Skip to main content Accessibility help
×
Home

Twenty years of active bat rabies surveillance in Germany: a detailed analysis and future perspectives

  • J. SCHATZ (a1), B. OHLENDORF (a2), P. BUSSE (a3), G. PELZ (a4), D. DOLCH (a5), J. TEUBNER (a5), J. A. ENCARNAÇÃO (a6), R.-U. MÜHLE (a7), M. FISCHER (a1), B. HOFFMANN (a1), L. KWASNITSCHKA (a1), A. BALKEMA-BUSCHMANN (a1), T. C. METTENLEITER (a1), T. MÜLLER (a1) and C. M. FREULING (a1)...

Summary

In Germany, active bat rabies surveillance was conducted between 1993 and 2012. A total of 4546 oropharyngeal swab samples from 18 bat species were screened for the presence of EBLV-1- , EBLV-2- and BBLV-specific RNA. Overall, 0·15% of oropharyngeal swab samples tested EBLV-1 positive, with the majority originating from Eptesicus serotinus. Interestingly, out of seven RT–PCR-positive oropharyngeal swabs subjected to virus isolation, viable virus was isolated from a single serotine bat (E. serotinus). Additionally, about 1226 blood samples were tested serologically, and varying virus neutralizing antibody titres were found in at least eight different bat species. The detection of viral RNA and seroconversion in repeatedly sampled serotine bats indicates long-term circulation of the virus in a particular bat colony. The limitations of random-based active bat rabies surveillance over passive bat rabies surveillance and its possible application of targeted approaches for future research activities on bat lyssavirus dynamics and maintenance are discussed.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Twenty years of active bat rabies surveillance in Germany: a detailed analysis and future perspectives
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Twenty years of active bat rabies surveillance in Germany: a detailed analysis and future perspectives
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Twenty years of active bat rabies surveillance in Germany: a detailed analysis and future perspectives
      Available formats
      ×

Copyright

Corresponding author

* Author for correspondence: Dr C. M. Freuling, Institute of Molecular Biology, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Südufer 10, 17493 Greifswald-Insel Riems, Germany. (Email: conrad.freuling@fli.bund.de)

References

Hide All
1. World Health Organisation. Expert consultation on rabies, first report. World Health Organisation: Technical Report Series 2005; 931, 188.
2. Dietzgen, RG, et al. Family Rhabdoviridae. In: King, AMQ, Adams, MJ, Carstens, EB, Lefkowitz, EJ, eds. Virus Taxonomy: Classification and Nomenclature of Viruses – Ninth Report of the International Committee on Taxonomy of Viruses. San Diego: Elsevier, 2012, pp. 686713.
3. Banyard, AC, et al. Bat rabies. In: Jackson, AC, Wunner, W, eds. Rabies. New York: Academic Press, 2013.
4. Vos, A, et al. European bat lyssaviruses – an ecological enigma. Acta Chiropterologica 2007; 9: 283296.
5. Banyard, AC, et al. Bats and lyssaviruses. In: Jackson, AC, ed. Advance in Virus Research. Amsterdam: Elsevier, 2011, pp. 239289.
6. Schatz, J, et al. Bat rabies surveillance in Europe. Zoonoses and Public Health 2013; 60: 2234.
7. Freuling, CM, et al. Novel lyssavirus in Natterer's bat, Germany. Emerging Infectious Diseases 2011; 17: 15191522.
8. Picard-Meyer, E, et al. Isolation of the novel BBLV lyssavirus in Natterer's bat in France. Bulletin epidemiologique 2012; 55: 25.
9. Ceballos, NA, et al. Novel lyssavirus in bat, Spain. Emerging Infectious Diseases 2013; 19: 793795.
10. Botvinkin, AD, et al. Novel lyssaviruses isolated from bats in Russia. Emerging Infectious Diseases 2003; 9: 16231625.
11. Anon. Agreement on the conservation of populations of European bats (EUROBATS), 1991.
12. Med Vet Net Working Group. Passive and active surveillance of bat lyssavirus infections. Rabies Bulletin Europe 2005; 29: 5.
13. Anon. Agreement on the conservation of populations of bats in Europe (EUROBATS), Annex 5: bat rabies, 2006.
14. Trimarchi, CV, Debbie, JG. Naturally occurring rabies virus and neutralizing antibody in two species of insectivorous bats of New York State. Journal of Wildlife Diseases 1977; 13: 366369.
15. Constantine, DG, et al. Rabies in New Mexico cavern bats. Public Health Reports 1968; 83: 303316.
16. Steece, R, Altenbach, JS. Prevalence of rabies specific antibodies in the Mexican free-tailed bat (Tadarida brasiliensis mexicana) at Lava cave, New Mexico. Journal of Wildlife Diseases 1989; 25: 490496.
17. Harris, SL, et al. Targeted surveillance for European bat lyssaviruses in English bats (2003–06). Journal of Wildlife Diseases 2009; 45: 1030–41.
18. Brookes, SM, et al. European bat lyssavirus in Scottish bats. Emerging Infectious Diseases 2005; 11: 572578.
19. Picard-Meyer, E, et al. Active surveillance of bat rabies in France: a 5-year study (2004–2009). Veterinary Microbiology 2011; 151: 390395.
20. Vazquez-Moron, S, et al. Endemic circulation of European bat lyssavirus type 1 in serotine bats, Spain. Emerging Infectious Diseases 2008; 14: 12631266.
21. Serra-Cobo, J, et al. European bat lyssavirus infection in Spanish bat populations. Emerging Infectious Diseases 2002; 8: 413420.
22. Perez-Jorda, JL, et al. Lyssavirus in Eptesicus-Serotinus (Chiroptera, Vespertilionidae). Journal of Wildlife Diseases 1995; 31: 372377.
23. Amengual, B, et al. Temporal dynamics of European bat lyssavirus type 1 and survival of Myotis myotis bats in natural colonies. PLoS ONE 2007; 2: 17.
24. Echevarria, JE, et al. Screening of active lyssavirus infection in wild bat populations by viral RNA detection on oropharyngeal swabs. Journal of Clinical Microbiology 2001; 39: 36783683.
25. Megali, A, et al. Surveillance for European bat lyssavirus in Swiss bats. Archives in Virology 2010; 155: 1655–62.
26. National Veterinary Institute. Surveillance and control programmes: domestic and wild animals in Sweden 2008, 2009.
27. Hostnik, P, et al. Determination of bat lyssavirus in Slovenia. Zdravniski Vestnik 2010; 79: 265271.
28. Presetnik, P, et al. . Sunny new from the sunny side of the Alps – active surveillance for lyssaviruses in bats did not reveal the presence of EBLV in Slovenia. In: 2nd International Berlin Bat Meeting: Bat Biology and Infectious Diseases. Berlin, 19–21 February 2010: Leibniz Institute for Zoo and Wildlife Research, 2010.
29. Vranies, N, et al. Passive und active surveillance of lyssavirus in bats in Serbia. In: 2nd International Berlin Bat Meeting: Bat Biology and Infectious Diseases. Berlin, 19–21 February 2010: Leibniz Institute for Zoo and Wildlife Research, 2010, p. 94.
30. Klein, F, et al. First clue of circulation of lyssaviruses in bat populations. In: 2nd Symposium: ‘Wildlife Diseases Environment and Man’. Belgian Wildlife Disease Society, Brussels, 13 October 2007, p. 45.
31. Dietz, C, Helversen, O. von, Nill, D. Handbuch der Fledermäuse Europas und Nordwestafrikas. Biologie, Kennzeichen, Gefährdung. Stuttgart: Kosmos, 2007.
32. Schober, W, Grimmberger, E. Die Fledermäuse Europas – Kennen, bestimmen, schützen, 2nd edn. Stuttgart Franckh-Kosmos Verlags-GmbH, 1998.
33. Kunz, TH, Nagy, KA. Methods of energy budget analysis. In: Ecological and Behavioral Methods for the Study of Bats. Washington, DC: Smithsonian Institution Press, 1988, pp. 277302.
34. Vos, A, et al. Susceptibility of ferrets (Mustela putorius furo) to experimentally induced rabies with European bat lyssaviruses (EBLV). Journal of Veterinary Medicine. B, Infectious Diseases and Veterinary Public Health 2004; 51: 5560.
35. Freuling, CM, et al. Molecular diagnostics for the detection of Bokeloh bat lyssavirus in a bat from Bavaria, Germany. Virus Research. Published online: 7 August 2013 . doi:10.1016/j.virusres.2013.07.021.
36 Webster, WA, Casey, GA. Virus isolation in neuroblastoma cell culture. In: Meslin, FX, Kaplan, MM, Koprowski, H, eds. Laboratory Techniques in Rabies, 4th edn. Geneva: World Health Organization, 1996, pp. 93104.
37. Freuling, C, et al. A random grid based molecular epidemiological study on EBLV isolates from Germany. Developments in Biologicals (Basel) 2008; 131: 301309.
38. Smith, JS, Yager, PA, Baer, GM. A rapid reproducible test for determining rabies neutralizing antibody. Bulletin of the World Health Organization 1973; 48: 535541.
39. Cox, JH, Schneider, LG. Prophylactic immunization of humans against rabies by intradermal inoculation of human diploid cell culture vaccine. Journal of Clinical Microbiology 1976; 3: 96101.
40. Müller, T, et al. Epidemiology of bat rabies in Germany. Archives of Virology 2007; 152: 273288.
41. Franka, R, et al. Susceptibility of North American big brown bats (Eptesicus fuscus) to infection with European bat lyssavirus type 1. Journal of General Virology 2008; 89: 19982010.
42. Freuling, C, et al. Experimental infection of serotine bats (Eptesicus serotinus) with European bat lyssavirus type 1a. Journal of Genral Virology 2009; 90: 24932502.
43. Jakava-Viljanen, M, et al. First encounter of European bat lyssavirus type 2 (EBLV-2) in a bat in Finland. Epidemiology and Infection 2010; 138: 15811585.
44. Johnson, N, et al. Experimental study of European bat lyssavirus type-2 infection in Daubenton's bats (Myotis daubentonii). Journal of General Virology 2008; 89: 26622672.
45. Freuling, CM, et al. First isolation of EBLV-2 in Germany. Veterinary Microbiology 2008; 131: 2634.
46. Hayman, DTS, et al. A universal real-time assay for the detection of lyssaviruses. Journal of Virological Methods 2011; 177: 8793.
47. Hayman, DTS, et al. Endemic Lagos bat virus infection in Eidolon helvum . Epidemiology and Infection 2012; 140: 21632171.
48. Bowen, RA, et al. Prevalence of neutralizing antibodies to rabies virus in serum of seven species of insectivorous bats from colorado and new Mexico, United States. Journal of Wildlife Diseases 2013; 49: 367374.
49. Horton, DL, et al. Quantifying antigenic relationships among the lyssaviruses. Journal of Virology 2010; 84: 1184111848.
50. SNH. Scottish Natural Heritage releases latest bat lyssavirus monitoring results. (http://wwwsnhorguk/press/detailasp?id=2104 2009).
51. Hanlon, CA, et al. Efficacy of rabies biologics against new lyssaviruses from Eurasia. Virus Research 2005; 111: 4454.
52. Andrulonis, JA, et al. A micromethod for measuring rabies-neutralizing antibody. Journal of Wildlife Diseases 1976; 12: 552554.
53. Freuling, C, et al. Bat rabies – a Gordian knot? Berliner und Münchener Tierärztliche Wochenschrift 2009; 122: 425433.
54. Gilbert, AT, et al. Deciphering serology to understand the ecology of infectious diseases in wildlife. Ecohealth. Published online: 6 August 2013 . doi:10.1007/s10393-013-0856-0.

Keywords

Type Description Title
WORD
Supplementary materials

Schatz Supplementary Material
Fig S1

 Word (34 KB)
34 KB
UNKNOWN
Supplementary materials

Schatz Supplementary Material
Image

 Unknown (229 KB)
229 KB

Twenty years of active bat rabies surveillance in Germany: a detailed analysis and future perspectives

  • J. SCHATZ (a1), B. OHLENDORF (a2), P. BUSSE (a3), G. PELZ (a4), D. DOLCH (a5), J. TEUBNER (a5), J. A. ENCARNAÇÃO (a6), R.-U. MÜHLE (a7), M. FISCHER (a1), B. HOFFMANN (a1), L. KWASNITSCHKA (a1), A. BALKEMA-BUSCHMANN (a1), T. C. METTENLEITER (a1), T. MÜLLER (a1) and C. M. FREULING (a1)...

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed