;150:70–79.
 

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