1887

Abstract

Bats are natural reservoirs for the majority of lyssaviruses globally, and are unique among mammals in having exceptional sociality and longevity. Given these facets, and the recognized status of bats as reservoirs for rabies viruses (RABVs) in the Americas, individual bats may experience repeated exposure to RABV during their lifetime. Nevertheless, little information exists with regard to within-host infection dynamics and the role of immunological memory that may result from abortive RABV infection in bats. In this study, a cohort of big brown bats () was infected intramuscularly in the left and right masseter muscles with varying doses [10–10 median mouse intracerebral lethal doses (MICLD)] of an RABV variant isolated from a naturally infected big brown bat. Surviving bats were infected a second time at 175 days post-(primary) infection with a dose (10–10 MICLD) of the same RABV variant. Surviving bats were infected a third time at either 175 or 305 days post-(secondary) infection with a dose (10 MICLD) of the same RABV variant. When correcting for dose, similar mortality was observed following primary and secondary infection, but reduced mortality was observed following the third and last RABV challenge, despite infection with a high viral dose. Inducible RABV-neutralizing antibody titres post-infection were ephemeral among infected individuals, and dropped below levels of detection in several bats between subsequent infections. These results suggest that long-term repeated infection of bats may confer significant immunological memory and reduced susceptibility to RABV infection.

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2010-09-01
2024-03-28
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References

  1. Austad, S. N. & Fischer, K. E.(1991). Mammalian aging, metabolism, and ecology: evidence from the bats and marsupials. J Gerontol 46, B47–B53.[CrossRef] [Google Scholar]
  2. Baer, G. M. & Bales, G. L.(1967). Experimental rabies infection in the Mexican freetail bat. J Infect Dis 117, 82–90.[CrossRef] [Google Scholar]
  3. Blanton, J. D., Robertson, K., Palmer, D. & Rupprecht, C. E.(2009). Rabies surveillance in the United States during 2008. J Am Vet Med Assoc 235, 676–689.[CrossRef] [Google Scholar]
  4. Brunet-Rossinni, A. K. & Wilkinson, G. S.(2009). Methods for age estimation and the study of senescence in bats. In Ecological and Behavioral Methods for the Study of Bats, pp. 315–325. Edited by T. H. Kunz & S. Parsons. Baltimore, MD: Johns Hopkins University Press.
  5. Daniels, J. B., Stuart, G., Wheeler, R. E., Gifford, C., Ahearn, J. P., Philbrook, R., Hayes, R. O. & MacCready, R. A.(1960). A search for encephalitis and rabies in bats of eastern Massachusetts. N Engl J Med 263, 516–520.[CrossRef] [Google Scholar]
  6. Dean, D. J., Abelseth, M. K. & Atanasiu, P.(1996). The fluorescent antibody test. In Laboratory Techniques in Rabies, 4th edn, pp. 88–93. Edited by F. X. Meslin, M. M. Kaplan & H. Koprowski. Geneva: WHO.
  7. Dietzschold, B., Li, J., Faber, M. & Schnell, M.(2008). Concepts in the pathogenesis of rabies. Future Virol 3, 481–490.[CrossRef] [Google Scholar]
  8. Dimitrov, D. T. & Hallam, T. G.(2009). Effects of immune system diversity and physical variation of immunotypic mixing on the dynamics of rabies in bats. J Biol Dyn 3, 164–179.[CrossRef] [Google Scholar]
  9. Girard, K. F., Hitchcock, H. B., Edsall, G. & MacCready, R. A.(1965). Rabies in bats in southern New England. N Engl J Med 272, 75–80.[CrossRef] [Google Scholar]
  10. Goehring, H. H.(1972). Twenty-year study of Eptesicus fuscus in Minnesota. J Mammal 53, 201–207.[CrossRef] [Google Scholar]
  11. Hall, E. R.(1981).The Mammals of North America. New York: Wiley.
  12. Hitchcock, H. B.(1965). Twenty-three years of bat banding in Ontario and Quebec. Can Field Nat 79, 4–14. [Google Scholar]
  13. Jackson, F. R., Turmelle, A. S., Farino, D. M., Franka, R., McCracken, G. F. & Rupprecht, C. E.(2008). Experimental rabies virus infection of big brown bats (Eptesicus fuscus). J Wildl Dis 44, 612–621.[CrossRef] [Google Scholar]
  14. Koopman, K. F.(1982). Biogeography of the bats of South America. In Mammalian Biology in South America, pp. 273–302. Edited by M. A. Mares & H. H. Genoways. Pittsburgh, PA: University of Pittsburgh.
  15. Kunz, T. H. & Pierson, E. D.(1994). Bats of the world: an introduction. In Bats of the World, pp. 1–46. Edited by R. M. Nowak. Baltimore, MD: Johns Hopkins University Press.
  16. Kurta, A. & Baker, R. H.(1990).Eptesicus fuscus. Mamm Species 356, 1–10. [Google Scholar]
  17. Lafon, M.(2007). Immunology. In Rabies, 2nd edn, pp. 489–504. Edited by A. Jackson & W. Wunner. London: Academic Press.
  18. Leslie, M. J., Messenger, S., Rohde, R. E., Smith, J., Cheshier, R., Hanlon, C. & Rupprecht, C. E.(2006). Bat-associated rabies virus in skunks. Emerg Infect Dis 12, 1274–1277.[CrossRef] [Google Scholar]
  19. McQuiston, J. H., Yager, P. A., Smith, J. S. & Rupprecht, C. E.(2001). Epidemiologic characteristics of rabies virus variants in dogs and cats in the United States, 1999. J Am Vet Med Assoc 218, 1939–1942.[CrossRef] [Google Scholar]
  20. Messenger, S. L., Smith, J. S. & Rupprecht, C. E.(2002). Emerging epidemiology of bat-associated cryptic cases of rabies in humans in the United States. Clin Infect Dis 35, 738–747.[CrossRef] [Google Scholar]
  21. Messenger, S. L., Smith, J. S., Orciari, L. A., Yager, P. A. & Rupprecht, C. E.(2003). Emerging pattern of rabies deaths and increased viral infectivity. Emerg Infect Dis 9, 151–154.[CrossRef] [Google Scholar]
  22. Mondul, A. M., Krebs, J. W. & Childs, J. E.(2003). Trends in national surveillance for rabies among bats in the United States (1993–2000). J Am Vet Med Assoc 222, 633–639.[CrossRef] [Google Scholar]
  23. Moore, M. S., Jackson, F. R., Turmelle, A. S., Panasuk, B. J., Mendonca, M. T., Rupprecht, C. E., Kunz, T. H. & McCracken, G. F.(2008). Rabies exposure, relative immune function, and life-history traits in the big brown bat (Eptesicus fuscus). Bat Res News 49, 150 [Google Scholar]
  24. O'Shea, T. J., Shankar, V., Bowen, R. A., Rupprecht, C. E. & Wimsatt, J. H.(2003). Do bats acquire immunity to rabies? Evidence from the field. Bat Res News 44, 161 [Google Scholar]
  25. Pybus, M. J.(1986). Rabies in insectivorous bats of western Canada, 1979 to 1983. J Wildl Dis 22, 307–313.[CrossRef] [Google Scholar]
  26. Reed, L. J. & Muench, H.(1938). A simple method of estimating fifty per cent endpoints. Am J Hyg 27, 493–497. [Google Scholar]
  27. Schowalter, D. B.(1980). Characteristics of bat rabies in Alberta. Can J Comp Med 44, 70–76. [Google Scholar]
  28. Smith, J. S.(1981). Mouse model for abortive rabies infection of the central nervous system. Infect Immun 31, 297–308. [Google Scholar]
  29. Smith, J. S.(1996). New aspects of rabies with emphasis on epidemiology, diagnosis, and prevention of the disease in the United States. Clin Microbiol Rev 9, 166–176. [Google Scholar]
  30. Smith, J. S., McCelland, C. L., Reid, F. L. & Baer, G. M.(1982). Dual role of the immune response in street rabiesvirus infection of mice. Infect Immun 35, 213–221. [Google Scholar]
  31. Smith, J. S., Yager, P. & Baer, G.(1996). A rapid fluorescent focus inhibition test (RFFIT) for determining rabies virus-neutralizing antibody. In Laboratory Techniques in Rabies, pp. 181–192. Edited by F. X. Meslin, M. M. Kaplan & H. Koprowski. Geneva: WHO.
  32. Trimarchi, C. & Debbie, J. G.(1977). Naturally occurring rabies virus and neutralizing antibody in two species of insectivorous bats of New York state. J Wildl Dis 13, 366–369.[CrossRef] [Google Scholar]
  33. Trimarchi, C. V. & Smith, J.(2002). Diagnostic evaluation. In Rabies, pp. 308–344. Edited by A. C. Jackson & W. H. Wunner. San Diego, CA: Academic Press.
  34. Turmelle, A. S.(2002).Phylogeography and population structure of the big brown bat (Eptesicus fuscus). Honors thesis, Boston University, Boston, MA, USA.
  35. Turmelle, A. S., Allen, L. C., Jackson, F. R., Kunz, T. H., Rupprecht, C. & McCracken, G. F.(2010). Ecology of rabies virus exposure in colonies of Brazilian free-tailed bats (Tadarida brasiliensis) at natural and man-made roosts in Texas. Vector Borne Zoonotic Dis 10, 165–175.[CrossRef] [Google Scholar]
  36. Voigt, C. & Cruz-Neto, A.(2009). Energetic analysis of bats. In Ecological and Behavioral Methods for the Study of Bats, pp. 623–645. Edited by T. H. Kunz & S. Parsons. Baltimore, MD: Johns Hopkins University Press.
  37. Wang, Z. W., Sarmento, L., Wang, Y., Li, X. Q., Dhingra, V., Tseggai, T., Jiang, B. & Fu, Z. F.(2005). Attenuated rabies virus activates, while pathogenic rabies virus evades, the host innate immune responses in the central nervous system. J Virol 79, 12554–12565.[CrossRef] [Google Scholar]
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