1887

Abstract

The serotine bat () accounts for the vast majority of bat rabies cases in Europe and is considered the main reservoir for European bat lyssavirus type 1 (EBLV-1, genotype 5). However, so far the disease has not been investigated in its native host under experimental conditions. To assess viral virulence, dissemination and probable means of transmission, captive bats were infected experimentally with an EBLV-1a virus isolated from a naturally infected conspecific from Germany. Twenty-nine wild caught bats were divided into five groups and inoculated by intracranial (i.c.), intramuscular (i.m.) or subcutaneous (s.c.) injection or by intranasal (i.n.) inoculation to mimic the various potential routes of infection. One group of bats was maintained as uninfected controls. Mortality was highest in the i.c.-infected animals, followed by the s.c. and i.m. groups. Incubation periods varied from 7 to 26 days depending on the route of infection. Rabies did not develop in the i.n. group or in the negative-control group. None of the infected bats seroconverted. Viral antigen was detected in more than 50 % of the taste buds of an i.c.-infected animal. Shedding of viable virus was measured by virus isolation in cell culture for one bat from the s.c. group at 13 and 14 days post-inoculation, i.e. 7 days before death. In conclusion, it is postulated that s.c. inoculation, in nature caused by bites, may be an efficient way of transmitting EBLV-1 among free-living serotine bats.

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2009-10-01
2019-11-12
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References

  1. Amengual, B., Whitby, J. E., King, A., Cobo, J. S. & Bourhy, H. ( 1997; ). Evolution of European bat lyssaviruses. J Gen Virol 78, 2319–2328.
    [Google Scholar]
  2. Amengual, B., Bourhy, H., López-Roig, M. & Serra-Cobo, J. ( 2007; ). Temporal dynamics of European bat lyssavirus type 1 and survival of Myotis myotis bats in natural colonies. PLoS One 2, e566 [CrossRef]
    [Google Scholar]
  3. Baer, G. M. & Bales, G. L. ( 1967; ). Experimental rabies infection in Mexican freetail bat. J Infect Dis 117, 82–90.[CrossRef]
    [Google Scholar]
  4. Baltazar, R. S., Blancou, J. & Artois, M. ( 1988; ). Study of rabies virus isolated from an European bat Eptesicus serotinus – virulence for sheep and fox. Revue Med Vet (Toulouse) 139, 615–621.
    [Google Scholar]
  5. Botvinkin, A. D., Kuzmin, I. & Chernov, S. M. ( 1992; ). Experimental infection of bats with lyssaviruses serotype-1 and serotype-4. Vopr Virusol 37, 215–218.
    [Google Scholar]
  6. Botvinkin, A. D., Selnikova, O. P., Antonova, L. A., Moiseeva, A. B. & Nesterenko, E. Y. ( 2005; ). Human rabies case caused from a bat bite in Ukraine. Rabies Bulletin Europe 29, 5–7.
    [Google Scholar]
  7. Bourhy, H., Kissi, B., Lafon, M., Sacramento, D. & Tordo, N. ( 1992; ). Antigenic and molecular characterization of bat rabies virus in Europe. J Clin Microbiol 30, 2419–2426.
    [Google Scholar]
  8. Brookes, S. M., Klopfleisch, R., Müller, T., Healy, D. M., Teifke, J. P., Lange, E., Kliemt, J., Johnson, N., Johnson, L. & other authors ( 2007; ). Susceptibility of sheep to European bat lyssavirus type-1 and -2 infection: a clinical pathogenesis study. Vet Microbiol 125, 210–223.[CrossRef]
    [Google Scholar]
  9. Cox, J. H. & Schneider, L. G. ( 1976; ). Prophylactic immunization of humans against rabies by intradermal inoculation of human diploid cell culture vaccine. J Clin Microbiol 3, 96–101.
    [Google Scholar]
  10. Dacheux, L., Larrous, F., Mailles, A., Boisseleau, D., Delmas, O., Biron, C., Bouchier, C., Capek, I., Muller, M. & other authors ( 2009; ). European bat lyssavirus transmission among cats, Europe. Emerg Infect Dis 15, 280–284.[CrossRef]
    [Google Scholar]
  11. Davis, P. L., Holmes, E. C., Larrous, F., van der Poel, W. H., Tjornehoj, K., Alonso, W. & Bourhy, H. ( 2005; ). Phylogeography, population dynamics, and molecular evolution of European bat lyssaviruses. J Virol 79, 10487–10497.[CrossRef]
    [Google Scholar]
  12. Dean, D. J., Abelseth, M. K. & Athanasiu, P. ( 1996; ). The fluorescence antibody test. In Laboratory Techniques in Rabies, 4th edn, pp. 88–93. Edited by F.-X. Meslin, M. M. Kaplan & H. Koprowski. Geneva, Switzerland: World Health Organization.
  13. Echevarría, J. E., Avellón, A., Juste, J., Vera, M. & Ibáñez, C. ( 2001; ). Screening of active lyssavirus infection in wild bat populations by viral RNA detection on oropharyngeal swabs. J Clin Microbiol 39, 3678–3683.[CrossRef]
    [Google Scholar]
  14. Fekadu, M., Shaddock, J. H., Chandler, F. W. & Sanderlin, D. W. ( 1988; ). Pathogenesis of rabies virus from a Danish bat (Eptesicus serotinus): neuronal changes suggestive of spongiosis. Arch Virol 99, 187–203.[CrossRef]
    [Google Scholar]
  15. Fooks, A. R., Brookes, S. M., Johnson, N., McElhinney, L. M. & Hutson, A. M. ( 2003; ). European bat lyssaviruses: an emerging zoonosis. Epidemiol Infect 131, 1029–1039.[CrossRef]
    [Google Scholar]
  16. Fooks, A. R., Johnson, N., Müller, T., Vos, A., Mansfield, K., Hicks, D., Nuñez, A., Freuling, C., Neubert, A. & other authors ( 2009; ). Detection of high levels of European bat lyssavirus type-1 viral RNA in the thyroid gland of experimentally-infected Eptesicus fuscus bats. Zoonoses Public Health 56, 270–277.[CrossRef]
    [Google Scholar]
  17. Franka, R., Johnson, N., Müller, T., Vos, A., Neubert, L., Freuling, C., Rupprecht, C. E. & Fooks, A. R. ( 2008; ). Susceptibility of North American big brown bats (Eptesicus fuscus) to infection with European bat lyssavirus type 1. J Gen Virol 89, 1998–2010.[CrossRef]
    [Google Scholar]
  18. Freuling, C., Grossmann, E., Conraths, F. J., Schameitat, A., Kliemt, J., Auer, E., Greiser-Wilke, I. & Müller, T. ( 2008; ). First isolation of EBLV-2 in Germany. Vet Microbiol 131, 26–34.[CrossRef]
    [Google Scholar]
  19. Heaton, P. R., Johnstone, P., McElhinney, L. M., Cowley, R., O'Sullivan, E. & Whitby, J. E. ( 1997; ). Heminested PCR assay for detection of six genotypes of rabies and rabies-related viruses. J Clin Microbiol 35, 2762–2766.
    [Google Scholar]
  20. Hicks, D. J., Nuñez, A., Healy, D. M., Brookes, S. M., Johnson, N. & Fooks, A. R. ( 2009; ). Comparative pathological study of the murine brain after experimental infection with classical rabies virus and European bat lyssaviruses. J Comp Pathol 140, 113–126.[CrossRef]
    [Google Scholar]
  21. Hughes, G. J., Kuzmin, I. V., Schmitz, A., Blanton, J., Manangan, J., Murphy, S. & Rupprecht, C. E. ( 2006; ). Experimental infection of big brown bats (Eptesicus fuscus) with Eurasian bat lyssaviruses Aravan, Khujand, and Irkut virus. Arch Virol 151, 2021–2035.[CrossRef]
    [Google Scholar]
  22. Hutson, A. M., Spitzenberger, F., Aulagnier, S., Alcaldé, J. T., Csorba, G., Bumrungsri, S., Francis, C., Bates, P., Gumal, M. & other authors ( 2008; ). Eptesicus serotinus, IUCN Red List of Threatened Species, http://www.iucnredlist.org/
  23. Johnson, N., Wakeley, P. R., Brookes, S. M. & Fooks, A. R. ( 2006a; ). European bat lyssavirus type 2 RNA in Myotis daubentonii. Emerg Infect Dis 12, 1142–1144.[CrossRef]
    [Google Scholar]
  24. Johnson, N., Phillpotts, R. & Fooks, A. R. ( 2006b; ). Airborne transmission of lyssaviruses. J Med Microbiol 55, 785–790.[CrossRef]
    [Google Scholar]
  25. Johnson, N., Vos, A., Neubert, L., Freuling, C., Mansfield, K. L., Kaipf, I., Denzinger, A., Hicks, D., Nuñez, A. & other authors ( 2008; ). Experimental study of European bat lyssavirus type-2 infection in Daubenton's bats (Myotis daubentonii). J Gen Virol 89, 2662–2672.[CrossRef]
    [Google Scholar]
  26. King, A. A., Haagsma, J. & Kappeler, A. ( 2004; ). Lyssavirus infections in European bats. In Historical Perspective of Rabies in Europe and the Mediterranean Basin, pp. 221–241. Edited by A. A. King, A. R. Fooks, M. Aubert & A. I. Wandeler. Paris: World Organization for Animal Health (OIE).
  27. Kuzmin, I. V. & Rupprecht, C. E. ( 2007; ). Bat rabies. In Rabies, 2nd edn, pp. 259–307. Edited by A. C. Jackson & W. Wunner. New York: Academic Press.
  28. Kuzmin, I. V., Botvinkin, A. D. & Shaimardanov, R. T. ( 1994; ). Experimental rabies and rabies-related infections in bats. Vopr Virusol 39, 17–21 (in Russian).
    [Google Scholar]
  29. Kuzmin, I. V., Hughes, G. J., Botvinkin, A. D., Orciari, L. A. & Rupprecht, C. E. ( 2005; ). Phylogenetic relationships of Irkut and West Caucasian bat viruses within the Lyssavirus genus and suggested quantitative criteria based on the N gene sequence for lyssavirus genotype definition. Virus Res 111, 28–43.[CrossRef]
    [Google Scholar]
  30. Kuzmin, I. V., Franka, R. & Rupprecht, C. E. ( 2008; ). Experimental infection of big brown bats (Eptesicus fuscus) with West Caucasian bat virus (WCBV). Dev Biol (Basel) 131, 327–337.
    [Google Scholar]
  31. Markotter, W. ( 2007; ). Molecular epidemiology and pathogenesis of Lagos bat virus, a rabies related virus specific to Africa. PhD thesis, Department of Microbiology and Plant Pathology, University of Pretoria, Pretoria, South Africa.
  32. Mohr, W. ( 1957; ). Die Tollwut. Med Klin 52, 1057–1060 (in German).
    [Google Scholar]
  33. Morimoto, K., Patel, M., Corisdeo, S., Hooper, D. C., Fu, Z. F., Rupprecht, C. E., Koprowski, H. & Dietzschold, B. ( 1996; ). Characterization of a unique variant of bat rabies virus responsible for newly emerging human cases in North America. Proc Natl Acad Sci U S A 93, 5653–5658.[CrossRef]
    [Google Scholar]
  34. Müller, T., Cox, J., Peter, W., Schafer, R., Johnson, N., McElhinney, L. M., Geue, J. L. & Tjornehoj, K. ( 2004; ). Spill-over of European bat lyssavirus type 1 into a stone marten (Martes foina) in Germany. J Vet Med B Infect Dis Vet Public Health 51, 49–54.[CrossRef]
    [Google Scholar]
  35. Müller, T., Johnson, N., Freuling, C. M., Fooks, A. R., Selhorst, T. & Vos, A. ( 2007; ). Epidemiology of bat rabies in Germany. Arch Virol 152, 273–288.[CrossRef]
    [Google Scholar]
  36. Ondrejkova, A., Franka, R., Ondrejka, R., Svrcek, S., Süli, J., Zubricky, P., Benisek, Z., Bajova, V., Bugarsky, A. & Bourhy, H. ( 2004; ). Identification of a lyssavirus isolate from a bat (Eptesicus serotinus). Bull Vet Inst Pulawy 48, 11–13.
    [Google Scholar]
  37. Padgett, D. A. & Glaser, R. ( 2003; ). How stress influences the immune response. Trends Immunol 24, 444–448.[CrossRef]
    [Google Scholar]
  38. Pajamo, K., Harkess, G., Goddard, T., Marston, D., McElhinney, L., Johnson, N. & Fooks, A. R. ( 2008; ). Isolation of European bat lyssavirus type 2 (EBLV-2) in a Daubenton's bat in the UK with a minimum incubation period of 9 months. Rabies Bulletin Europe 32, 6–7.
    [Google Scholar]
  39. Pérez-Jordá, J. L., Ibánez, C., Muños-Cervera, M. & Téllez, A. ( 1995; ). Lyssavirus in Eptesicus serotinus (Chiroptera, Vespertilionidae). J Wildl Dis 31, 372–377.[CrossRef]
    [Google Scholar]
  40. Picard-Meyer, E., Brookes, S. M., Barrat, J., Litaize, E., Patron, C., Biarnais, M., Healy, D. M., Johnson, L., Fooks, A. R. & Cliquet, F. ( 2008; ). Experimental infection of foxes with European bat lyssaviruses type-1 and -2. Dev Biol (Basel) 131, 339–345.
    [Google Scholar]
  41. Rønsholt, L. ( 2002; ). A new case of European bat lyssavirus (EBL) infection in Danish sheep. Rabies Bulletin Europe 26, 15
    [Google Scholar]
  42. Schneider, L. G. ( 1982; ). Antigenic variants of rabies virus. Comp Immunol Microbiol Infect Dis 5, 101–107.[CrossRef]
    [Google Scholar]
  43. Serra-Cobo, J., Amengual, B., Abellán, C. & Bourhy, H. ( 2002; ). European bat lyssavirus infection in Spanish bat populations. Emerg Infect Dis 8, 413–420.[CrossRef]
    [Google Scholar]
  44. Smith, J. S., Yager, P. A. & Baer, G. M. ( 1973; ). A rapid reproducible test for determining rabies neutralizing antibody. Bull World Health Organ 48, 535–541.
    [Google Scholar]
  45. Smreczak, M., Orlowska, A., Trêbas, P. & Zmudzinski, J. F. ( 2007; ). The first case of European bat lyssavirus type 1b infection in E. serotinus in Poland. Joint OIE/WHO/EU International Conference: ‘Towards the Elimination of Rabies in Eurasia’, Paris, France, 27–30 May 2007, abstract 89.
  46. Tjornehoj, K., Fooks, A. R., Agerholm, J. S. & Ronsholt, L. ( 2006; ). Natural and experimental infection of sheep with European bat lyssavirus type-1 of Danish bat origin. J Comp Pathol 134, 190–201.[CrossRef]
    [Google Scholar]
  47. Tordo, N., Benmansour, A., Calisher, C., Dietzgen, R. G., Fang, R. X., Jackson, A. O., Kurath, G., Nadin-Davis, S., Tesh, R. B. & Walker, P. J. ( 2004; ). Rhabdoviridae. In Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses, pp. 623–644. Edited by C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger & L. A. Ball. London: Elsevier/Academic Press.
  48. Van der Poel, W. H., Van der Heide, R., Verstraten, E. R., Takumi, K., Lina, P. H. & Kramps, J. A. ( 2005; ). European bat lyssaviruses, The Netherlands. Emerg Infect Dis 11, 1854–1859.[CrossRef]
    [Google Scholar]
  49. Vázquez-Morón, S., Juste, J., Ibáñez, C., Aznar, C., Ruiz-Villamor, E. & Echevarría, J. E. ( 2008a; ). Asymptomatic rhabdovirus infection in meridional serotine bats (Eptesicus isabellinus) from Spain. Dev Biol (Basel) 131, 311–316.
    [Google Scholar]
  50. Vázquez-Morón, S., Juste, J., Ibáñez, C., Ruiz-Villamor, R., Avellón, A., Vera, M. & Echevarría, J. E. ( 2008b; ). Endemic circulation of European bat lyssavirus type 1 in serotine bats, Spain. Emerg Infect Dis 14, 1263–1266.[CrossRef]
    [Google Scholar]
  51. Vos, A., Muller, T., Cox, J., Neubert, L. & Fooks, A. R. ( 2004a; ). Susceptibility of ferrets (Mustela putorius furo) to experimentally induced rabies with European bat lyssaviruses (EBLV). J Vet Med B Infect Dis Vet Public Health 51, 55–60.[CrossRef]
    [Google Scholar]
  52. Vos, A., Muller, T., Neubert, L., Zurbriggen, A., Botteron, C., Pohle, D., Schoon, H., Haas, L. & Jackson, A. C. ( 2004b; ). Rabies in red foxes (Vulpes vulpes) experimentally infected with European bat lyssavirus type 1. J Vet Med B Infect Dis Vet Public Health 51, 327–332.[CrossRef]
    [Google Scholar]
  53. Vos, A., Kaipf, I., Denzinger, A., Fooks, A. R., Johnson, N. & Müller, T. ( 2007; ). European bat lyssaviruses – an ecological enigma. Acta Chiropt 9, 283–296.[CrossRef]
    [Google Scholar]
  54. Wakeley, P. R., Johnson, N., McElhinney, L. M., Marston, D., Sawyer, J. & Fooks, A. R. ( 2005; ). Development of a real-time, TaqMan reverse transcription-PCR assay for detection and differentiation of lyssavirus genotypes 1, 5, and 6. J Clin Microbiol 43, 2786–2792.[CrossRef]
    [Google Scholar]
  55. Webster, W. A. & Casey, G. A. ( 1996; ). Virus isolation in neuroblastoma cell culture. In Laboratory Techniques in Rabies, 4th edn, pp. 93–104. Edited by F.-X. Meslin, M. M. Kaplan & H. Koprowski. Geneva, Switzerland: World Health Organization.
  56. WHO ( 2005; ). Expert consultation on rabies, first report. World Health Organ Tech Rep Ser 931, 1–121.
    [Google Scholar]
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