European bat lyssaviruses - An ecological enigma

Acta Chiropterologica

Volumn 9, Issue 1, 2007, Pages 283-296

  Vos, Ad ^a   Kaipf, Ingrid ^b   Denzinger, Annette ^b   Fooks, Anthony R ^c   Johnson, Nick ^c   Müller, Thomas ^d  

^a Impfstoffwerk Dessau Tornau GmbH   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c VETERINARY LABORATORIES AGENCY   (United Kingdom)

^d FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

Author keywords

Chiroptera; EBLV 1; EBLV 2; Ecology; Rabies

Indexed keywords

BAT; HEALTH RISK; HOST; VIRUS;

CHIROPTERA; EPTESICUS SEROTINUS; EUROPEAN BAT LYSSAVIRUS 1; MYOTIS DASYCNEME; RABIES VIRUS;

EID: 34548483933     PISSN: 15081109     EISSN: None     Source Type: Journal    
DOI: 10.3161/1733-5329(2007)9[283:EBLAEE]2.0.CO;2     Document Type: Review

References (78)

1. ADAMS, D. B., and G M. BAER. 1966. Cesariary section and artificial feeding device for suckling bats. Journal of Mammalogy, 47: 524-525.
2. ALMEIDA, M. F., L. F. A. MARTORELLI, C. C. AIRES, P. C. SALLUM, E. L. DURIGON, and E. MASSAD. 2005. Experimental rabies infection in heamatophagous bats Desmodus rotundus. Epidemiology and Infection, 133: 523-527.
3. AMENGUAL, B., J. E. WHITBY, A. KING J. S. COBO, and H. BOURHY. 1997. Evolution of European bat lyssaviruses. Journal of General Virology, 78: 2319-2328.
4. ANONYMOUS. 1986. Bat rabies in the Union of Soviet Socialist Republics. Rabies Bulletin Europe, 10: 12-14.
5. ANONYMOUS. 1989. Observations on the course of a bat rabies case in the Federal Republic in Germany. Rabies Bulletin Europe, 13: 11.
6. AQUILAR-SETIEN, A., B. BROCHIER, N. TORDO, O. DE PAZ, P. DESMETTRE, D. PEHARPRE, and P. P. PASTORET. 1998. Experimental rabies infection and oral vaccination in vampire bats (Desmodus rotundus). Vaccine, 16: 1122-1126.
7. BADRANE, H., and N. TORDO. 2001. Host switching in Lyssavirus history from the Chiroptera to the Carnivora orders. Journal of Virology, 75: 8096-8104.
8. BARRAT, J., M. ARTOIS, and H. BOURHY. 1989. Two bats diagnosed rabid in France. Rabies Bulletin Europe, 13: 10-11.
9. BOTVINKIN, A. D., E. M. POLESCHUK, I. V. KUZMIN, T. I. BORISOVA, S. V. GAZARYAN, P. YAGER, and C. E. RUPPRECHT. 2003. Novel lyssavirus isolated from bats in Russia. Emerging Infectious Diseases, 9: 1623-1625.
10. BOURHY, H., B. KISSI, M. LAFON, D. SACRAMENTO, and N. TORDO. 1992. Antigenic and molecular characterization of bat rabies virus in Europe. Journal of Clinical Microbiology, 30: 2419-2426.
11. BRASS, D. A. 1994. Rabies in bats - natural history and public health implications. Livia Press, Ridgefield, 352 pp.
12. BROOKES, S. M., J. N. AEGERTER, G. C. SMITH, D. M. HEALY, T. A. JOLLIFFE, S. M. SWIFT, I. J. MACKEI, J. S. PRITCHARD, P. A. RACEY, N. P. MOORE, and A. R. FOOKS. 2005a. European bat lyssaviruses in Scottish bats. Emerging Infectious Diseases, 11: 572-578.
13. BROOKES, S. M., G. PARSONS, N. JOHNSON, L. M. MCELHINNEY, and A. R. FOOKS. 2005b. Rabies human diploid cell vaccine elicits cross-neutralising and cross-protecting immune responses against European and Australian bat lyssaviruses. Vaccine, 23: 4101-4109.
14. BROOKES, S. M., R. KLOPFLEISCH, T. MULLER, D. M. HEALEY, J. TIEFKE, E. LANGE, J. KLIEMT, N. JOHNSON, C. FINNEGAN, L. JOHNSON, V. KADEN, A. VOS, and A. R. FOOKS. 2006. Differences between EBLV-1 and EBLV-2 pathogenesis: sheep as a model of disease recovery. P. 62, in Abstracts of the XVII International Conference Rabies in the Americas, October 15-20, Brasilia, Brazil.
15. BROSSET, A. 1990. Les migrations de la pipistrelle de Nathusius, Pipistrellus nathusii, en France. Ses incidences possibles sur la propagation de la rage. Mammalia, 54: 207-212.
16. BRUIJN, Z. 2003. Behavioural observations in some rabid bats. Rabies Bulletin Europe, 27: 7-8.
17. CALISHER, C. H., J. E. CHILDS, H. E. FIELD, K. V. HOLMES, and T. SCHOUNTZ. 2006. Bats: important reservoir hosts of emerging viruses. Clinical Microbiology Reviews, 19: 531-545.
18. CHAKRAVARTY, A. K., and S. K. SARKAR. 1994. Immunofluorescence analysis of immunoglobulin bearing lymphocytes in the Indian fruit bat: Pteropus giganteus. Lymphology, 27: 97-104.
19. CONSTANTINE, D. G. 1962. Rabies transmission by nonbite route. Public Health Reports, 77: 287-289.
20. CONSTANTINE, D. G., G. C. SOLOMON, and D. F. WOODALL. 1968. Transmission experiments with bat rabies isolates: responses of certain carnivores and rodents to rabies viruses from four species of bats. American Journal of Veterinary Research, 29: 181-190.
21. DAVIS, P. L., E. C. HOLMES, F. LARROUS, W. H. VAN DER POEL, K. TJORNEHOJ, W. J. ALONSO, and H. BOURHY. 2005. Phylogeography, population dynamics, and molecular evolution of European bat lyssaviruses. Journal of Virology, 79: 10487-10497.
22. DAVIS, P. L., H. BOURHY, and E. C. HOLMES. 2006. The evolutionary history and dynamics of bat rabies. Infection, Genetics and Evolution, 6: 464-473.
23. DE BOO, M. 2002. Bomen, beesten en buitens. Staatsbosbeheer in Gelderland. Staatsbosbeheer, Arnhem, 280 pp.
24. ECHEVARRIA, J. E., A. AVELLON, J. JUSTE, M. VERA, and C. IBAÑEZ. 2001. Screening of active lyssavirus infection in wild bat populations by viral RNA on oropharyngeal swabs. Journal of Clinical Microbiology, 39: 3678-3683.
25. EVERARD, C. O., and J. D. EVERARD. 1988. Mongoose rabies. Reviews of Infectious Diseases, 10: S610-S614.
26. FOOKS, A. R., S. M. BROOKES, N. JOHNSON, L. M. MCELHINNEY, and A. M. HUTSON. 2003. European bat lyssavirus: an emerging zoonoses. Epidemiology and Infection, 131: 1029-1039.
27. GAEDE, T. 1992. Bat rabies in Denmark 1985-1990. Pp. 76-78, in Wildlife rabies control (K. BÖGEL, F. X. MESLIN, and M. KAPLAN, eds.). Wells Medical Ltd., Kent, 222 pp.
28. GIBBONS, R. V. 2002. Cryptogenic rabies, bats, and the question of aerosol transmission. Annals of Emergency Medicine 39: 528-536.
29. GRAUBALLE, P. C., H. J. BAAGØE, M. FEKADU, J. M. WESTERGAARD, and H. ZOFFMANN. 1987. Bat rabies in Denmark. Lancet, 1: 379-380.
30. HARRIS, S. L., S. M. BROOKES, G. JONES, A. M. HUTSON, P. A. RACEY, J. AEGERTER, G. C. SMITH, L. M. MCELHINNEY, and A. R. FOOKS. 2006a. European bat lyssaviruses: distribution, prevalence and implications for conservation. Biological Conservation, 131: 193-210.
31. HARRIS S. L., S. M. BROOKES, G. JONES, A. M. HUTSON, and A. R. FOOKS. 2006b. Passive surveillance (1987 to 2004) of United Kingdom bats for European bat lyssaviruses. Veterinary Record, 159: 439-446.
32. HUGHES, G. J., L. A. ORCIARI, and C. E. RUPPRECHT. 2005. Evolutionary timescale of rabies virus adaptation to North America bats inferred from the substitution rate of the nucleoprotein gene. Journal of General Virology, 86: 1467-1474.
33. HUGHES, G. J., I. V. KUZMIN, A. SCHMITZ, J. BLANTON, J. MANANGAN, S. MURPHY, and C. E. RUPPRECHT. 2006. Experimental infection of big brown bats (Eptesicus fuscus) with Eurasian bat lyssaviruses Aravan, Khujand, and Irkut virus. Archives of Virology, 151: 2021-2035.
34. HUTTERER, R., T. IVANOVA, C. MEYER-CORDS, and L. RODRIQUEZ. 2005. Bat migration in Europe - a review of banding data and literature. Bundesamt fuer Naturschutz, Bonn - Bad Godesberg, 162 pp.
35. JOHNSON, N., D. SELDEN, G. PARSONS, D. HEALY, S. M. BROOKES, L. M. MCELHINNEY, A. M. HUTSON, and A. R. FOOKS. 2003. Isolation of a European bat lyssavirus type 2 from a Daubenton's bat in the United Kingdom. Veterinary Record, 152: 383-387.
36. JOHNSON, N., P. R. WAKELEY, S. M.BROOKES, and A. R. FOOKS. 2006. European bat lyssavirus Type 2 RNA in Myotis daubentonii. Emerging Infectious Diseases, 12: 1142-1144.
37. KAPPELER, A. 1989. Bat rabies surveillance in Europe. Rabies Bulletin Europe, 13: 12-13.
38. KAPPELER, A. 1992. First case of rabies in a bat in Switzerland. Rabies Bulletin Europe, 16: 11.
39. KAPTEYN, K. 1995. Vleermuizen in het landschap; over hun ecologie, gedrag en verspreiding. Schuyt and Co., Haarlem, 224 pp.
40. KAPTEYN, K. 1997. Laatvlieger Eptesicus serotinus (Schreber, 1774). Pp. 191-201, in Atlas van de Nederlandse vleermuizen: onderzoek naar verspreiding en ecologie (H. LIMPENS, K. MOSTERT, and W. BONGERS, eds.). KNNV Uitgeverij, Utrecht, 260 pp.
41. KING, A. A., J. HAAGSMA, and A. KAPPELER. 2004, Lyssavirus infections in European bats. Pp. 221-242, in Historical perspective of rabies in Europe and the Mediterranean Basin (A. A. KING, A. R. FOOKS, M. AUBERT, and A. I. WANDELER, eds.). Office Internationale des Epizootics, Paris, 361 pp.
42. KUIKEN, T., E. C. HOLMES, J. MCCAULEY, G. F. RIMMELZWAAN, C. S. WILLIAMS, and B. T. GRENFELL. 2006. Host species barriers to influenza virus infections. Science, 312: 394-397.
43. KUNZ, T. H., and M. B. FENTON (eds.). 2003. Bat ecology. University of Chicago Press, Chicago, 798 pp.
44. KUZMIN, I. V., and A. D. BOTVINKIN. 1996. The behaviour of bats Pipistrellus pipistrellus after experimental inoculation with rabies and rabies-like viruses and some aspects of pathogenesis. Myotis, 34: 93-99.
45. KUZNIN, I. V., L. A. ORCIARI, Y. T ARAI, J. S. SMITH, C. A. HANLON, Y. KAMEOKA, and C. E. RUPPRECHT. 2003. Bat lyssaviruses (Aravan and Khujand) from Central Asia: phylogenetic relationships according to N, P and G gene sequences. Virus Research, 97: 65-79.
46. KUZMIN, I. V., A. D. BOTVINKIN, E. M. POLESCHUK, L. A. ORCIAI, and C. E. RUPPRECHT. 2006. Bat rabies surveillance in the former Soviet Union. Developments in Biologicals, 125: 273-282.
47. MACDONALD, D. W. 1980. Rabies and wildlife: a biologist's perspective. Oxford University Press, Oxford, 151 pp.
48. MARSTON, D. A., L. M. MCELHINEY, N. JOHNSON, T. MÜLLER, K. K. CONZELMANN, N. TORDO, and A. R. FOOKS. 2007. Comparative analysis of the full genome sequence for European bat lyssavirus type-1 and type-2 with other lyssaviruses and evidence for a conserved transcription termination and polyadenylation motif in the G-L 3′-non-translated region. Journal of General Virology, 88: 1302-1314.
49. MCCOLL, K. A., N. TORDO, and A. A. AGUILAR-SETIEN. 2000. Bat lyssavirus infections. Revue Scientifique et Technique, 19: 177-196.
50. MOLLGAARD, S. 1985. Bat-rabies in Denmark. Rabies Bulletin Europe, 9: 8.
51. MÜLLER, T. H., J. H. COX, W. MÜLLER, and H. SCHLÜTER. 2001. Bat rabies in Germany with emphasis on molecular comparison of EBL isolates. P. 31, in Abstracts of the 12th International Meeting on Advances in Rabies Research and Control in the Americas, November 12-16, 2001, Peterborough, Ontario, Canada.
52. MÜLLER, T., N. JOHNSON, C. M. FREULING A. R. FOOKS, T. SELHORST, and A. VOS. 2007, Epidemiology of bat rabies in Germany. Archives of Virology, 152: 273-288.
53. MÜLLER, W. W. 1992. Recent bat rabies epizootic in Europe - a review. Pp. 65-69, in Wildlife rabies control (K. BÖGEL, F. X. MESLIN, and M. KAPLAN, eds.). Wells Medical Ltd., Kent, 222 pp.
54. PAUL, B., and A. K. CHAKRAVARTY. 1986. In vitro analysis of delayed immune response in a bat, Pteropus giganteus: process of con-A mediated activation. Developmental Comparative Immunology, 10: 55-67.
55. PEREZ-JORDA, J. L., C. IBAÑEZ, M. MUNOZ-CERVERA, and A. TELLEZ. 1995. Lyssavirus in Eptesicus serotinus (Chiroptera, Vespertilionidae). Journal of Wildlife Diseases 31: 372-377.
56. PETIT, E., and F. MAYER. 2000. A population genetic analysis of migration: the case of the noctule bat (Nyctalus noctula). Molecular Ecology, 9: 683-690.
57. PICARD-MEYER, E., J. BARRAT, E. TISSOT, A. VERDOT, C. PATRON, M. J. BARRAT, and F. CLIQUET. 2006. Bat rabies surveillance in France, from 1989 through May 2005. Development in Biologicals, 125: 283-288.
58. ROSATTE, R. C., and J. R. GUNSON. 1984. Presence of neutralizing antibodies to rabies virus in striped skunks from areas free of skunk rabies in Alberta. Journal of Wildlife Diseases, 20: 171-176.
59. SCHINDLER, R., and H. K. DENNING. 1958. Untersuchungen über die Bedeutung der Fledermäuse für den gegenwärtigen Tollwut-Seuchenzug in Deutschland. Monatsschrift für Tierheilkunde, 10: 169-177.
60. SCHNEIDER, L. G., and J. H. COX. 1994. Bat lyssaviruses in Europe. Current Topics in Microbiology and Immunology, 187: 207-218.
61. SEIDLER, M., H.-J. BREHMER, B. POTT B, J. H. COX, and H. ZINKE. 1987. Tollwut bei Fledermäusen in Niedersachsen. Berliner und Münchener Tierärztliche Wochenschrift, 100: 199-203.
62. SERRA-COBO J., B. AMENGUAL, C. ABELLÁN, and H. BOURHY. 2002. European bat lyssavirus infection in Spanish bat populations. Emerging Infectious Diseases, 8: 413-420.
63. SHANKAR, V., R. A. BOWEN, A. D. DAVIS, C. E. RUPPRECHT, and T. J. O'SHEA. 2004. Rabies in a colony of big brown bats (Eptesicus fuscus). Journal of Wildlife Diseases, 40: 403-413.
64. SHANKAR, V., L. A. ORCIARI, C. D. MATTOS, I. V. KUZMIN, W. J. PAPE, T. J. O'SHEA, and C. E. RUPPRECHT. 2005. Genetic divergence of rabies viruses from bat species of Colorado, USA. Vector-Borne Zoonotic Diseases, 5: 330-341.
65. SIMMS, R. A., R. ALLEN, and S. E. SULKIN. 1963. Studies of the pathogenesis of rabies in insectivorous bats III influence of the gravid state. Journal of Infectious Diseases, 112: 17-27.
66. SMITH, G. C., S. M. BROOKES, S. L. HARRIS, J. N. AEGERTER, G. JONES, and A. R. FOOKS. 2006. EBLV-2 prevalence in the United Kingdom as determined by surveillance testing. Developments in Biologicals, 125: 265-171.
67. SMITH, J. S., L. A. ORCIARI, and P. A. YAGER. 1995. Molecular epidemiology of rabies in the United States. Virology, 6: 387-400.
68. STEECE, R. S., and C. H. CALISHER. 1989. Evidence for prenatal transfer of rabies virus in the Mexican free-tailed bat ( Tadarida brasiliensis mexicana). Journal of Wildlife Diseases, 25: 329-334.
69. VAN DER POEL W. H. M., R. VAN DER HEIDE, G. VAN AMERONGEN, L. J. M. VAN KEULEN, G. J. WELLENBERG, H. BOURHY, W. SCHAFTENAAR, J. GROEN, and A. D. M. E. OSTERHAUS. 2000. Characterisation of a recently isolated lyssavirus in frugivorous zoo bats. Archives of Virology, 145: 1919-1931.
70. VAN DER POEL, W. H. M., R. VAN DER HEIDE, E. R. A. M. VERSTATEN, K. TAKUMI, P. H. C. LINA, and J. A. KRAMPS. 2005. European bat lyssaviruses, the Netherlands. Emerging Infectious Diseases, 11: 1854-1859.
71. VAN DER POEL, W. H. M., P. H. C. LINA, and J. A. KRAMPS. 2006. Public health awareness of emerging zoonotic viruses of bats: a European perspective. Vector-Borne and Zoonotic Diseases, 6: 315-324.
72. VAZQUEZ, S., C. IBAÑEZ, J. JUSTE, and J. E. ECHEVARRIA. 2006. EBLV1 circulation in natural bat colonies of Eptesicus serotinus: a six year survey. Developments in Biologicals, 125: 257-261.
73. VOS, A., T. MÜLLER, L. NEUBERT, A. ZURBRIGGEN, C. BOTTERON, D. PÖHLE, H. SCHOON, L. HAAS, and A. JACKSON. 2004a. Rabies in red foxes (Vulpes vulpes) experimentally infected with European bat lyssavirus Type 1 (EBLV-1). Journal of Veterinary Medicine, 51B: 327-332.
74. VOS, A., T. MÜLLER, J. COX, L. NEUBERT, and A. R. FOOKS. 2004b. Susceptibility of ferrets (Mustela putorius furo) to experimentally induced rabies with European bat lyssaviruses (EBLV). Journal of Veterinary Medicine, 51B: 55-60.
75. VOS, A., N. JOHNSON, T. MÜLLER, L. NEUBERT, R. FRANKA, I. KAIPF, K. MANSFELD, C. FREULING, A. DENZINGER, C. E. RUPPRECHT, and A. R. FOOKS. 2006. Experimental infection of Eptesicus fuscus with European bat lyssavirus Type 1. P. 61, in Abstracts of the XVII International Conference Rabies in the Americas, October 15-20, Brasilia, Brazil.
76. VERENIGING VOOR ZOOGDIERKUNDE EN ZOOGDIER-BESCHERMING. 2006. Jaarboek 2005. Vereniging voor Zoogdierkunde en Zoogdierbescherming, Arnhem, 66 pp.
77. WANDELER, A. I., S. A. NADIN-DAVIS, R. R. TINLINE, and C. E. RUPPRECHT. 1994. Rabies epidemiology: some ecological and evolutionary perspectives. Pp. 297-324, in Lyssaviruses (B. DIETZSCHOLD, H. KOPROWSKI, and C. E. RUPPRECHT, eds.). Springer Verlag, Berlin, 350 pp.
78. WHITBY, J. E., P. R. HEATON, E. M. BLACK, M. WOOLDRIDGE, L. M. MCELHINNEY, and P. JOHNSTONE. 2000. First isolation of a rabies-related virus from a Daubenton's bat in the United Kingdom. Veterinary Record, 147: 385-388.