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. 1997 Apr-Jun;3(2):205–211. doi: 10.3201/eid0302.970218

The hantaviruses of Europe: from the bedside to the bench.

J Clement 1, P Heyman 1, P McKenna 1, P Colson 1, T Avsic-Zupanc 1
PMCID: PMC2627610  PMID: 9204306

Abstract

In Europe, hantavirus disease can hardly be called an emerging zoonosis; it is rather a rediscovered disease. Since 1934 an epidemic condition with primarily renal involvement has been described in Sweden. Nowadays, hundreds to thousands of cases per year are registered in Fennoscandia, fluctuating with the numbers of the specific Arvicoline-rodent reservoir, the red bank vole, which carries the main European serotype, Puumala (PUU). In the early 1980s, the rat-transmitted serotype, Seoul (SEO), caused laboratory outbreaks throughout Europe, and recent reports also suggest sporadic, wild rat-spread hantavirus disease. In the Balkans, at least four serotypes are present simultaneously: PUU, SEO, the "Korean" prototype Hantaan (HTN) or HTN-like types, and Dobrava, the latter causing a mortality rate of up to 20%. Moreover, recent genotyping studies have disclosed several PUU-like genotypes spread in Europe and/or Russia by other genera of the Arvicoline-rodent subfamily: Tula, Tobetsu, Khabarovsk, and Topografov. Their importance for human pathogenicity is still unclear, but serologic cross-reactions with PUU antigen might have caused their misdiagnosis as PUU-infections in the past.

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Selected References

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  1. Alexeyev O. A., Elgh F., Zhestkov A. V., Wadell G., Juto P. Hantaan and Puumala virus antibodies in blood donors in Samara, an HFRS-endemic region in European Russia. Lancet. 1996 May 25;347(9013):1483–1483. doi: 10.1016/s0140-6736(96)91717-1. [DOI] [PubMed] [Google Scholar]
  2. Antoniades A., Grekas D., Rossi C. A., LeDuc J. W. Isolation of a hantavirus from a severely ill patient with hemorrhagic fever with renal syndrome in Greece. J Infect Dis. 1987 Dec;156(6):1010–1013. doi: 10.1093/infdis/156.6.1010. [DOI] [PubMed] [Google Scholar]
  3. Antoniadis A., Stylianakis A., Papa A., Alexiou-Daniel S., Lampropoulos A., Nichol S. T., Peters C. J., Spiropoulou C. F. Direct genetic detection of Dobrava virus in Greek and Albanian patients with hemorrhagic fever with renal syndrome. J Infect Dis. 1996 Aug;174(2):407–410. doi: 10.1093/infdis/174.2.407. [DOI] [PubMed] [Google Scholar]
  4. Avsic-Zupanc T., Poljak M., Furlan P., Kaps R., Xiao S. Y., Leduc J. W. Isolation of a strain of a Hantaan virus from a fatal case of hemorrhagic fever with renal syndrome in Slovenia. Am J Trop Med Hyg. 1994 Oct;51(4):393–400. [PubMed] [Google Scholar]
  5. Avsic-Zupanc T., Xiao S. Y., Stojanovic R., Gligic A., van der Groen G., LeDuc J. W. Characterization of Dobrava virus: a Hantavirus from Slovenia, Yugoslavia. J Med Virol. 1992 Oct;38(2):132–137. doi: 10.1002/jmv.1890380211. [DOI] [PubMed] [Google Scholar]
  6. Brummer-Korvenkontio M., Vaheri A., Hovi T., von Bonsdorff C. H., Vuorimies J., Manni T., Penttinen K., Oker-Blom N., Lähdevirta J. Nephropathia epidemica: detection of antigen in bank voles and serologic diagnosis of human infection. J Infect Dis. 1980 Feb;141(2):131–134. doi: 10.1093/infdis/141.2.131. [DOI] [PubMed] [Google Scholar]
  7. Clement J., Colson P., McKenna P. Hantavirus pulmonary syndrome in New England and Europe. N Engl J Med. 1994 Aug 25;331(8):545–548. [PubMed] [Google Scholar]
  8. Clement J., Heyman P., Colson P., Groeneveld P. H. Spread of hantavirus infections in Europe. Lancet. 1996 Mar 16;347(9003):771–771. doi: 10.1016/s0140-6736(96)90128-2. [DOI] [PubMed] [Google Scholar]
  9. Clement J., McKenna P., Avsic-Zupanc T., Skinner C. R. Rat-transmitted hantavirus disease in Sarajevo. Lancet. 1994 Jul 9;344(8915):131–131. doi: 10.1016/s0140-6736(94)91319-6. [DOI] [PubMed] [Google Scholar]
  10. Clement J., Underwood P., Ward D., Pilaski J., LeDuc J. Hantavirus outbreak during military manoeuvres in Germany. Lancet. 1996 Feb 3;347(8997):336–336. doi: 10.1016/s0140-6736(96)90519-x. [DOI] [PubMed] [Google Scholar]
  11. Colson P., Damoiseaux P., Brisbois J., Duvivier E., Levecque P., Roger J. M., Bouilliez D. J., McKenna P., Clement J. Epidémie d'hantavirose dans l'Entre-Sambre-et-Meuse: année 1992-1993 Données cliniques et biologiques. Acta Clin Belg. 1995;50(4):197–206. doi: 10.1080/17843286.1995.11718447. [DOI] [PubMed] [Google Scholar]
  12. Filipe A. R., Andrade H. R., Sommer A. I., Traavik T. Hantaviral antigens and antibodies in wild rodents in Portugal. Acta Virol. 1991 May;35(3):287–291. [PubMed] [Google Scholar]
  13. Gerding M. N., Groen J., Jordans J. G., Osterhaus A. D. Hantavirus nephropathy in The Netherlands: clinical, histopathological and epidemiological findings. Neth J Med. 1995 Sep;47(3):106–112. doi: 10.1016/0300-2977(95)00054-q. [DOI] [PubMed] [Google Scholar]
  14. Gligic A., Dimkovic N., Xiao S. Y., Buckle G. J., Jovanovic D., Velimirovic D., Stojanovic R., Obradovic M., Diglisic G., Micic J. Belgrade virus: a new hantavirus causing severe hemorrhagic fever with renal syndrome in Yugoslavia. J Infect Dis. 1992 Jul;166(1):113–120. doi: 10.1093/infdis/166.1.113. [DOI] [PubMed] [Google Scholar]
  15. Groen J., Gerding M. N., Jordans J. G., Clement J. P., Nieuwenhuijs J. H., Osterhaus A. D. Hantavirus infections in The Netherlands: epidemiology and disease. Epidemiol Infect. 1995 Apr;114(2):373–383. doi: 10.1017/s0950268800058003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Groen J., Jordans H. G., Clement J. P., Rooijakkers E. J., UytdeHaag F. G., Dalrymple J., Van der Groen G., Osterhaus A. D. Identification of Hantavirus serotypes by testing of post-infection sera in immunofluorescence and enzyme-linked immunosorbent assays. J Med Virol. 1991 Jan;33(1):26–32. doi: 10.1002/jmv.1890330106. [DOI] [PubMed] [Google Scholar]
  17. Hukic M., Kurt A., Torstensson S., Lundkvist A., Wiger D., Niklasson B. Haemorrhagic fever with renal syndrome in north-east Bosnia. Lancet. 1996 Jan 6;347(8993):56–57. doi: 10.1016/s0140-6736(96)91586-x. [DOI] [PubMed] [Google Scholar]
  18. Hörling J., Chizhikov V., Lundkvist A., Jonsson M., Ivanov L., Dekonenko A., Niklasson B., Dzagurova T., Peters C. J., Tkachenko E. Khabarovsk virus: a phylogenetically and serologically distinct hantavirus isolated from Microtus fortis trapped in far-east Russia. J Gen Virol. 1996 Apr;77(Pt 4):687–694. doi: 10.1099/0022-1317-77-4-687. [DOI] [PubMed] [Google Scholar]
  19. Kariwa H., Yoshizumi S., Arikawa J., Yoshimatsu K., Takahashi K., Takashima I., Hashimoto N. Evidence for the existence of Puumula-related virus among Clethrionomys rufocanus in Hokkaido, Japan. Am J Trop Med Hyg. 1995 Sep;53(3):222–227. doi: 10.4269/ajtmh.1995.53.222. [DOI] [PubMed] [Google Scholar]
  20. LeDuc J. W., Smith G. A., Childs J. E., Pinheiro F. P., Maiztegui J. I., Niklasson B., Antoniades A., Robinson D. M., Khin M., Shortridge K. F. Global survey of antibody to Hantaan-related viruses among peridomestic rodents. Bull World Health Organ. 1986;64(1):139–144. [PMC free article] [PubMed] [Google Scholar]
  21. Lee P. W., Amyx H. L., Gajdusek D. C., Yanagihara R. T., Goldgaber D., Gibbs C. J., Jr New hemorrhagic fever with renal syndrome-related virus in rodents in the United States. Lancet. 1982 Dec 18;2(8312):1405–1405. [PubMed] [Google Scholar]
  22. McCaughey C., Montgomery W. I., Twomey N., Addley M., O'Neill H. J., Coyle P. V. Evidence of hantavirus in wild rodents in Northern Ireland. Epidemiol Infect. 1996 Oct;117(2):361–365. doi: 10.1017/s0950268800001540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. McKenna P., Clement J., Matthys P., Coyle P. V., McCaughey C. Serological evidence of Hantavirus disease in Northern Ireland. J Med Virol. 1994 May;43(1):33–38. doi: 10.1002/jmv.1890430107. [DOI] [PubMed] [Google Scholar]
  24. McKenna P., van der Groen G., Hoofd G., Beelaert G., Leirs H., Verhagen R., Kints J. P., Cormont F., Nisol F., Bazin H. Eradication of hantavirus infection among laboratory rats by application of caesarian section and a foster mother technique. J Infect. 1992 Sep;25(2):181–190. doi: 10.1016/0163-4453(92)94035-v. [DOI] [PubMed] [Google Scholar]
  25. Mustonen J., Vaheri A., Clement J. Third International Conference on Haemorrhagic Fever with Renal Syndrome (HFRS) and Hantaviruses. Nephrol Dial Transplant. 1996 Apr;11(4):730–733. doi: 10.1093/oxfordjournals.ndt.a027376. [DOI] [PubMed] [Google Scholar]
  26. Niklasson B., LeDuc J. W. Epidemiology of nephropathia epidemica in Sweden. J Infect Dis. 1987 Feb;155(2):269–276. doi: 10.1093/infdis/155.2.269. [DOI] [PubMed] [Google Scholar]
  27. Niklasson B., Leduc J., Nyström K., Nyman L. Nephropathia epidemica: incidence of clinical cases and antibody prevalence in an endemic area of Sweden. Epidemiol Infect. 1987 Oct;99(2):559–562. doi: 10.1017/s0950268800068060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Papadimitriou M. G., Antoniadis A. Hantavirus nephropathy in Greece. Lancet. 1994 Apr 23;343(8904):1038–1038. doi: 10.1016/s0140-6736(94)90157-0. [DOI] [PubMed] [Google Scholar]
  29. Plyusnin A., Vapalahti O., Lankinen H., Lehväslaiho H., Apekina N., Myasnikov Y., Kallio-Kokko H., Henttonen H., Lundkvist A., Brummer-Korvenkontio M. Tula virus: a newly detected hantavirus carried by European common voles. J Virol. 1994 Dec;68(12):7833–7839. doi: 10.1128/jvi.68.12.7833-7839.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rodríguez J. A., Vaqué J. La enfermedad por Hantavirus: una infección emergente. Enferm Infecc Microbiol Clin. 1994 Dec;12(10):477–479. [PubMed] [Google Scholar]
  31. Song W., Torrez-Martinez N., Irwin W., Harrison F. J., Davis R., Ascher M., Jay M., Hjelle B. Isla Vista virus: a genetically novel hantavirus of the California vole Microtus californicus. J Gen Virol. 1995 Dec;76(Pt 12):3195–3199. doi: 10.1099/0022-1317-76-12-3195. [DOI] [PubMed] [Google Scholar]
  32. Stuart L. M., Rice P. S., Lloyd G., Beale R. J. A soldier in respiratory distress. Lancet. 1996 Jan 6;347(8993):30–30. doi: 10.1016/s0140-6736(96)91560-3. [DOI] [PubMed] [Google Scholar]
  33. Zöller L., Faulde M., Meisel H., Ruh B., Kimmig P., Schelling U., Zeier M., Kulzer P., Becker C., Roggendorf M. Seroprevalence of hantavirus antibodies in Germany as determined by a new recombinant enzyme immunoassay. Eur J Clin Microbiol Infect Dis. 1995 Apr;14(4):305–313. doi: 10.1007/BF02116523. [DOI] [PubMed] [Google Scholar]

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