1887

Abstract

The capability of rodent-borne viruses to survive outside the host is critical for the transmission dynamics within rodent populations and to humans. The transmission of Puumala virus (PUUV) in colonized bank voles () was investigated and additional longevity studies in cell culture with PUUV and Tula (TULV) hantaviruses were performed. Wild-type PUUV excreted by experimentally infected donor bank voles was shown to be transmitted indirectly between rodents through contaminated beddings, and maintained its infectivity to recipient voles at room temperature for 12–15 days. In cell culture supernatants, PUUV and TULV remained infectious for 5–11 days at room temperature and up to 18 days at 4 °C, but were inactivated after 24 h at 37 °C. Interestingly, a fraction of dried virus was still infectious after 1 h at 56 °C. These results demonstrated that hantavirus transmission does not require direct contact between rodents, or between rodents and humans, and that the indirect transmission of PUUV through contaminated environment takes place among the rodents for a prolonged period of time. The results also have implications for safety recommendations for work with hantaviruses and for preventive measures.

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2006-08-01
2019-10-21
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References

  1. Barker, I. K. & Parrish, C. R. ( 2001; ). Parvovirus infections. In Infectious Diseases of Wildlife Mammals, 3rd edn, pp. 131–146. Edited by E. S. Williams & I. K. Barker. London: Manson.
  2. Begon, M., Hazel, S. M., Telfer, S., Bown, K., Carslake, D., Cavanagh, R., Chantrey, J., Jones, T. & Bennett, M. ( 2003; ). Rodents, cowpox virus and islands: densities, numbers and thresholds. J Anim Ecol 72, 343–355.[CrossRef]
    [Google Scholar]
  3. Bernshtein, A. D., Apekina, N. S., Mikhailova, T. V., Myasnikov, Y. A., Khlyap, L. A., Korotkov, Y. S. & Gavrilovskaya, I. N. ( 1999; ). Dynamics of Puumala hantavirus infection in naturally infected bank voles (Clethrionomys glareolus). Arch Virol 144, 2415–2428.[CrossRef]
    [Google Scholar]
  4. Botten, J., Mirowsky, K., Ye, C., Gottlieb, K., Saavedra, M., Ponce, L. & Hjelle, B. ( 2002; ). Shedding and intracage transmission of Sin Nombre hantavirus in the deer mouse (Peromyscus maniculatus) model. J Virol 76, 7587–7594.[CrossRef]
    [Google Scholar]
  5. Brummer-Korvenkontio, M., Vaheri, A., Hovi, T., von Bonsdorff, C.-H., Vuorimies, J., Manni, T., Penttinen, K., Oker-Blom, N. & Lähdevirta, J. ( 1980; ). Nephropathia epidemica: detection of antigen in bank voles and serologic diagnosis of human infection. J Infect Dis 141, 131–134.[CrossRef]
    [Google Scholar]
  6. Compton, S. R., Jacoby, R. O., Paturzo, F. X. & Smith, A. L. ( 2004; ). Persistent Seoul virus infection in Lewis rats. Arch Virol 149, 1325–1339.
    [Google Scholar]
  7. Crance, J. M., Gantzer, C., Schwartzbrod, L. & Deloince, R. ( 1998; ). Effect of temperature on the survival of hepatitis A virus and its capsidal antigen in synthetic seawater. Environ Toxicol Water Qual 13, 89–92.[CrossRef]
    [Google Scholar]
  8. Escutenaire, S., Chalon, P., Verhagen, R., Heyman, P., Thomas, I., Karelle-Bui, L., Avsic-Zupanc, T., Lundkvist, Å. & Plyusnin, A. ( 2000; ). Spatial and temporal dynamics of Puumala hantavirus infection in red bank vole (Clethrionomys glareolus) populations in Belgium. Virus Res 67, 91–107.[CrossRef]
    [Google Scholar]
  9. Escutenaire, S., Chalon, P., De Jaegere, F., Karelle-Bui, L., Mees, G., Brochier, B., Rozenfeld, F. & Pastoret, P. ( 2002; ). Behavioral, physiologic, and habitat influences on the dynamics of Puumala virus infection in bank voles (Clethrionomys glareolus). Emerg Infect Dis 8, 930–936.[CrossRef]
    [Google Scholar]
  10. Gavrilovskaya, I. N., Apekina, N. S., Bernshtein, A. D., Demina, V. T., Okulova, N. M., Myasnikov, Y. A. & Chumakov, M. P. ( 1990; ). Pathogenesis of hemorrhagic fever with renal syndrome virus infection and mode of horizontal transmission of hantavirus in bank voles. Arch Virol Suppl 1, 57–62.
    [Google Scholar]
  11. Hanski, I., Henttonen, H. & Hansson, L. ( 1994; ). Temporal variability and geographical patterns in the population density of microtine rodents: a reply to Xia and Boonstra. Am Nat 144, 329–342.[CrossRef]
    [Google Scholar]
  12. Hansson, L. & Henttonen, H. ( 1988; ). Rodent dynamics as community processes. Trends Ecol Evol 3, 195–200.[CrossRef]
    [Google Scholar]
  13. Hinson, E. R., Shone, S. M., Zink, M. C., Glass, G. E. & Klein, S. L. ( 2004; ). Wounding: the primary mode of Seoul virus transmission among male Norway rats. Am J Trop Med Hyg 70, 310–317.
    [Google Scholar]
  14. Hutchinson, K. L., Rollin, P. E. & Peters, C. J. ( 1998; ). Pathogenesis of a North American hantavirus, Black Creek Canal virus, in experimentally infected Sigmodon hispidus. Am J Trop Med Hyg 59, 58–65.
    [Google Scholar]
  15. Johnson, K. M. ( 1989; ). Laboratory safety. In Manual of Hemorrhagic Fever with Renal Syndrome, 1st edn, pp. 109–110. Edited by H. Lee & J. Dalrymple. Seoul: WHO Collaborating Center for Virus Reference and Research.
  16. Kariwa, H., Fujiki, M., Yoshimatsu, K., Arikawa, J., Takashima, I. & Hashimoto, N. ( 1998; ). Urine-associated horizontal transmission of Seoul virus among rats. Arch Virol 143, 365–374.[CrossRef]
    [Google Scholar]
  17. Klein, S. L., Bird, B. H. & Glass, G. E. ( 2000; ). Sex differences in Seoul virus infection are not related to adult sex steroid concentrations in Norway rats. J Virol 74, 8213–8217.[CrossRef]
    [Google Scholar]
  18. Klein, S. L., Bird, B. H. & Glass, G. E. ( 2001; ). Sex differences in immune responses and viral shedding following Seoul virus infection in Norway rats. Am J Trop Med Hyg 65, 57–63.
    [Google Scholar]
  19. Klein, S. L., Zink, M. C. & Glass, G. E. ( 2004; ). Seoul virus infection increases aggressive behaviour in male Norway rats. Anim Behav 67, 421–429.[CrossRef]
    [Google Scholar]
  20. Klingström, J., Maljkovic, I., Zuber, B., Rollman, E., Kjerrstrom, A. & Lundkvist, Å. ( 2004; ). Vaccination of C57/BL6 mice with Dobrava hantavirus nucleocapsid protein in Freund's adjuvant induced partial protection against challenge. Vaccine 22, 4029–4034.[CrossRef]
    [Google Scholar]
  21. Lee, H. W., Lee, P. W., Baek, L. J., Song, C. K. & Seong, I. W. ( 1981; ). Intraspecific transmission of Hantaan virus, etiologic agent of Korean hemorrhagic fever, in the rodent Apodemus agrarius. Am J Trop Med Hyg 30, 1106–1112.
    [Google Scholar]
  22. Lundkvist, Å., Kallio-Kokko, H., Sjölander, K. B., Lankinen, H., Niklasson, B., Vaheri, A. & Vapalahti, O. ( 1996; ). Characterization of Puumala virus nucleocapsid protein: identification of B-cell epitopes and domains involved in protective immunity. Virology 216, 397–406.[CrossRef]
    [Google Scholar]
  23. Lundkvist, Å., Cheng, Y., Sjölander, K. B., Niklasson, B., Vaheri, A. & Plyusnin, A. ( 1997; ). Cell culture adaptation of Puumala hantavirus changes the infectivity for its natural reservoir, Clethrionomys glareolus, and leads to accumulation of mutants with altered genomic RNA S segment. J Virol 71, 9515–9523.
    [Google Scholar]
  24. Meyer, B. J. & Schmaljohn, C. S. ( 2000; ). Persistent hantavirus infections: characteristics and mechanisms. Trends Microbiol 8, 61–67.[CrossRef]
    [Google Scholar]
  25. Niklasson, B., Hörnfeldt, B., Lundkvist, Å., Bjorsten, S. & Leduc, J. ( 1995; ). Temporal dynamics of Puumala virus antibody prevalence in voles and of nephropathia epidemica incidence in humans. Am J Trop Med Hyg 53, 134–140.
    [Google Scholar]
  26. Nuzum, E. O., Rossi, C. A., Stephenson, E. H. & LeDuc, J. W. ( 1988; ). Aerosol transmission of Hantaan and related viruses to laboratory rats. Am J Trop Med Hyg 38, 636–640.
    [Google Scholar]
  27. Olsson, G. E., White, N., Ahlm, C., Elgh, F., Verlemyr, A. C., Juto, P. & Palo, R. T. ( 2002; ). Demographic factors associated with hantavirus infection in bank voles (Clethrionomys glareolus). Emerg Infect Dis 8, 924–929.[CrossRef]
    [Google Scholar]
  28. Padula, P., Figueroa, R., Navarrete, M. & 7 other authors ( 2004; ). Transmission study of Andes hantavirus infection in wild Sigmodontine rodents. J Virol 78, 11972–11979.[CrossRef]
    [Google Scholar]
  29. Plyusnin, A., Vapalahti, O., Lankinen, H. & 9 other authors ( 1994; ). Tula virus: a newly detected hantavirus carried by European common voles. J Virol 68, 7833–7839.
    [Google Scholar]
  30. Plyusnin, A., Hörling, J. & Kanerva, M. & 10 other authors ( 1997; ). Puumala hantavirus genome in patients with nephropathia epidemica: correlation of PCR positivity with HLA haplotype and link to viral sequences in local rodents. J Clin Microbiol 35, 1090–1096.
    [Google Scholar]
  31. Prévot-Julliard, A.-C., Henttonen, H., Yoccoz, N. G. & Stenseth, N. C. ( 1999; ). Delayed maturation in female bank voles: optimal decision or social constraint? J Anim Ecol 68, 684–697.[CrossRef]
    [Google Scholar]
  32. Sauvage, F., Langlais, M., Yoccoz, N. G. & Pontier, D. ( 2003; ). Modelling hantavirus in fluctuating populations of bank voles: the role of indirect transmission on virus persistence. J Anim Ecol 72, 1–13.[CrossRef]
    [Google Scholar]
  33. Schmaljohn, C., Huggins, J. & Calisher, C. H. ( 1998; ). Laboratory and field safety. In Manual of Hemorrhagic Fever with Renal Syndrome and Hantavirus Pulmonary Syndrome, 2nd edn, pp. 192–198. Edited by C. Schmaljohn, C. H. Calisher & H. W. Lee. Seoul: WHO Collaborating Center for Virus Reference and Research (Hantaviruses) Asian Institute for Life Sciences.
  34. Stallknecht, D. E., Kearney, M. T., Shane, S. M. & Zwank, P. J. ( 1990; ). Effects of pH, temperature, and salinity on persistence of avian influenza viruses in water. Avian Dis 34, 412–418.[CrossRef]
    [Google Scholar]
  35. Thomson, G. R., Vosloo, W. & Bastos, A. D. S. ( 2003; ). Foot and mouth disease in wildlife. Virus Res 91, 145–161.[CrossRef]
    [Google Scholar]
  36. Vapalahti, O., Kallio-Kokko, H., Salonen, E.-M., Brummer-Korvenkontio, M. & Vaheri, A. ( 1992; ). Cloning and sequencing of Puumala virus Sotkamo strain S and M RNA segments: evidence for strain variation in hantaviruses and expression of the nucleocapsid protein. J Gen Virol 73, 829–838.[CrossRef]
    [Google Scholar]
  37. Vapalahti, O., Kallio-Kokko, H., Närvänen, A., Julkunen, I., Lundkvist, Å., Plyusnin, A., Lehväslaiho, H., Brummer-Korvenkontio, M. & Vaheri, A. ( 1995; ). Human B-cell epitopes of Puumala virus nucleocapsid protein, the major antigen in early serological response. J Med Virol 46, 293–303.[CrossRef]
    [Google Scholar]
  38. Vapalahti, O., Lundkvist, Å. & Kukkonen, S. K. & 10 other authors ( 1996; ). Isolation and characterization of Tula virus, a distinct serotype in the genus Hantavirus, family Bunyaviridae. J Gen Virol 77, 3063–3067.[CrossRef]
    [Google Scholar]
  39. Vapalahti, O., Lundkvist, A. & Fedorov, V. & 11 other authors ( 1999; ). Isolation and characterization of a hantavirus from Lemmus sibiricus: evidence for host switch during hantavirus evolution. J Virol 73, 5586–5592.
    [Google Scholar]
  40. Vapalahti, O., Mustonen, J., Lundkvist, A., Henttonen, H., Plyusnin, A. & Vaheri, A. ( 2003; ). Hantavirus infections in Europe. Lancet Infect Dis 3, 653–661.[CrossRef]
    [Google Scholar]
  41. Verhagen, R., Leirs, H., Tkachenko, E. & van der Groen, G. ( 1986; ). Ecological and epidemiological data on hantavirus in bank vole populations in Belgium. Arch Virol 91, 193–205.[CrossRef]
    [Google Scholar]
  42. Verhagen, R., van der Groen, G., Ivanov, A., van Rompaey, J., Leirs, H. & Verheyen, W. ( 1987; ). Occurrence and distribution of hantavirus in wild living mammals in Belgium. Acta Virol 31, 43–52.
    [Google Scholar]
  43. Woods, L. W. ( 2001; ). Adenoviral diseases. In Infectious Diseases of Wildlife Mammals, 3rd edn, pp. 202–212. Edited by E. S. Williams & I. K. Barker. London: Manson.
  44. Yanagihara, R., Amyx, L. & Gajdusek, D. C. ( 1985; ). Experimental infection with Puumala virus, the etiologic agent of nephropathia epidemica, in bank voles (Clethrionomys glareolus). J Virol 55, 34–38.
    [Google Scholar]
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