Seoul hantavirus in Europe: first demonstration of the virus genome in wild Rattus norvegicus captured in France

  • P. HeymanEmail author
  • A. Plyusnina
  • P. Berny
  • C. Cochez
  • M. Artois
  • M. Zizi
  • J. P. Pirnay
  • A. Plyusnin


Although rats (Rattus rattus or Rattus norvegicus) worldwide have been found to carry Seoul hantavirus, there are at present only a very few reports of confirmed human Seoul hantavirus infections outside Asia, where the virus, in certain areas, is responsible for approximately 25% of the human hantavirus infections. In Europe, no confirmed human infections outside laboratories have been described, and although rats occasionally have been found to be antibody positive, the viral genome has not been demonstrated in these animals. The present report describes the first confirmed finding of Seoul hantavirus in R. norvegicus captured in Europe.


Genetic Lineage Hemorrhagic Fever With Renal Syndrome Lung Tissue Sample Hantavirus Infection Nephropathia Epidemica 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This study was made possible by grants STE/R and T WB11 from the Belgian Ministry of Defence, and grants RFA915 and 202012 from the Academy of Finland. The collection of rats was carried out during a preliminary research program on PUUV infection in bank voles (AER 2002), a program supported by the Veterinary School of Lyon in collaboration with Claude Bernard University, Lyon, and the Pasteur Institute, Paris. The experiments described comply with current European Union laws and regulations.


  1. 1.
    Elliott RM, Bouloy M, Calisher CH, Goldbach R, Moyer JT, Nichol ST, Pettersson R, Plyusnin A, Schmaljohn CS (2000) Bunyaviridae. In: van Regenmortel MHV, Fauquet CM, Bishop DHL, Carsten EB, Estes MK, Lemon SM, Maniloff J, Mayo MA, McGeoch DJ, Pringle CR, Wickner RB (eds) Virus taxonomy. VII report of the international committee on taxonomy of viruses. Academic, San Diego, pp 599–621Google Scholar
  2. 2.
    Vapalahti O, Mustonen J, Lundkvist Å, Henttonen H, Plyusnin A, Vaheri A (2003) Hantavirus infections in Europe. Lancet Infect Dis 3:653–661CrossRefPubMedGoogle Scholar
  3. 3.
    Brummer-Korvenkontio M, Henttonen H, Vaheri A (1982) Hemorrhagic fever with renal syndrome in Finland: ecology and virology of nephropathia epidemica. Scand J Infect Dis 36(Suppl):88–91Google Scholar
  4. 4.
    Avsic-Zupanc T, Xiao SY, Stojanovic R, Gligic A, van der Groen G, Leduc JW (1992) Characterization of Dobrava virus: a hantavirus from Slovenia, Yugoslavia. J Med Virol 38:132–137PubMedGoogle Scholar
  5. 5.
    Lee HW, Lee PW, Johnson KM (1978) Isolation of the etiologic agent of Korean hemorrhagic fever. J Infect Dis 137:298–308PubMedGoogle Scholar
  6. 6.
    Nemirov K, Vapalahti O, Lundkvist A, Vasilenko V, Golovljova I, Plyusnina A, Niemimaa J, Laakkonen J, Henttonen H, Vaheri A, Plyusnin A (1999) Isolation and characterization of Dobrava hantavirus carried by the striped field mouse (Apodemus agrarius) in Estonia. J Gen Virol 80(Pt 2):371–379PubMedGoogle Scholar
  7. 7.
    Plyusnin A, Morzunov SP (2001) Virus evolution and genetic diversity of hantaviruses and their rodent hosts. Curr Top Microbiol Immunol 256:47–75PubMedGoogle Scholar
  8. 8.
    Plyusnin A, Vapalahti O, Lankinen H, Lehvaslaiho H, Apekina N, Myasnikov Y, Kallio-Kokko H, Henttonen H, Lundkvist A, Brummer-Korvenkontio M (1994) Tula virus: a newly detected hantavirus carried by European common voles. J Virol 68:7833–7839Google Scholar
  9. 9.
    Plyusnin A, Cheng Y, Vapalahti O, Pejcoch M, Unar J, Jelinkova Z, Lehväslaiho H, Lundkvist Å, Vaheri A (1995) Genetic variation in Tula hantaviruses: sequence analysis of the S and M segments of strains from Central Europe. Virus Res 39:237–250PubMedGoogle Scholar
  10. 10.
    Sibold C, Meisel H, Labuda M, Kozuch O, Lysy J, Pejcock M, Krüger DH, Vaheri A, Plyusnin A (1999) Recombination in Tula hantavirus evolution: analysis of genetic lineages from Slovakia. J Virol 73:667–675PubMedGoogle Scholar
  11. 11.
    Heyman P, Klingstrom J, de Jaegere F, Leclercq G, Rozenfeld F, Escutenaire S, Vandenvelde C, Zizi M, Plyusnin A, Lundkvist A (2002) Tula hantavirus in Belgium. Epidemiol Infect 128:251–256PubMedGoogle Scholar
  12. 12.
    Klempa B, Meisel H, Rath S, Bartel J, Ulrich R, Kruger DH (2003) Occurrence of renal and pulmonary syndrome in a region of northeast Germany where Tula hantavirus circulates. J Clin Microbiol 41:4894–4897Google Scholar
  13. 13.
    Schultze D, Lundkvist A, Blauenstein U, Heyman P (2002) Tula virus infection associated with fever and exanthema after a wild rodent bite. Eur J Clin Microbiol Infect Dis 21:304–306Google Scholar
  14. 14.
    Schmaljohn C, Hjelle B (1997) Hantaviruses: a global disease problem. Emerg Infect Dis 3:95–104PubMedGoogle Scholar
  15. 15.
    Chu YK, Rossi C, Leduc JW, Lee HW, Schmaljohn CS, Dalrymple JM (1994) Serological relationships among viruses in the Hantavirus genus, family Bunyaviridae. Virology 198:196–204CrossRefPubMedGoogle Scholar
  16. 16.
    Lee HW, Baek LJ, Johnson KM (1982) Isolation of Hantaan virus, the etiologic agent of Korean hemorrhagic fever, from wild urban rats. J Infect Dis 146:638–644PubMedGoogle Scholar
  17. 17.
    Kim YS, Ahn C, Han JS, Kim S, Lee JS, Lee PW (1995) Hemorrhagic fever with renal syndrome caused by the Seoul virus. Nephron 71:419–427PubMedGoogle Scholar
  18. 18.
    Wang H, Yoshimatsu K, Ebihara H, Ogino M, Araki K, Kariwa H (2000) Genetic diversity of hantaviruses isolated in China and characterization of novel hantaviruses isolated from Niviventer confucianus and Rattus rattus. Virology 278:332–345CrossRefPubMedGoogle Scholar
  19. 19.
    Reynes JM, Soares JL, Hue T, Bouloy M, Sun S, Kruy SL, Flye Sainte Marie F, Zeller H (2003) Evidence of the presence of Seoul virus in Cambodia. Microbes Infect 5:769–773CrossRefPubMedGoogle Scholar
  20. 20.
    Plyusnina A, Ibrahim I-N, Winoto I, Porter KR, Gotama IBI, Lundkvist Å, Vaheri A, Plyusnin A (2004) Identification of Seoul hantavirus in Rattus norvegicus in Indonesia. Scand J Inf Dis 36:356–359CrossRefPubMedGoogle Scholar
  21. 21.
    Glass GE, Watson AJ, Leduc JW, Childs JE (1994) Domestic cases of hemorrhagic fever with renal syndrome in the United States. Nephron 68:48–51Google Scholar
  22. 22.
    Iversson LB, da Rosa AP, Rosa MD, Lomar AV, Sasaki MG, Leduc JW (1994) Human infection by Hantavirus in southern and southeastern Brazil. Rev Assoc Med Bras 40:85–92PubMedGoogle Scholar
  23. 23.
    Shi X, McCaughey C, Elliott RM (2003) Genetic characterisation of a hantavirus isolated from a laboratory-acquired infection. J Med Virol 71:105–109CrossRefPubMedGoogle Scholar
  24. 24.
    Kariwa H, Kimura M, Yoshizumi S, Arikawa J, Yoshimatsu K, Takashima I, Hashimoto N (1996) Modes of Seoul virus infections: persistency in newborn rats and transiency in adult rats. Arch Virol 141:2327–2338Google Scholar
  25. 25.
    Lee HW (1996) Epidemiology and pathogenesis of hemorrhagic fever with renal syndrome. In: Elliott RM (ed) The Bunyaviridae. Plenum, New York, pp 253–267Google Scholar
  26. 26.
    Webster JP, Macdonald DW (1995) Parasites of wild brown rats (Rattus norvegicus) on UK farms. Parasitology 111(Pt 3):247–255PubMedGoogle Scholar
  27. 27.
    Mitchell-Jones AJ, Amori G, Bogdanowicz W, Krystufek B, Reijnders PJH, Spitzenberger F, Stubbe M, Thissen JBM, Vohralik V, Zima J (1999) The atlas of European mammals. Academic, San Diego, pp 278Google Scholar
  28. 28.
    Krinke GJ (2000) The laboratory rat. Academic Press, San DiegoGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • P. Heyman
    • 1
    Email author
  • A. Plyusnina
    • 2
  • P. Berny
    • 3
  • C. Cochez
    • 4
  • M. Artois
    • 5
  • M. Zizi
    • 6
  • J. P. Pirnay
    • 6
  • A. Plyusnin
    • 2
  1. 1.Research Laboratory for Vector-Borne DiseasesQueen Astrid Military HospitalBrusselsBelgium
  2. 2.Department of Virology, Haartman InstituteUniversity of HelsinkiHelsinkiFinland
  3. 3.Pharmacy—Toxicology DepartmentEcole Nationale Vétérinaire de LyonMarcy l’EtoileFrance
  4. 4.National Reference Center for Hantavirus InfectionsQueen Astrid Military HospitalBrusselsBelgium
  5. 5.Infectious Diseases and Epidemiology UnitEcole Nationale Vétérinaire de LyonMarcy l’EtoileFrance
  6. 6.ACOS WB, Epidemiology and BiostatisticsQueen Astrid Military HospitalBrusselsBelgium

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