Paramyxoviruses in reptiles: A review

Veterinary Microbiology

Volumn 165, Issue 3-4, 2013, Pages 200-213

  Hyndman, Timothy H ^a   Shilton, Cathy M ^b   Marschang, Rachel E ^c  

^a MURDOCH UNIVERSITY   (Australia)

^b Berrimah Veterinary Laboratories   (Australia)

^c UNIVERSITY OF HOHENHEIM   (Germany)

Author keywords

Ferlavirus; Paramyxovirus; Reptile; Snake; Sunshine virus; Virus

Indexed keywords

SIALIDASE;

ANOREXIA; ANTIBODY TITER; AVULAVIRUS; CROCODILE; CROSS REACTION; DYSPNEA; EPIDEMIC; FERLAVIRAL INFECTION; FERLAVIRUS; FLACCID PARALYSIS; HEMAGGLUTINATION; HEMAGGLUTINATION INHIBITION TEST; HISTOPATHOLOGY; IGUANA; IMMUNOASSAY; IMMUNOHISTOCHEMISTRY; INCUBATION TIME; INFECTION CONTROL; LIZARD; LUNG CONGESTION; LUNG INFECTION; NONHUMAN; OPISTHOTONUS; PALLIATIVE THERAPY; PARAINFLUENZA VIRUS 2; PARAMYXOVIRUS; PARAMYXOVIRUS INFECTION; PHYLOGENY; PNEUMOVIRINAE; POLYMERASE CHAIN REACTION; REPTILE; REVIEW; SNAKE; SUNSHINE VIRUS; TAXONOMY; TRANSMISSION ELECTRON MICROSCOPY; VACCINATION; VERTICAL TRANSMISSION; VIRUS ISOLATION; VIRUS NUCLEOCAPSID; VIRUS TRANSMISSION; ZOONOSIS;

PARAMYXOVIRIDAE; PYTHONIDAE; REPTILIA; REPTILIAN PARAMYXOVIRUS; SERPENTES;

ANIMALS; AUSTRALIA; PARAMYXOVIRIDAE; PARAMYXOVIRIDAE INFECTIONS; PHYLOGENY; REPTILES;

EID: 84893012403     PISSN: 03781135     EISSN: 18732542     Source Type: Journal    
DOI: 10.1016/j.vetmic.2013.04.002     Document Type: Review

References (80)

1. 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.
2. Ahne W., Adrian J., Mayr A. Replication of reptilian paramyxovirus in avian host systems. J. Vet. Med. B 1999, 46:57-62.
3. Ahne W., Batts W.N., Kurath G., Winton J.R. Comparative sequence analyses of sixteen reptilian paramyxoviruses. Virus Res. 1999, 63:65-74.
4. Ahne W., Mayr A. Reptilian paramyxoviruses induce cytokine production in human leukocytes. Comp. Immunol. Microbiol. Infect. Dis. 2000, 23:9-13.
5. Ahne W., Neubert W. Isolation of paramyxovirus-like agents from teju (Callopsites maculatus) and python (Python regius). Proceedings of the 2nd International Symposium of Viruses in Lower Vertebrates, Oregan State University, OR 1991, 203-210.
6. Ahne W., Neubert W.J., Thomson I. Reptilian viruses: isolation of myxovirus-like particles from the snake Elaphe oxycephala. Zentralbl. Veterinarmed. B 1987, 34:607-612.
7. Allender M.C., Mitchell M.A., Dreslik M.J., Phillips C.A., Beasley V.R. Measuring agreement and discord among hemagglutination inhibition assays against different ophidian paramyxovirus strains in the Eastern massasauga (Sistrurus catenatus catenatus). J. Zoo Wildlife Med. 2008, 39:358-361.
8. Allender M.C., Mitchell M.A., Phillips C.A., Grusznski K., Beasley V.R. Hematology, plasma biochemistry, and antibodies to select viruses in wild-caught eastern massasauga rattlesnakes (Sistrurus catenatus catenatus) from Illinois. J. Wildlife Dis. 2006, 42:107-114.
9. Alymova I.V., Taylor G., Portner A. Neuraminidase inhibitors as antiviral agents. Curr. Drug Targets Infect. Dis. 2005, 5:401-409.
10. Ariel E. Viruses in reptiles. Vet. Res. 2011, 42:100.
11. Blahak S. Untersuchungen zum Vorkommen von Paramyxoviren bei Schlangen und Charakterisierung ausgewählter Isolate. Justus-Liebig-Universität Giessen 1994.
12. Blahak S. Isolation and characterisation of paramyxoviruses from snakes and their relationship to Avian Paramyxoviruses. Zentralbl Veterinarmed B 1995, 42:216-224.
13. Blahak S., Göbel T., Alexander D.J., Manvell R. Some investigations of the occurrence of paramyxoviruses in snakes in German zoos. Proceedings of the 4th International Colloquium on Pathology and Medicine of Reptiles and Amphibians, Bad Nauheim 1991, 17-24.
14. Boyer T.H., Garner M.M., Latimer K.S. Paramyxovirus infection in a Thai Water Dragon (Physignathus concinus). Proceedings of the 12th Annual Meeting of the Association of Reptilian and Amphibian Veterinarians 2005, 93-95.
15. Bronson E., Cranfield M.R. Paramyxovirus. Reptile Medicine and Surgery 2006, 858-861.
16. Brousset D., Lewy C., Yarto E. Detection of antibodies against paramyxovirus (OPMV) on Mexican captive snakes. Proceedings of the Association of Reptilian and Amphibian Veterinarians 1994, 101.
17. Calle P.P., Rivas J., Munoz M., Thorbjarnarson J., Holmstrom W., Karesh W.B. Infectious disease serologic survey in free-ranging Venezuelan Anacondas (Eunectes murinus). J. Zoo Wildlife Med. 2001, 32:320-323.
18. Chakrabarti S., Collingham K.E., Holder K., Fegan C.D., Osman H., Milligan D.W. Pre-emptive oral ribavirin therapy of paramyxovirus infections after haematopoietic stem cell transplantation: a pilot study. Bone Marrow Transplant. 2001, 28:759-763.
19. 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.
20. Folsch D.W., Leloup P. Fatal endemic infection in a serpentarium, diagnosis, treatment and preventive measures. Tierarztl. Prax. 1976, 4:527-536.
21. Franke J., Batts W.N., Ahne W., Kurath G., Winton J.R. Sequence motifs and prokaryotic expression of the reptilian paramyxovirus fusion protein. Arch. Virol. 2006, 151:449-464.
22. Franke J., Essbauer S., Ahne W., Blahak S. Identification and molecular characterisation of 18 paramyxoviruses isolated from snakes. Virus Res. 2001, 80:67-74.
23. Freeman A.F., Jacobsohn D.A., Shulman S.T., Bellini W.J., Jaggi P., de Leon G., Keating G.F., Kim F., Pachman L.M., Kletzel M., Duerst R.E. A new complication of stem cell transplantation: measles inclusion body encephalitis. Pediatrics 2004, 114:657-660.
24. Gillespie D.S. Large Collections: Special Considerations. Reptile Medicine and Surgery 2006, 1013-1016. Elsevier, St. Louis.
25. Gravendyck M., Ammermann P., Marschang R.E., Kaleta E.F. Paramyxoviral and reoviral infections of iguanas on Honduran Islands. J. Wildlife Dis. 1998, 34:33-38.
26. Heard D., Harr K., Wellehan J. Diagnostic Sampling and Laboratory Tests. BSAVA Manual of Reptiles 2004, 71-86. British Small Animal Veterinary Association, Gloucester.
27. Hernandez-Divers S.J. Appendix A reptile viral diseases - summary table. Reptile Medicine and Surgery 2006, 1147-1158.
28. Homer B.L., Sundberg J.P., Gaskin J.M., Schumacher J., Jacobson E.R. Immunoperoxidase detection of ophidian paramyxovirus in snake lung using a polyclonal antibody. J. Vet. Diagn. Invest. 1995, 7:72-77.
29. Huchzermeyer F., Gerdes G., Putterill J. Viruses and mycoplasms from faeces of farmed Nile crocodiles. Proceedings of the 12th Working Meeting of the Crocodile Specialist Group 1994, 303-308.
30. Hyndman T.H., Marschang R.E., Wellehan J.F., Nicholls P.K. Isolation and molecular identification of Sunshine virus, a novel paramyxovirus found in Australian snakes. Infect. Genet. Evol. 2012, 12:1436-1446.
31. Hyndman T.H., Shilton C.M., Doneley R.J.T., Nicholls P.K. Sunshine virus in Australian pythons. Vet. Microbiol. 2012, 161:77-87.
32. ICTV, 2013. Virus Taxonomy: 2011 Release (International Committee on Taxonomy of Viruses).
33. Jackson O.F., Needham J.R. Rhinitis and virus antibody titres in Chelonians. J. Small Animal Pract. 1983, 24:31-36.
34. Jacobson E., Gaskin J.M., Page D., Iverson W.O., Johnson J.W. Illness associated with paramyxo-like virus infection in a zoologic collection of snakes. J. Am. Vet. Med. Assoc. 1981, 179:1227-1230.
35. Jacobson E.R. Viruses and viral diseases of reptiles. In: Infectious Diseases and Pathology of Reptiles 2007, 395-460.
36. Jacobson E.R., Adams H.P., Geisbert T.W., Tucker S.J., Hall B.J., Homer B.L. Pulmonary lesions in experimental ophidian paramyxovirus pneumonia of Aruba Island Rattlesnakes, Crotalus unicolor. Vet. Pathol. 1997, 34:450-459.
37. Jacobson E.R., Flanagan J.P., Rideout B.R., Ramsay E.C., Morris P. Ophidian paramyxovirus - roundtable forum. J. Herpetol. Med. Surg. 1999, 9:15-22.
38. Jacobson E.R., Gaskin J.M., Flanagan J.P., Odum R.A. Antibody responses of Western Diamondback rattlesnakes (Crotalus atrox) to inactivated ophidian paramyxovirus vaccines. J. Zoo Wildlife Med. 1991, 22:184-190.
39. Jacobson E.R., Gaskin J.M., Simpson C.F., Terrell T.G. Paramyxo-like virus infection in a rock rattlesnake. J. Am. Vet. Med. Assoc. 1980, 177:796-799.
40. 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 Wildlife Med. 1992, 23:318-327.
41. Jacobson E.R., Origgi F., Pessier A.P., Lamirande E.W., Walker I., Whitaker B., Stalis I.H., Nordhausen R., Owens J.W., Nichols D.K., Heard D., Homer B. Paramyxovirus infection in Caiman Lizards (Draecena guianensis). J. Vet. Diagn. Invest. 2001, 13:143-151.
42. Jacobson E.R., Origgi F.C. Serodiagnostics. Infectious Diseases and Pathology of Reptiles 2007, 381-394.
43. Jacobson E.R., Samuelson D.A. Identifying reptile pathogens using electron microscopy. Infectious Diseases and Pathology of Reptiles 2007, 299-350.
44. Junqueira de Azevedo I., Prieto da Silva d.L.M., Carmona A.R.B., Lee Ho E.P. Characterisation of a paramyxovirus from a Fer de Lance Viper (Bothrops jararaca): partial nucleotide sequence of the Putative Fusion Protein. Arch. Virol. 2001, 146:51-57.
45. Kania S.A., Kennedy M., Nowlin N., Diderrich V., Ramsay E. Development of an enzyme linked immunosorbent assay for the diagnosis of ophidian paramyxovirus. Proceedings of the European Association of Zoo and Wildlife Veterinarians 2000, 71-73.
46. Keeble E. Neurology. BSAVA Manual of Reptiles 2004, 273-288. British Small Animal Veterinary Association, Gloucester.
47. Kik M.J.L., Van Zon R.T., Van Asten F.J.A.M. Retrospective Studies on Ophidian Paramyxovirus Infection in Snakes in the Netherlands Using the Polymerase Chain Reaction (PCR). Preliminary Results. Proceedings of the 7th International Symposium on Pathology and Medicine in Reptiles and Amphibians 2004, 43-48.
48. Kindermann J., Kubber-Heiss A., Kerschbaumer P., Nowotny N. Phylogenetic analysis of the L and HN gene of ophidian paramyxoviruses. Arch. Virol. 2001, 146:1021-1035.
49. Kolesnikovas C.K.M., Grego K.F., Rameh de Albuquerque L.C., Jacobson E.R., Monezi T.A., Mehnert D.U., Catao-Dias J.L. Ophidian paramyxovirus in Brazilian vipers (Bothrops alternatus). Vet. Record 2006, 159:390-392.
50. Kummrow M., Lopez J., Hatt J., Dorrestein G.M. Disease-risk Assessment for Free-ranging Geckoes (Gecko monarchus, Gehyra mutilata) in a Captive Reptile Stock. Proceedings of the AAZV, AAWV, WDA Joint Conference 2004, 591.
51. Kurath G. Reptile paramyxoviruses: 1 new species and new genus. Ferlavirus 2009.
52. Kurath G., Batts W.N., Ahne W., Winton J.R. Complete genome sequence of Fer-de-Lance Virus reveals a novel gene in reptilian paramyxoviruses. J. Virol. 2004, 78:2045-2056.
53. Lloyd C., Manvell R., Drury S., Sainsbury A.W. Seroprevalence and significance of paramyxovirus titres in a zoological collection of lizards. Vet. Record 2005, 156:578-580.
54. Lloyd M.L., Flanagan J. Recent developments in ophidian paramyxovirus research and recommendations on control. In: Proceedings of the American Association of Zoo Veterinarians 1991, 148-153.
55. Lunger P.D., Clark H.F. Reptilia-related viruses. Adv. Virus Res. 1978, 23:159-204.
56. Manvell R.J., Drury S.E., Geach M., Lewis J.C.M. Isolation of Ophidian Paramyxovirus type 7 from a Reticulated Python in the UK. Vet. Record 2000, 147:696.
57. Marschang R.E. Viruses infecting reptiles. Viruses 2011, 3:2087-2126.
58. Marschang R.E., Chitty J. Infectious Diseases. BSAVA Manual of Reptiles 2004, 330-345.
59. Marschang R.E., Donahoe S., Manvell R., Lemos-Espinal J. Paramyxovirus and reovirus infections in wild-caught Mexican Lizards (Xenosaurus and Abronia sp.). J. Zoo Wildlife Med. 2002, 33:317-321.
60. Marschang R.E., Papp T., Frost J.W. Comparison of paramyxovirus isolates from snakes, lizards and a tortoise. Virus Res. 2009, 144:272-279.
61. Mayr A., Franke J., Ahne W. Adaptation of reptilian paramyxovirus to mammalian cells (Vero Cells). J. Vet. Med. B 2000, 47:95-98.
62. Nogueira M.F., Barrella T.H., Da Silva R.J., Lopes C.A.M., Araujo Junior J.P. Isolation of an Ophidian Paramyxovirus (OPMV) in a Captive Rattlesnake (Crotalus durissus terrificus) from Botucatu, Sao Paulo State, Brazil. J. Venom. Anim. Toxins 2002, 8:168-173.
63. Oettle E., Steytler Y., Williams M. High mortality in a tortoise colony. South African J. Wildlife Res. 1990, 20:21-25.
64. Oros J., Sicilia J., Torrent A., Castro P., Deniz S., Arencibia A., Jacobson E.R., Homer B.L. Immunohistochemical detection of ophidian paramyxovirus in snakes in the Canary Islands. Vet. Record 2001, 149:21-23.
65. Papp T., Pees M., Schmidt V., Marschang R.E. RT-PCR diagnosis followed by sequence characterization of paramyxoviruses in clinical samples from snakes reveals concurrent infections within populations and/or individuals. Vet. Microbiol. 2010, 144:466-472.
66. Papp T., Seybold J., Marschang R.E. Paramyxovirus infection in a leopard tortoise (Geochelone pardalis babcocki) with respiratory disease. J. Herpetol. Med. Surg. 2010, 20:64-68.
67. 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.
68. Potgieter L.N.D., Sigler R.E., Russell R.G. Pneumonia in Ottoman Vipers (Vipera xanthena xanthena) Associated with a Parainfluenza 2-like Virus. J. Wildlife Dis. 1987, 23:355-360.
69. Quinn P.J., Markey B.K., Carter M.E., Donnelly W.J., Leonard F.C. Paramyxoviridae. Veterinary Microbiology and Microbial Disease 2002, 381-389. Blackwell Science Ltd, Oxford.
70. Richter G.A., Homer B.L., Moyer S.A., Williams D.S., Scherba G., Tucker S.J., Hall B.J., Pederson J.C., Jacobson E.R. Characterisation of paramyxoviruses isolated from three snakes. Virus Res. 1996, 43:77-83.
71. Ritchie B. Virology. Medicine and Surgery of Reptiles 2006, 391-417. Elsevier, St. Louis.
72. Rösler, R., Abbas, M.D., Papp, T., Marschang, R.E., 2013, Detection of antibodies against paramyxoviruses in tortoises. Journal of Zoo and Wildlife Medicine In press.
73. Rossi J.V. General Husbandry and Management. Reptile Medicine and Surgery 2006, 25-41. Elsevier, St. Louis.
74. Sand M.A., Latimer K.S., Gregory C.R., Rakich P.M., Jacobson E.R., Pennick K.E. Molecular diagnosis of paramyxovirus infection in snakes using reverse transcriptase-polymerase chain reaction and complementary deoxyribonucleic acid: ribonucleic acid in situ hybridisation. J. Vet. Diagn. Invest. 2004, 16:442-448.
75. Watanabe M., Mishin V.P., Brown S.A., Russell C.J., Boyd K., Babu Y.S., Taylor G., Xiong X., Yan X., Portner A., Alymova I.V. Effect of hemagglutinin-neuraminidase inhibitors BCX 2798 and BCX 2855 on growth and pathogenicity of Sendai/human parainfluenza type 3 chimera virus in mice. Antimicrob. Agents Chem. 2009, 53:3942-3951.
76. Wellehan J.F., Johnson A.J. Reptile virology. The Veterinary Clinics of North America. Exotic Anim. Pract. 2005, 8:27.
77. West G., Garner M., Raymond J., Latimer K.S., Nordhausen R. Meningoencephalitis in a Boelen's Python (Morelia boeleni) associated with Paramyxovirus infection. J. Zoo Wildlife Med. 2001, 32:360-365.
78. Witte, A., 1993. Ein Beitrag zum Nachweis von Antikörpern gegen Herpes- und Paramyxoviren bei verschiedenen Landschildkrötenarten. Dissertation. Justus-Liebig-Universität Gießen.
79. Yolken R.H., Torsch V.M., Berg R., Murphy B.R., Lee Y.C. Fluorometric assay for measurement of viral neuraminidase-application to the rapid detection of influenza virus in nasal wash specimens. J. Infect. Dis. 1980, 142:516-523.
80. Zangger N., Muller M., Pagan O. Viral dermatitis in the Spur-Tailed (Testudo graeca) and the Spur-Thighed Tortoise (Testudo hermanni) in Switzerland. Proceedings of the 4th International Colloquium on Pathology Medicine of Reptiles and Amphibians 1991, 25-29.