Virus Genes

, Volume 30, Issue 2, pp 157–180 | Cite as

New Ecological Aspects of Hantavirus Infection: A Change of A Paradigm and a Challenge of Prevention- A Review

  • Martin Zeier
  • Michaela Handermann
  • Udo Bahr
  • Baldur Rensch
  • Sandra Müller
  • Roland Kehm
  • Walter Muranyi
  • Gholamreza Darai


In the last decades a significant number of so far unknown or underestimated pathogens have emerged as fundamental health hazards of the human population despite intensive research and exceptional efforts of modern medicine to embank and eradicate infectious diseases. Almost all incidents caused by such emerging pathogens could be ascribed to agents that are zoonotic or expanded their host range and crossed species barriers. Many different factors influence the status of a pathogen to remain unnoticed or evolves into a worldwide threat. The ability of an infectious agent to adapt to changing environmental conditions and variations in human behavior, population development, nutrition, education, social, and health status are relevant factors affecting the correlation between pathogen and host. Hantaviruses belong to the emerging pathogens having gained more and more attention in the last decades. These viruses are members of the family Bunyaviridae and are grouped into a separate genus known as Hantavirus. The serotypes Hantaan (HTN), Seoul (SEO), Puumala (PUU), and Dobrava (DOB) virus predominantly cause hemorrhagic fever with renal syndrome (HFRS), a disease characterized by renal failure, hemorrhages, and shock. In the recent past, many hantavirus isolates have been identified and classified in hitherto unaffected geographic regions in the New World (North, Middle, and South America) with characteristic features affecting the lungs of infected individuals and causing an acute pulmonary syndrome. Hantavirus outbreaks in the United States of America at the beginning of the 10th decade of the last century fundamentally changed our knowledge about the appearance of the hantavirus specific clinical picture, mortality, origin, and transmission route in human beings. The hantavirus pulmonary syndrome (HPS) was first recognized in 1993 in the Four Corners Region of the United States and had a lethality of more than 50%. Although the causative virus was first termed in connection with the geographic name of its outbreak region the analysis of the individual viruses indicate that the causing virus of HPS was a genetically distinct hantavirus and consequently termed as Sin Nombre virus. Hantaviruses are distributed worldwide and are assumed to share a long time period of co-evolution with specific rodent species as their natural reservoir. The degree of relatedness between virus serotypes normally coincides with the relatedness between their respective hosts. There are no known diseases that are associated with hantavirus infections in rodents underlining the amicable relationship between virus and host developed by mutual interaction in hundreds of thousands of years. Although rodents are the major reservoir, antibodies against hantaviruses are also present in domestic and wild animals like cats, dogs, pigs, cattle, and deer. Domestic animals and rodents live jointly in a similar habitat. Therefore the transmission of hantaviruses from rodents to domestic animals seems to be possible, if the target organs, tissues, and cell parenchyma of the co-habitat domestic animals possess adequate virus receptors and are suitable for hantavirus entry and replication. The most likely incidental infection of species other than rodents as for example humans turns hantaviruses from harmless to life-threatening pathogenic agents focusing the attention on this virus group, their ecology and evolution in order to prevent the human population from a serious health risk. Much more studies on the influence of non-natural hosts on the ecology of hantaviruses are needed to understand the directions that the hantavirus evolution could pursue. At least, domestic animals that share their environmental habitat with rodents and humans particularly in areas known as high endemic hantavirus regions have to be copiously screened. Each transfer of hantaviruses from their original natural hosts to other often incidental hosts is accompanied by a change of ecology, a change of environment, a modulation of numerous factors probably influencing the pathogenicity and virulence of the virus. The new environment exerts a modified evolutionary pressure on the virus forcing it to adapt and probably to adopt a form that is much more dangerous for other host species compared to the original one.


bovine aortic endothelial cell Bunyaviridae ecology Hantaan virus hantavirus Hemorrhagic fever with renal syndrome Puumala virus 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Schmaljohn, C.S., Dalrymple, J.M. 1983Virology131482491Google Scholar
  2. van Regenmortel M.H.V., Fauquet C.M., Bishop D.H.L., Carstens E.B., Estes M.K., Lemon S.M., Maniloff J., Mayo M.A., McGeoch D.J., Pringle C.R., and Wickner R.B., Virus Taxonomy. Seventh Report of the International Committee on Taxonomy of Viruses. Academic Press, San Diego, San Francisco, New York, Boston, London, Sydney, Tokyo, 2000.Google Scholar
  3. Tidona C.A. and Darai G., The Springer Index of Viruses. Springer-Verlag, Berlin, Heidelberg, New York, 2002.Google Scholar
  4. Lee, H.W., Lee, P.W., Johnson, K.M. 1978J Infect Dis137298308PubMedGoogle Scholar
  5. Lee, H.W., Lee, P.W., Baek, L.J., Chu, Y.K. 1990Arch Virol1 Suppl.518Google Scholar
  6. Myhrman, G. 1951Acta Med Scand1405256Google Scholar
  7. Fjellstrom, K.E. 1960Acta Med Scand167111120Google Scholar
  8. Niklasson, B.S. 1992Pediatr Nephrol6201204Google Scholar
  9. Vanhille, P., Binaut, R., Kyndt, X., Launay, D., Thomas, C., Fleury, D. 2001Nephrologie22301305Google Scholar
  10. Olsson, G.E., Dalerum, F., Hornfeldt, B., Elgh, F., Palo, T.R., Juto, P., Ahlm, C. 2003Emerg Infect Dis913951401Google Scholar
  11. van Yperselede Strihou, C., van der Groen, G., Desmyter, J. 1986Adv Nephrol Necker Hosop15143172Google Scholar
  12. Zeier, M., Andrassy, K., Waldherr, R., Ritz, E. 1986Dtsch Med Wochenschr111207210Google Scholar
  13. Clement, J., Heyman, P., McKenna, P., Colson, P., Avsic-Zupanc, T. 1997Emerg Infect Dis3205211Google Scholar
  14. Settergren, B. 1991Rev Infect Dis13736744Google Scholar
  15. Zeier, M., Zoller, L., Weinreich, T., Padberg-Wolf, E., Andrassy, K., Ritz, E. 1992Clin Nephrol38190192Google Scholar
  16. Papa, A., Antoniadis, A., Eur, J 2001Epidemiol17189194Google Scholar
  17. Linderholm, M., Elgh, F. 2001Curr Top Microbiol Immunol256135151Google Scholar
  18. Vapalahti,  O., Mustonen, J., Lundkvist, A., Henttonen, H., Plyusnin, A., Vaheri, A. 2003Lancet Infect Dis3653661CrossRefPubMedGoogle Scholar
  19. Slonova, R.A., Astakhova, T.I., Kompanets, G.G. 1997Zh Mikrobiol Epidemiol Immunobiol597101Google Scholar
  20. Miyamoto, H., Kariwa, H., Araki, K., Lokugamage, K., Hayasaka, D., Cui, B.Z., Lokugamage, N., Ivanov, L.I., Mizutani, T., Iwasa, M.A., Yoshimatsu, K., Arikawa, J., Takashima, I. 2003Arch Virol14815431556Google Scholar
  21. Nichol, S.T., Spiropoulou, C.F., Morzunov, S., Rollin, P.E., Ksiazek, T.G., Feldmann, H., Sanchez, A., Childs, J., Zaki, S., Peters, C.J. 1993Science262914917Google Scholar
  22. Feldmann, H., Sanchez, A., Morzunov, S., Spiropoulou, C.F., Rollin, P.E., Ksiazek, T.G., Peters, C.J., Nichol, S.T. 1993Virus Res30351367Google Scholar
  23. Hjelle, B., Chavez-Giles, F., Torrez-Martinez, N., Yates, T., Sarisky, J., Webb, J., Ascher, M. 1994J Virol6867516754Google Scholar
  24. Hjelle, B., Anderson, B., Torrez-Martinez, N., Song, W., Gannon, W.L., Yates, T.L. 1995Virology207452459Google Scholar
  25. Hjelle, B., Krolikowski, J., Torrez-Martinez, N., Chavez-Giles, F., Vanner, C., Laposata, E. 1995J Med Virol462127Google Scholar
  26. Hjelle, B., Lee, S.W., Song, W., Torrez-Martinez, N., Song, J.W., Yanagihara, R., Gavrilovskaya, I., Mackow, E.R. 1995J Virol6981378141Google Scholar
  27. Khan, A.S., Khabbaz, R.F., Armstrong, L.R., Holman, R.C., Bauer, S.P., Graber, J., Strine, T., Miller, G., Reef, S., Tappero, J., Rollin, P.E., Nichol, S.T., Zaki, S.R., Bryan, R.T., Chapman, L.E., Peters, C.J., Ksiazek, T.G. 1996J Infect Dis17312971331Google Scholar
  28. Chizhikov, V.E., Spiropoulou, C.F., Monroe, M.C., Peters, C.J, Nichol, S.T., Morzunov, S.P. 1995J Virol6981328136Google Scholar
  29. Gavrilovskaya, I., La Monica, R., Fay, M.E., Hjelle, B., Schmaljohn, C., Shaw, R., Mackow, E.R. 1999J Clin Microbiol37122126Google Scholar
  30. Iversson, L.B., da Rosa, A.P., Rosa, M.D., Lomar, A.V., Sasaki Mda, G., LeDuc, J.W. 1994Rev Assoc Med Bras408592PubMedGoogle Scholar
  31. Hjelle, B., Torrez-Martinez, N., Koster, F.T. 1996Lancet34757Google Scholar
  32. Weissenbacher, M., Cura, E., Segura, E.L., Hortal, M., Baek, L.J., Chu, Y.K., Lee, H.W. 1996Medicina561722Google Scholar
  33. Bharadwaj, M., Botten, J., Torrez-Martinez, N., Hjelle, B. 1997Am J Trop Med Hyg57368374Google Scholar
  34. da Silva M.V., Vasconcelos M.J., Hidalgo N.T., Veiga A.P., Canzian M., Marotto P.C., and de Lima V.C., Rev Inst Med Trop Sao Paulo 39, 231–234, 1997.Google Scholar
  35. Johnson, A.M., Bowen, M.D., Ksiazek, T.G., Williams, R.J., Bryan, R.T., Mills, J.N., Peters, C.J., Nichol, S.T. 1997Virology238115127Google Scholar
  36. Levis, S., Morzunov, S.P., Rowe, J.E., Enria, D., Pini, N., Calderon, G., Sabattini, M., St Jeor, S. 1998J Infect Dis177529538Google Scholar
  37. Ferrer, J.F., Jonsson, C.B., Esteban, E., Galligan, D., Basombrio, M.A., Peralta-Ramos, M., Bharadwaj, M., Torrez-Martinez, N., Callahan, J., Segovia, A., Hjelle, B. 1998Am J Trop Med Hyg59438444Google Scholar
  38. Levis, S., Rowe, J.E., Morzunov, S., Enria, D.A., Jeor, S. 1997St Lancet349998999Google Scholar
  39. Malecki, T.M., Jillson, G.P., Thilsted, J.P., Elrod, J., Torres-Martinez, N., Hjelle, B. 1998J Am Vet Med Assoc212970973Google Scholar
  40. Espinoza, R., Vial, P., Noriega, L.M., Johnson, A., Nichol, S.T., Rollin, P.E., Wells, R., Zaki, S., Reynolds, E., Ksiazek, T.G. 1998Emerg Infect Dis49395Google Scholar
  41. Padula, P.J., Edelstein, A., Miguel, S.D., Lopez, N.M., Rossi, C.M., Rabinovich, R.D. 1998Virology241323330Google Scholar
  42. Calderon, G., Pini, N., Bolpe, J., Levis, S., Mills, J., Segura, E., Guthmann, N., Cantoni, G., Becker, J., Fonollat, A., Ripoll, C., Bortman, M., Benedetti, R. 1999Emerg Infect Dis5792797Google Scholar
  43. Johnson, A.M., de Souza, L.T., Ferreira, I.B. 1999J Med Virol59527535Google Scholar
  44. Vincent, M.J., Quiroz, E., Gracia, F., Sanchez, A.J., Ksiazek, T.G., Kitsutani, P.T., Ruedas, L.A., Tinnin, D.S., Caceres, L., Garcia, A., Rollin, P.E., Mills, J.N., Peters, C.J., Nichol, S.T. 2000Virology2771419Google Scholar
  45. Yahnke, C.J., Meserve, P.L., Ksiazek, T.G., Mills, J.N. 2001Am J Trop Med Hyg65768776Google Scholar
  46. Bohlman,  M.C., Morzunov, S.P., Meissner, J., Taylor, M.B., Ishibashi, K., Rowe, J., Levis, S., Enria, D., Jeor, S.C. 2002St J Virol7637653773Google Scholar
  47. Gonzalez Della Valle, M., Edelstein, A., Miguel, S., Martinez, V., Cortez, J., Cacace, M.L., Jurgelenas, G., Estani, S.S., Padula, P. 2002Am J Trop Med Hyg66713720Google Scholar
  48. Galeno, H., Mora, J., Villagra, E., Fernandez, J., Hernandez, J., Mertz, G.J., Ramirez, E. 2002Emerg Infect Dis8657661Google Scholar
  49. Delfraro, A., Clara, M., Tome, L., Achaval, F., Levis, S., Calderon, G., Enria, D., Lozano, M., Russi, J., Arbiza, J. 2003Emerg Infect Dis9846852Google Scholar
  50. Chu, Y.K., Owen, R.D., Gonzalez, L.M., Jonsson, C.B. 2003Am J Trop Med Hyg69263268Google Scholar
  51. Torres-Perez, F., Navarrete-Droguett, J., Aldunate, R., Yates, T.L., Mertz, G.J., Vial, P.A., Ferres, M., Marquet, P.A., Palma, R.E. 2004Am J Trop Med Hyg70305309Google Scholar
  52. Williams E.C. and Barker I.K. (eds), Infectious Diseases of Wild Mammals. 3rd edn, Iowa State University Press, Ames, 2001, pp. 254–270.Google Scholar
  53. Mills, J.N., Ksiazek, T.G., Ellis, B.A., Rollin, P.E., Nichol, S.T., Yates, T.L., Gannon, W.L., Levy, C.E., Engelthaler, D.M., Davis, T., Tanda, D.T., Frampton, J.W., Nichols, C.R., Peters, C.J., Childs, J.E. 1997Am J Trop Med Hyg56273284Google Scholar
  54. Williams, E.S., Yuill, T., Artois, M., Fischer, J., Haigh, S.A. 2002Rev Sci Tech21139157Google Scholar
  55. Nowotny, N., Weissenboeck, H., Aberle, S., Hinterdorfer, F. 1994JAMA27211001101Google Scholar
  56. Stallknecht D.E., Blue J.L., Rollor E.A. III, Nettles V.F., Davidson W.R., and Pearson J.E., J Wildl Dis 27, 238–247, 1991.Google Scholar
  57. Pejcoch,  M., Danes, L., Zahradkova, S., Pekna, E. 1992Cesk Epidemiol Mikrobiol Immunol4192100Google Scholar
  58. Danes,  L., Pejcoch, M., Bukovjan, K., Veleba, J., Halackova, M. 1992Cesk Epidemiol Mikrobiol Immunol411518Google Scholar
  59. Vapalahti, O., Lundkvist, A., Fedorov, V., Conroy, C.J., Hirvonen, S., Plyusnina, A., Nemirov, K., Fredga, K., Cook, J.A., Niemimaa, J., Kaikusalo, A., Henttonen, H., Vaheri, A., Plyusnin, A. 1999J Virol7355865592Google Scholar
  60. McCaughey,  C., Hart, C.A. 2000J Med Microbiol49587589Google Scholar
  61. Xiao, S.Y., Liang, M., Schmaljohn, C.S. 1993J Gen Virol7416571659Google Scholar
  62. Kariwa, H., Isegawa, Y., Arikawa, J., Takashima, I., Ueda, S., Yamanishi, K., Hashimoto, N. 1994Virus Res332738Google Scholar
  63. Antic, D., Lim, B.U., Kang, C.Y. 1991Virus Res195965Google Scholar
  64. Antic, D., Lim, B.U., Kang, C.Y. 1991Virus Res194758Google Scholar
  65. Horling, J., Chizhikov, V., Lundkvist, A., Jonsson, M., Ivanov, L., Dekonenko, A., Niklasson, B., Dzagurova, T., Peters, C.J., Tkachenko, E., Nichol, S. 1996J Gen Virol77687694Google Scholar
  66. Xiao, S.Y., Leduc, J.W., Chu, Y.K., Schmaljohn, C.S. 1994Virology198205217Google Scholar
  67. Stohwasser, R., Giebel, L.B., Zoller, L., Bautz, E.K., Darai, G. 1990Virology1747986Google Scholar
  68. Giebel, L.B., Stohwasser, R., Zoller, L., Bautz, E.K., Darai, G. 1989Virology172498505Google Scholar
  69. Stohwasser, R., Raab, K., Darai, G., Bautz, E.K. 1991Virology183386391Google Scholar
  70. Hjelle, B., Glass, G.E. 2000J Infect Dis18115691573Google Scholar
  71. Avsic-Zupanc, T., Xiao, S.Y., Stojanovic, R., Gligic, A., van der Groen, G., LeDuc, J.W. 1992Med Virol38132137Google Scholar
  72. Scharninghausen, J.J., Meyer, H., Pfeffer, M., Davis, D.S. 1999Emerg Infect Dis5468470Google Scholar
  73. Klempa, B., Schmidt, H.A., Ulrich, R., Kaluz, S., Labuda, M., Meisel, H., Hjelle, B., Krüger, D.H. 2003J Virol77804809Google Scholar
  74. Sibold, C., Ulrich, R., Labuda, M., Lundkvist, A., Martens, H., Schütt, M., Gerke, P., Leitmeyer, K., Meisel, H., Krüger, D.H. 2001J Med Virol63158167Google Scholar
  75. Nemirov, K., Vapalahti, O., Papa, A., Plyusnina, A., Lundkvist, A., Antoniadis, A., Vaheri, A., Plyusnin, A. 2003J Med Virol69408416Google Scholar
  76. Nemirov, K., Andersen, H.K., Leirs, H., Henttonen, H., Vaheri, A., Lundkvist, A., Plyusnin, A. 2004J Clin Virol30254257Google Scholar
  77. Plyusnin, A., Cheng, Y., Vapalahti, O., Pejcoch, M., Unar, J., Jelinkova, Z., Lehvaslaiho, H., Lundkvist, A., Vaheri, A. 1995Virus Res39237250PubMedGoogle Scholar
  78. Vapalahti, O., Lundkvist, A., Kukkonen, S., Cheng, Y., Gilljam, M., Kanerva, M., Manni, T., Pejcoch, M., Niemimaa, J., Kaikusalo, A., Henttonen, H., Vaheri, A., Plyusnin, A 1996J Gen Virol7730633067Google Scholar
  79. Ravkov, E.V., Rollin, P.E., Ksiazek, T.G., Peters, C.J., Nichol, S.T. 1995Virology210482489Google Scholar
  80. Rodriguez, L.L., Owens, J.H., Peters, C.J., Nichol, S.T. 1998Virology24299106Google Scholar
  81. Parrington, M.A., Kang, C.Y. 1990Virology175167175Google Scholar
  82. Parrington, M.A., Lee, P.W., Kang, C.Y. 1991J Gen Virol7218451854Google Scholar
  83. Song, W., Torrez-Martinez, N., Irwin, W., Harrison, F.J., Davis, R., Ascher, M., Jay, M., Hjelle, B. 1995J Gen Virol7631953199Google Scholar
  84. Morzunov, S., Feldmann, H., Spiropoulou, C.F., Semenova, V.A., Rollin, P.E., Ksiazek, T.G., Peters, C.J., Nichol, S.T. 1995J Virol6919801983Google Scholar
  85. Torrez-Martinez, N., Hjelle, B. 1983Lancet346780781Google Scholar
  86. Torrez-Martinez, N., Song, W., Hjelle, B. 1995Virology211336338Google Scholar
  87. Song, J.W., Baek, L.J., Nagle, J.W., Schlitter, D., Yanagihara, R. 1996Arch Virol141959967Google Scholar
  88. Rawlings, J.A., Torrez-Martinez, N., Neill, S.U., Moore, G.M., Hicks, B.N., Pichuantes, S., Nguyen, A., Bharadwaj, M., Hjelle, B. 1996Am J Trop Med Hyg55672679Google Scholar
  89. Sanchez, A.J., Abbott, K.D., Nichol, S.T. 2001Virology286345353Google Scholar
  90. López, N., Padula, P., Rossi, C., Miguel, S., Edelstein, A., Ramírez, E., Franze-Fernández, M.T. 1997Virus Res507784Google Scholar
  91. Meissner, J.D., Rowe, J.E., Borucki, M.K., St. Jeor, S.C. 2002 Virus Res89131143Google Scholar
  92. Fulhorst C.F., Monroe M.C., Salas R.A., Duno G., Utrera A., Ksiazek T.G., Nichol S.T., de Manzione N.M., Tovar D., and Tesh R.B., Virus Res 51, 159–171, 1997.Google Scholar
  93. Caramello, P., Canta, F., Bonino, L., Moiraghi, C., Navone, F., Lipani, F., Balbiano, R., Caputo, A.M., Gai, V. 2002J Travel Med9326329Google Scholar
  94. Gajdusek, D.C. 1982Scand J Infect Dis Suppl3696108Google Scholar
  95. Gonzalez, J.P., McCormick, J.B., Baudon, D., Gautun, J.P., Meunier, D.Y., Dournon, E., Georges, A.J. 1984Lancet210361037Google Scholar
  96. Gonzalez, J.P., Mathiot, C.C., Bouquety, J.C., Diemer, J.M., Guerre, L., Lesborder, J.L., Madelon, M.C., Georges, A.J. 1988Ann Inst Pasteur Virol139301304Google Scholar
  97. Gavrilovskaya, I.N., Brown, E.J., Ginsberg, M.H., Mackow, E.R. 1999J Virol7339513959Google Scholar
  98. Cheresh D. A., Proc Natl Acad Sci 84, 6471–6475, 1987.Google Scholar
  99. Hynes, R.O. 1992Cell691125CrossRefPubMedGoogle Scholar
  100. Temonen, M., Mustonen, J., Helin, H., Pasternack, A., Vaheri, A., Holthofer, H. 1996Clin Immunol Immunopathol784755Google Scholar
  101. Xu, Z.Y., Tang, Y.W., Kann, L.Y., Tsai, T.F., Am, J 1987Epidemiol126942948Google Scholar
  102. Tokarevich N., Stoyanova N., Kozhukhova E., Makarova G., Volkova G., and Khnykin A., Epi North 2, 1, 2001.Google Scholar
  103. Tkachenko, E.A., Lee, H.W. 1991Kidney Int Suppl355461Google Scholar
  104. Leighton, F.A., Artsob, H.A., Chu, M.C., Olson, J.G., Can, J 2001Public Health926771Google Scholar
  105. Bennett, M., Lloyd, G., Jones, N., Brown, A., Trees, A.J., McCracken, C., Smyth, N.R., Gaskell, C.J., Gaskell, R.M. 1990Vet Rec127548549Google Scholar
  106. Nowotny N., Lancet 343, 921, 1994.Google Scholar
  107. Nowotny, N. 1996Zentralbl Hyg Umweltmed198452461Google Scholar
  108. Mills, J.N., Johnson, J.M., Ksiazek, T.G., Ellis, B.A., Rollin, P.E., Yates, T.L., Mann, M.O., Johnson, M.R., Campbell, M.L., Miyashiro, J., Patrick, M., Zyzak, M., Lavender, D., Novak, M.G., Schmidt, K., Peters, C.J., Childs, J.E. 1998AmJ Trop Med Hyg58525532Google Scholar
  109. Klingstrom, J., Plyusnin, A., Vaheri, A., Lundkvist, A. 2002J Virol76444449Google Scholar
  110. Ahlm, C., Wallin, K., Lundkvist, A., Elgh, F., Juto, P., Merza, M., Tarnvik, A. 2000Am J Trop Med Hyg62106111Google Scholar
  111. Vahlenkamp, M., Muller, T., Tackmann, K., Loschner, U., Schmitz, H., Schreiber, M. 1998Virus Res57139150Google Scholar
  112. Arikawa, J., Ito, M., Yao, J.S., Kariwa, H., Takashima, I., Hashimoto, N. 1994J Vet Med Sci562732Google Scholar
  113. Zhang, Y., Li, X., Tang, J. 1995Zhonghua Yu Fang Yi Xue Za Zhi29344347Google Scholar
  114. Schmaljohn, C., Hjelle, B. 1997Emerg Infect Dis395104PubMedGoogle Scholar
  115. Center for Food Security and Public Health. Home page. <>. Accessed 2004 July 9.Google Scholar
  116. NMNH Department of Systematic Biology, Division of Mammals–Mammal Species of the World Home Page. Home page. <>. Accessed 2004 July 9.Google Scholar
  117. Nuzum, E.O., Rossi, C.A., Stephenson, E.H., LeDuc, J.W., Am, J 1988Trop Hyg38636640Google Scholar
  118. Muranyi, W., Kehm, R., Bahr, U., Müller, S., Handermann, M., Darai, G., Zeier, M. 2004Virology318112122Google Scholar
  119. Bahr, U., Muranyi, W., Müller, S., Kehm, R., Handermann, M., Darai, G., Zeier, M. 2004Virology32117Google Scholar
  120. Ruo, S.L., Li, Y.L., Tong, Z., Ma, Q.R., Liu, Z.L., Tang, Y.W., Ye, K.L., McCormick, J.B., Fisher-Hoch, S.P., Xu, Z.Y. 1994J Infect Dis170527534Google Scholar
  121. Klingstrom, J., Heyman, P., Escutenaire, S., Sjolander, K.B., De Jeagere, F., Henttonen, H., Lundkvist, A. 2002J Med Virol68581588Google Scholar
  122. Lednicky, J.A. 2003Arch Pathol Lab Med1273035Google Scholar
  123. Brummer-Korvenkontio, M., Vaheri, A., Hovi, T., von Bonsdorff, C.-H., Vuorimies, J., Manni, T., Penttinen, K., Oker-Blom, N., Lähdevirta, J. 1980J Infect Dis141131134Google Scholar
  124. Klempa, B., Meisel, H., Rath, S., Bartel, J., Ulrich, R., Kruger, D.H. 2003J. Clin. Microbiol4148944897Google Scholar
  125. Hjelle B., Emerging Viruses Research Center. Home page. <>. Accessed 2004 July 9.Google Scholar
  126. Bridson, E., Br, J 2001Biomed Sci5816Google Scholar
  127. Harper T.K. Hantavirus: Description, Vector, Mechanisms, Symptoms, etc. Website. <>. Accessed 2004 July 9.Google Scholar
  128. Hentonnen H., and Kaikusalo A., in Stenseth N.C., and Inns R.A. (eds), The Biology of Lemmings, AcademicPress Inc., New York (NY), 1993, pp. 157–186.Google Scholar
  129. Stuhlfault, K. 1943Dtsch Med Wochenschr69, 439–443474477Google Scholar
  130. French, G.R., Foulke, R.S., Brand, O.A., Eddy, G.A., Lee, H.W., Lee, P.W. 1981Science21110461048Google Scholar
  131. Pon, E., McKee, K.T., Diniega, B.M., Merrell, B., Corwin, A., Ksiazek, T.G. 1990Am J Trop Med Hyg42612619Google Scholar
  132. Hawes, S., Seabolt, J.P. 2003Clin Lab Sci163942Google Scholar
  133. Elliott, L.H., Ksiazek, T.G., Rollin, P.E., Spiropoulou, C.F., Morzunov, S., Monroe, M., Goldsmith, C.S., Humphrey, C.D., Zaki, S.R., Krebs, J.W. 1994J.W. Am J Trop Med Hyg51102108Google Scholar
  134. Williams, R.J., Bryan, R.T., Mills, J.N., Palma, R.E., Vera, I., De Velasquez, F., Baez, E., Schmidt, W.E., Figueroa, R.E., Peters, C.J., Zaki, S.R., Khan, A.S., Ksiazek, T.G. 1997Am J Trop Med Hyg57274282Google Scholar
  135. Toro, J., Vega, J.D., Khan, A.S., Mills, J.N., Padula, P., Terry, W., Yadon, Z., Valderrama, R., Ellis, B.A., Pavletic, C., Cerda, R., Zaki, S., Shieh, W.J., Meyer, R., Tapia, M., Mansilla, C., Baro, M., Vergara, J.A., Concha, M., Calderon, G., Enria, D., Peters, C.J., Ksiazek, T.G. 1997Emerg Infect Dis4687694Google Scholar
  136. Mills J.N., and Childs J.E., in Williams E.C. and Barker I.K. (eds), Infectious Diseases of Wild Mammals, 3rd edn. Iowa State University Press, Ames, 2001, pp. 254–270.Google Scholar
  137. Padula, P.J., Sanchez, A.J., Edelstein, A., Nichol, S.T. 2002J Gen Virol8321172122Google Scholar
  138. Suarez, O.V., Cueto, G.R., Cavia, R., Gomez Villafane, I.E., Bilenca, D.N., Edelstein, A., Martinez, P., Miguel, S., Bellomo, C., Hodara, K., Padula, P.J., Busch, M. 2003Mem Inst Oswaldo Cruz98727732Google Scholar
  139. Pini, N., Levis, S., Calderon, G., Ramirez, J., Bravo, D., Lozano, E., Ripoll, C., St Jeor, S., Ksiazek, T.G., Barquez, R.M., Enria, D. 2003Emerg Infect Dis910701076Google Scholar
  140. Ferrer, J.F., Galligan, D., Esteban, E., Rey, V., Murua, A., Gutierrez, S., Gonzalez, L., Thakuri, M., Feldman, L., Poiesz, B., Jonsson, C. 2003Ann Trop Med Parasitol97269280Google Scholar
  141. Tang, Y.W., Xu, Z.Y., Zhu, Z.Y., Tsai, T.F. 1985Lancet1513514Google Scholar
  142. Pensiero, M.N., Sharefkin, J.B., Hay, J. 1992J Virol6659295936Google Scholar
  143. Davidovich, I.M. 1990Ter Arkh626871Google Scholar
  144. Kraus, A.A., Raftery, M.J., Giese, T., Ulrich, R., Zawatzky, R., Hippenstiel, S., Suttorp, N., Krüger, D.H., Schönrich, G. 2004J Virol7861436150Google Scholar
  145. Mackow, E.R., Gavrilovskaya, I.N. 2001Curr Top Microbiol Immunol25691115Google Scholar
  146. Raftery, M.J., Kraus, A.A., Ulrich, R., Krüger, D.H., Schönrich, G. 2002J Virol761072410733Google Scholar
  147. Mackow E.R., Ginsberg M.H., and Gavrilovskaya I.N., in Saluzzo J.F., and Dodet B. (eds), Factors in the Emergence and Control of Rodent-borne Viral Diseases (Hantaviral and Renal disease). Elsevier, Paris, 1999, pp. 113–123.Google Scholar
  148. Singh, B., Rawlings, N., Kaur, A. 2001Histol Histopathol1610371046Google Scholar
  149. LeDuc, J.W., Ksiazek, T.G., Rossi, C.A., Dalrymple, J.M. 1990J Infect Dis16211821184Google Scholar
  150. Avsic-Zupanc, T., Toney, A., Anderson, K., Chu, Y.K., Schmaljohn, C. 1995J Gen Virol7628012808Google Scholar
  151. Slonova, R.A., Tkachenko, E.A., Kushnarev, E.L., Dzagurova, T.K., Astakova, T.I. 1992Acta Virol36493Google Scholar
  152. Johnson, K.M., Lange, J.V., Webb, P.A., Murphy, F.A. 1977Lancet1569571Google Scholar
  153. Gonzalez, J.P., Josse, R., Johnson, E.D., Merlin, M., Georges, A.J. Abandja J., Danyod, M., Delaporte, E., Dupont, A., Ghogomu, A 1989Res Virol140319331Google Scholar
  154. Corwin, A., Habib, M., Olson, J., Scott, D., Ksiazek, T., Watts, D.M. 1992Trans R Soc Trop Med Hyg86677679Google Scholar
  155. Botros B.A., Sobh M., Wierzba T., Arthur R.R., Mohareb E.W., Frenck R., El Refaie A., Mahmoud I., Chapman G.D., and Graham R.R., Trans R Soc Trop Hyg 98, 331–336, 2004.Google Scholar
  156. Corwin, A., Habib, M., Watts, D., Darwish, M., Olson, J., Botros, B., Hibbs, R., Kleinosky, M., Lee, H.W., Shope, R., Kilpatrick, M. 1993Am J Trop Med Hyg48776783Google Scholar
  157. Rodier, G., Soliman, A.K., Bouloumie, J., Kremer, D. 1993Trans R Soc Trop Med Hyg87160161Google Scholar
  158. Nakounne, E., Selekon, B., Morvan, J. 2000Bull Soc Pathol Exot93340347Google Scholar
  159. Xu, Z., Wei, L., Wang, H., Jiang, S. 2002Biochem Biophys Res commun298552558Google Scholar
  160. Cho, H.W., Howard, C.R., Lee, H.W. 2002Intervirology45328333Google Scholar
  161. Choi, Y., Ahn, C.J., Seong, K.M., Jung, M.Y., Ahn, B.Y. 2003Vaccine2118671873Google Scholar
  162. Bharadwaj, M., Lyons, C.R., Wortman, I.A., Hjelle, B. 1999Vaccine1728362843Google Scholar
  163. Kamrud, K.I., Hooper, J.W., Elgh, F., Schmaljohn, C.S. 1999Virology263209219Google Scholar
  164. Koletzki, D., Schirmbeck, R., Lundkvist, A., Meisel, H., Kruger, D.H., Ulrich, R. 2001J Biotechnol847378Google Scholar
  165. Hooper, J.W., Custer, D.M., Thompson, E., Schmaljohn, C.S. 2001J Virol7584698477Google Scholar
  166. Johansson, P., Lindgren, T., Lundstrom, M., Holmstrom, A., Elgh, F., Bucht, G. 2002Vaccine2033793388Google Scholar
  167. Bharadwaj, M., Mirowsky, K., Ye, C., Botten, J., Masten, B., Yee, J., Lyons, C.R., Hjelle, B. 2002J Gen Virol8317451751Google Scholar
  168. Custer, D.M., Thompson, E., Schmaljohn, C.S., Ksiazek, T.G., Hooper, J.W. 2003J Virol7798949905Google Scholar
  169. Schmaljohn, C.S., Chu, Y.K., Schmaljohn, A.L., Dalrymple, J.M. 1990J Virol6431623170Google Scholar
  170. Schmaljohn, C.S., Hasty, S.E., Dalrymple, J.M. 1992Vaccine101013Google Scholar
  171. Lundkvist, A., Kalli-Kokko, H., Sjolander, K.B., Lankinen, H., Niklasson, B., Vaheri, A., Vapalahti, O. 1996Virology216397406Google Scholar
  172. Ulrich, R., Lundkvist, A., Meisel, H., Koletzki, D., Brus, K., Sjölander, H.R., Gelderblom, H.R., Borisova, G., Schnitzler, P., Darai, G., Krüger, D.H. 1998Vaccine16272280Google Scholar
  173. Welzel, T.M., Kehm, R., Tidona, C.A., Muranyi, W., Darai, G. 1998Virus Genes17185198Google Scholar
  174. De Carvalho Nicacio, C., Gonzalez Della Valle, M., Padula, P., Bjorling, E., Plyusnin, A., Lundkvist, A. 2002J Virol7666696677Google Scholar
  175. Zanskiene, A., Schmidt, J., Geldmacher, A., Ritzi, A., Niedrig, M., Lundkvist, A., Kruger, D.H., Meisel, H., Sasnauskas, K., Ulrich, R. 2004J Biotechnol111319333Google Scholar
  176. Gedvilaite, A., Zvirbliene, A., Staniulis, J., Sasnauskas, K., Kruger, D.H., Ulrich, R. 2004Viral Immunol175168Google Scholar
  177. Kehm, R., Jakob, N.J., Welzel, T.M., Tobiasch, E., Viczian, O., Jock, S., Geider, K., Sule, S., Darai, G. 2001Virus Genes227383Google Scholar
  178. Khattak, S., Darai, G., Rösen-Wolff, A. 2004Virus Genes29109116Google Scholar
  179. Koch, J., Liang, M., Queitsch, I., Kraus, A.A., Bautz, E.K. 2003Virology3086473Google Scholar
  180. Liang, M., Mahler, M., Koch, J., Ji, Y., Li, D., Schmaljohn, C., Bautz, E.K. 2003J Med Virol6999107Google Scholar
  181. Huggins, J.W., Kim, G.R., Brand, O.M., McKee, K.T. 1986J Infect Dis153489497Google Scholar
  182. Severson, W.E., Schmaljohn, C.S., Javadian, A., Jonsson, C.B. 2003J Virol77481488CrossRefPubMedGoogle Scholar
  183. Gubler, D.J., Reiter, P., Ebi, K.L., Yap, W., Nasci, R., Path, J.A. 2001Environ Health Perspect109223233Google Scholar
  184. Mustonen, J., Partanen, J., Kanerva, M., Pietilä, K., Vapalahti, O., Pasternack, A., Vaheri, A. 1996Kidney Int49217221Google Scholar
  185. Plyusnin, A., Vapalahti, O., Vaheri, A. 1996J Gen Virol7726772687Google Scholar
  186. Zhao, X., Hay, J. 1997Immunol Invest26191197Google Scholar
  187. Coulaud, X., Chouaib, E., Georges, A.J., Rollin, P., Gonzales, J.P. 1987Trans R Soc Trop Med Hyg81686Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  • Martin Zeier
    • 1
  • Michaela Handermann
    • 2
  • Udo Bahr
    • 1
  • Baldur Rensch
    • 2
  • Sandra Müller
    • 1
  • Roland Kehm
    • 2
  • Walter Muranyi
    • 2
  • Gholamreza Darai
    • 2
  1. 1.Sektion NephrologieKlinikum der Universität HeidelbergHeidelbergFederal Republic of Germany
  2. 2.Hygiene-Institut der Universität HeidelbergAbteilung VirologieHeidelbergFederal Republic of Germany

Personalised recommendations