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

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Abstract

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.

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References

  • C.S. Schmaljohn J.M. Dalrymple (1983) Virology 131 482–491

    Google Scholar 

  • 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.

  • Tidona C.A. and Darai G., The Springer Index of Viruses. Springer-Verlag, Berlin, Heidelberg, New York, 2002.

  • H.W. Lee P.W. Lee K.M. Johnson (1978) J Infect Dis 137 298–308 Occurrence Handle1:STN:280:CSeC3s7ltlw%3D Occurrence Handle24670

    CAS  PubMed  Google Scholar 

  • H.W. Lee P.W. Lee L.J. Baek Y.K. Chu (1990) Arch Virol 1 Suppl. 5–18

    Google Scholar 

  • G. Myhrman (1951) Acta Med Scand 140 52–56

    Google Scholar 

  • K.E. Fjellstrom (1960) Acta Med Scand 167 111–120

    Google Scholar 

  • B.S. Niklasson (1992) Pediatr Nephrol 6 201–204

    Google Scholar 

  • P. Vanhille R. Binaut X. Kyndt D. Launay C. Thomas D. Fleury (2001) Nephrologie 22 301–305

    Google Scholar 

  • G.E. Olsson F. Dalerum B. Hornfeldt F. Elgh T.R. Palo P. Juto C. Ahlm (2003) Emerg Infect Dis 9 1395–1401

    Google Scholar 

  • C. van Yperselede Strihou G. van der Groen J. Desmyter (1986) Adv Nephrol Necker Hosop 15 143–172

    Google Scholar 

  • M. Zeier K. Andrassy R. Waldherr E. Ritz (1986) Dtsch Med Wochenschr 111 207–210

    Google Scholar 

  • J. Clement P. Heyman P. McKenna P. Colson T. Avsic-Zupanc (1997) Emerg Infect Dis 3 205–211

    Google Scholar 

  • B. Settergren (1991) Rev Infect Dis 13 736–744

    Google Scholar 

  • M. Zeier L. Zoller T. Weinreich E. Padberg-Wolf K. Andrassy E. Ritz (1992) Clin Nephrol 38 190–192

    Google Scholar 

  • A. Papa A. Antoniadis J Eur (2001) Epidemiol 17 189–194

    Google Scholar 

  • M. Linderholm F. Elgh (2001) Curr Top Microbiol Immunol 256 135–151

    Google Scholar 

  • O. Vapalahti J. Mustonen A. Lundkvist H. Henttonen A. Plyusnin A. Vaheri (2003) Lancet Infect Dis 3 653–661 Occurrence Handle10.1016/S1473-3099(03)00774-6 Occurrence Handle14522264

    Article  PubMed  Google Scholar 

  • R.A. Slonova T.I. Astakhova G.G. Kompanets (1997) Zh Mikrobiol Epidemiol Immunobiol 5 97–101

    Google Scholar 

  • H. Miyamoto H. Kariwa K. Araki K. Lokugamage D. Hayasaka B.Z. Cui N. Lokugamage L.I. Ivanov T. Mizutani M.A. Iwasa K. Yoshimatsu J. Arikawa I. Takashima (2003) Arch Virol 148 1543–1556

    Google Scholar 

  • S.T. Nichol C.F. Spiropoulou S. Morzunov P.E. Rollin T.G. Ksiazek H. Feldmann A. Sanchez J. Childs S. Zaki C.J. Peters (1993) Science 262 914–917

    Google Scholar 

  • H. Feldmann A. Sanchez S. Morzunov C.F. Spiropoulou P.E. Rollin T.G. Ksiazek C.J. Peters S.T. Nichol (1993) Virus Res 30 351–367

    Google Scholar 

  • B. Hjelle F. Chavez-Giles N. Torrez-Martinez T. Yates J. Sarisky J. Webb M. Ascher (1994) J Virol 68 6751–6754

    Google Scholar 

  • B. Hjelle B. Anderson N. Torrez-Martinez W. Song W.L. Gannon T.L. Yates (1995) Virology 207 452–459

    Google Scholar 

  • B. Hjelle J. Krolikowski N. Torrez-Martinez F. Chavez-Giles C. Vanner E. Laposata (1995) J Med Virol 46 21–27

    Google Scholar 

  • B. Hjelle S.W. Lee W. Song N. Torrez-Martinez J.W. Song R. Yanagihara I. Gavrilovskaya E.R. Mackow (1995) J Virol 69 8137–8141

    Google Scholar 

  • A.S. Khan R.F. Khabbaz L.R. Armstrong R.C. Holman S.P. Bauer J. Graber T. Strine G. Miller S. Reef J. Tappero P.E. Rollin S.T. Nichol S.R. Zaki R.T. Bryan L.E. Chapman C.J. Peters T.G. Ksiazek (1996) J Infect Dis 173 1297–1331

    Google Scholar 

  • V.E. Chizhikov C.F. Spiropoulou M.C. Monroe C.J Peters S.T. Nichol S.P. Morzunov (1995) J Virol 69 8132–8136

    Google Scholar 

  • I. Gavrilovskaya R. La Monica M.E. Fay B. Hjelle C. Schmaljohn R. Shaw E.R. Mackow (1999) J Clin Microbiol 37 122–126

    Google Scholar 

  • L.B. Iversson A.P. da Rosa M.D. Rosa A.V. Lomar G. Sasaki Mda J.W. LeDuc (1994) Rev Assoc Med Bras 40 85–92 Occurrence Handle1:STN:280:ByqC38%2Fgt1Q%3D Occurrence Handle7820156

    CAS  PubMed  Google Scholar 

  • B. Hjelle N. Torrez-Martinez F.T. Koster (1996) Lancet 347 57

    Google Scholar 

  • M. Weissenbacher E. Cura E.L. Segura M. Hortal L.J. Baek Y.K. Chu H.W. Lee (1996) Medicina 56 17–22

    Google Scholar 

  • M. Bharadwaj J. Botten N. Torrez-Martinez B. Hjelle (1997) Am J Trop Med Hyg 57 368–374

    Google Scholar 

  • 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 

  • A.M. Johnson M.D. Bowen T.G. Ksiazek R.J. Williams R.T. Bryan J.N. Mills C.J. Peters S.T. Nichol (1997) Virology 238 115–127

    Google Scholar 

  • S. Levis S.P. Morzunov J.E. Rowe D. Enria N. Pini G. Calderon M. Sabattini S. St Jeor (1998) J Infect Dis 177 529–538

    Google Scholar 

  • J.F. Ferrer C.B. Jonsson E. Esteban D. Galligan M.A. Basombrio M. Peralta-Ramos M. Bharadwaj N. Torrez-Martinez J. Callahan A. Segovia B. Hjelle (1998) Am J Trop Med Hyg 59 438–444

    Google Scholar 

  • S. Levis J.E. Rowe S. Morzunov D.A. Enria S. Jeor (1997) St Lancet 349 998–999

    Google Scholar 

  • T.M. Malecki G.P. Jillson J.P. Thilsted J. Elrod N. Torres-Martinez B. Hjelle (1998) J Am Vet Med Assoc 212 970–973

    Google Scholar 

  • R. Espinoza P. Vial L.M. Noriega A. Johnson S.T. Nichol P.E. Rollin R. Wells S. Zaki E. Reynolds T.G. Ksiazek (1998) Emerg Infect Dis 4 93–95

    Google Scholar 

  • P.J. Padula A. Edelstein S.D. Miguel N.M. Lopez C.M. Rossi R.D. Rabinovich (1998) Virology 241 323–330

    Google Scholar 

  • G. Calderon N. Pini J. Bolpe S. Levis J. Mills E. Segura N. Guthmann G. Cantoni J. Becker A. Fonollat C. Ripoll M. Bortman R. Benedetti (1999) Emerg Infect Dis 5 792–797

    Google Scholar 

  • A.M. Johnson L.T. de Souza I.B. Ferreira (1999) J Med Virol 59 527–535

    Google Scholar 

  • M.J. Vincent E. Quiroz F. Gracia A.J. Sanchez T.G. Ksiazek P.T. Kitsutani L.A. Ruedas D.S. Tinnin L. Caceres A. Garcia P.E. Rollin J.N. Mills C.J. Peters S.T. Nichol (2000) Virology 277 14–19

    Google Scholar 

  • C.J. Yahnke P.L. Meserve T.G. Ksiazek J.N. Mills (2001) Am J Trop Med Hyg 65 768–776

    Google Scholar 

  • M.C. Bohlman S.P. Morzunov J. Meissner M.B. Taylor K. Ishibashi J. Rowe S. Levis D. Enria S.C. Jeor (2002) St J Virol 76 3765–3773

    Google Scholar 

  • M. Gonzalez Della Valle A. Edelstein S. Miguel V. Martinez J. Cortez M.L. Cacace G. Jurgelenas S.S. Estani P. Padula (2002) Am J Trop Med Hyg 66 713–720

    Google Scholar 

  • H. Galeno J. Mora E. Villagra J. Fernandez J. Hernandez G.J. Mertz E. Ramirez (2002) Emerg Infect Dis 8 657–661

    Google Scholar 

  • A. Delfraro M. Clara L. Tome F. Achaval S. Levis G. Calderon D. Enria M. Lozano J. Russi J. Arbiza (2003) Emerg Infect Dis 9 846–852

    Google Scholar 

  • Y.K. Chu R.D. Owen L.M. Gonzalez C.B. Jonsson (2003) Am J Trop Med Hyg 69 263–268

    Google Scholar 

  • F. Torres-Perez J. Navarrete-Droguett R. Aldunate T.L. Yates G.J. Mertz P.A. Vial M. Ferres P.A. Marquet R.E. Palma (2004) Am J Trop Med Hyg 70 305–309

    Google Scholar 

  • Williams E.C. and Barker I.K. (eds), Infectious Diseases of Wild Mammals. 3rd edn, Iowa State University Press, Ames, 2001, pp. 254–270.

  • J.N. Mills T.G. Ksiazek B.A. Ellis P.E. Rollin S.T. Nichol T.L. Yates W.L. Gannon C.E. Levy D.M. Engelthaler T. Davis D.T. Tanda J.W. Frampton C.R. Nichols C.J. Peters J.E. Childs (1997) Am J Trop Med Hyg 56 273–284

    Google Scholar 

  • E.S. Williams T. Yuill M. Artois J. Fischer S.A. Haigh (2002) Rev Sci Tech 21 139–157

    Google Scholar 

  • N. Nowotny H. Weissenboeck S. Aberle F. Hinterdorfer (1994) JAMA 272 1100–1101

    Google Scholar 

  • 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.

  • M. Pejcoch L. Danes S. Zahradkova E. Pekna (1992) Cesk Epidemiol Mikrobiol Immunol 41 92–100

    Google Scholar 

  • L. Danes M. Pejcoch K. Bukovjan J. Veleba M. Halackova (1992) Cesk Epidemiol Mikrobiol Immunol 41 15–18

    Google Scholar 

  • O. Vapalahti A. Lundkvist V. Fedorov C.J. Conroy S. Hirvonen A. Plyusnina K. Nemirov K. Fredga J.A. Cook J. Niemimaa A. Kaikusalo H. Henttonen A. Vaheri A. Plyusnin (1999) J Virol 73 5586–5592

    Google Scholar 

  • C. McCaughey C.A. Hart (2000) J Med Microbiol 49 587–589

    Google Scholar 

  • S.Y. Xiao M. Liang C.S. Schmaljohn (1993) J Gen Virol 74 1657–1659

    Google Scholar 

  • H. Kariwa Y. Isegawa J. Arikawa I. Takashima S. Ueda K. Yamanishi N. Hashimoto (1994) Virus Res 33 27–38

    Google Scholar 

  • D. Antic B.U. Lim C.Y. Kang (1991) Virus Res 19 59–65

    Google Scholar 

  • D. Antic B.U. Lim C.Y. Kang (1991) Virus Res 19 47–58

    Google Scholar 

  • J. Horling V. Chizhikov A. Lundkvist M. Jonsson L. Ivanov A. Dekonenko B. Niklasson T. Dzagurova C.J. Peters E. Tkachenko S. Nichol (1996) J Gen Virol 77 687–694

    Google Scholar 

  • S.Y. Xiao J.W. Leduc Y.K. Chu C.S. Schmaljohn (1994) Virology 198 205–217

    Google Scholar 

  • R. Stohwasser L.B. Giebel L. Zoller E.K. Bautz G. Darai (1990) Virology 174 79–86

    Google Scholar 

  • L.B. Giebel R. Stohwasser L. Zoller E.K. Bautz G. Darai (1989) Virology 172 498–505

    Google Scholar 

  • R. Stohwasser K. Raab G. Darai E.K. Bautz (1991) Virology 183 386–391

    Google Scholar 

  • B. Hjelle G.E. Glass (2000) J Infect Dis 181 1569–1573

    Google Scholar 

  • T. Avsic-Zupanc S.Y. Xiao R. Stojanovic A. Gligic G. van der Groen J.W. LeDuc (1992) Med Virol 38 132–137

    Google Scholar 

  • J.J. Scharninghausen H. Meyer M. Pfeffer D.S. Davis (1999) Emerg Infect Dis 5 468–470

    Google Scholar 

  • B. Klempa H.A. Schmidt R. Ulrich S. Kaluz M. Labuda H. Meisel B. Hjelle D.H. Krüger (2003) J Virol 77 804–809

    Google Scholar 

  • C. Sibold R. Ulrich M. Labuda A. Lundkvist H. Martens M. Schütt P. Gerke K. Leitmeyer H. Meisel D.H. Krüger (2001) J Med Virol 63 158–167

    Google Scholar 

  • K. Nemirov O. Vapalahti A. Papa A. Plyusnina A. Lundkvist A. Antoniadis A. Vaheri A. Plyusnin (2003) J Med Virol 69 408–416

    Google Scholar 

  • K. Nemirov H.K. Andersen H. Leirs H. Henttonen A. Vaheri A. Lundkvist A. Plyusnin (2004) J Clin Virol 30 254–257

    Google Scholar 

  • A. Plyusnin Y. Cheng O. Vapalahti M. Pejcoch J. Unar Z. Jelinkova H. Lehvaslaiho A. Lundkvist A. Vaheri (1995) Virus Res 39 237–250 Occurrence Handle1:CAS:528:DyaK28Xhtlemu70%3D Occurrence Handle8837887

    CAS  PubMed  Google Scholar 

  • O. Vapalahti A. Lundkvist S. Kukkonen Y. Cheng M. Gilljam M. Kanerva T. Manni M. Pejcoch J. Niemimaa A. Kaikusalo H. Henttonen A. Vaheri A Plyusnin (1996) J Gen Virol 77 3063–3067

    Google Scholar 

  • E.V. Ravkov P.E. Rollin T.G. Ksiazek C.J. Peters S.T. Nichol (1995) Virology 210 482–489

    Google Scholar 

  • L.L. Rodriguez J.H. Owens C.J. Peters S.T. Nichol (1998) Virology 242 99–106

    Google Scholar 

  • M.A. Parrington C.Y. Kang (1990) Virology 175 167–175

    Google Scholar 

  • M.A. Parrington P.W. Lee C.Y. Kang (1991) J Gen Virol 72 1845–1854

    Google Scholar 

  • W. Song N. Torrez-Martinez W. Irwin F.J. Harrison R. Davis M. Ascher M. Jay B. Hjelle (1995) J Gen Virol 76 3195–3199

    Google Scholar 

  • S. Morzunov H. Feldmann C.F. Spiropoulou V.A. Semenova P.E. Rollin T.G. Ksiazek C.J. Peters S.T. Nichol (1995) J Virol 69 1980–1983

    Google Scholar 

  • N. Torrez-Martinez B. Hjelle (1983) Lancet 346 780–781

    Google Scholar 

  • N. Torrez-Martinez W. Song B. Hjelle (1995) Virology 211 336–338

    Google Scholar 

  • J.W. Song L.J. Baek J.W. Nagle D. Schlitter R. Yanagihara (1996) Arch Virol 141 959–967

    Google Scholar 

  • J.A. Rawlings N. Torrez-Martinez S.U. Neill G.M. Moore B.N. Hicks S. Pichuantes A. Nguyen M. Bharadwaj B. Hjelle (1996) Am J Trop Med Hyg 55 672–679

    Google Scholar 

  • A.J. Sanchez K.D. Abbott S.T. Nichol (2001) Virology 286 345–353

    Google Scholar 

  • N. López P. Padula C. Rossi S. Miguel A. Edelstein E. Ramírez M.T. Franze-Fernández (1997) Virus Res 50 77–84

    Google Scholar 

  • J.D. Meissner J.E. Rowe M.K. Borucki S.C. St. Jeor (2002) Virus Res 89 131–143

    Google Scholar 

  • 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 

  • P. Caramello F. Canta L. Bonino C. Moiraghi F. Navone F. Lipani R. Balbiano A.M. Caputo V. Gai (2002) J Travel Med 9 326–329

    Google Scholar 

  • D.C. Gajdusek (1982) Scand J Infect Dis Suppl 36 96–108

    Google Scholar 

  • J.P. Gonzalez J.B. McCormick D. Baudon J.P. Gautun D.Y. Meunier E. Dournon A.J. Georges (1984) Lancet 2 1036–1037

    Google Scholar 

  • J.P. Gonzalez C.C. Mathiot J.C. Bouquety J.M. Diemer L. Guerre J.L. Lesborder M.C. Madelon A.J. Georges (1988) Ann Inst Pasteur Virol 139 301–304

    Google Scholar 

  • I.N. Gavrilovskaya E.J. Brown M.H. Ginsberg E.R. Mackow (1999) J Virol 73 3951–3959

    Google Scholar 

  • Cheresh D. A., Proc Natl Acad Sci 84, 6471–6475, 1987.

    Google Scholar 

  • R.O. Hynes (1992) Cell 69 11–25 Occurrence Handle10.1016/0092-8674(92)90115-S Occurrence Handle1:CAS:528:DyaK38XitFWmtrg%3D Occurrence Handle1555235

    Article  CAS  PubMed  Google Scholar 

  • M. Temonen J. Mustonen H. Helin A. Pasternack A. Vaheri H. Holthofer (1996) Clin Immunol Immunopathol 78 47–55

    Google Scholar 

  • Z.Y. Xu Y.W. Tang L.Y. Kann T.F. Tsai J Am (1987) Epidemiol 126 942–948

    Google Scholar 

  • Tokarevich N., Stoyanova N., Kozhukhova E., Makarova G., Volkova G., and Khnykin A., Epi North 2, 1, 2001.

  • E.A. Tkachenko H.W. Lee (1991) Kidney Int Suppl 35 54–61

    Google Scholar 

  • F.A. Leighton H.A. Artsob M.C. Chu J.G. Olson J Can (2001) Public Health 92 67–71

    Google Scholar 

  • M. Bennett G. Lloyd N. Jones A. Brown A.J. Trees C. McCracken N.R. Smyth C.J. Gaskell R.M. Gaskell (1990) Vet Rec 127 548–549

    Google Scholar 

  • Nowotny N., Lancet 343, 921, 1994.

  • N. Nowotny (1996) Zentralbl Hyg Umweltmed 198 452–461

    Google Scholar 

  • J.N. Mills J.M. Johnson T.G. Ksiazek B.A. Ellis P.E. Rollin T.L. Yates M.O. Mann M.R. Johnson M.L. Campbell J. Miyashiro M. Patrick M. Zyzak D. Lavender M.G. Novak K. Schmidt C.J. Peters J.E. Childs (1998) AmJ Trop Med Hyg 58 525–532

    Google Scholar 

  • J. Klingstrom A. Plyusnin A. Vaheri A. Lundkvist (2002) J Virol 76 444–449

    Google Scholar 

  • C. Ahlm K. Wallin A. Lundkvist F. Elgh P. Juto M. Merza A. Tarnvik (2000) Am J Trop Med Hyg 62 106–111

    Google Scholar 

  • M. Vahlenkamp T. Muller K. Tackmann U. Loschner H. Schmitz M. Schreiber (1998) Virus Res 57 139–150

    Google Scholar 

  • J. Arikawa M. Ito J.S. Yao H. Kariwa I. Takashima N. Hashimoto (1994) J Vet Med Sci 56 27–32

    Google Scholar 

  • Y. Zhang X. Li J. Tang (1995) Zhonghua Yu Fang Yi Xue Za Zhi 29 344–347

    Google Scholar 

  • C. Schmaljohn B. Hjelle (1997) Emerg Infect Dis 3 95–104 Occurrence Handle1:STN:280:ByiA2cfitl0%3D Occurrence Handle9204290

    CAS  PubMed  Google Scholar 

  • Center for Food Security and Public Health. Home page. <http://www.vetmed.iastate.edu/services/institutes/cfsph/default.html>. Accessed 2004 July 9.

  • NMNH Department of Systematic Biology, Division of Mammals–Mammal Species of the World Home Page. Home page. <http://www.nmnh.si.edu/msw/>. Accessed 2004 July 9.

  • E.O. Nuzum C.A. Rossi E.H. Stephenson J.W. LeDuc J Am (1988) Trop Hyg 38 636–640

    Google Scholar 

  • W. Muranyi R. Kehm U. Bahr S. Müller M. Handermann G. Darai M. Zeier (2004) Virology 318 112–122

    Google Scholar 

  • U. Bahr W. Muranyi S. Müller R. Kehm M. Handermann G. Darai M. Zeier (2004) Virology 321 1–7

    Google Scholar 

  • S.L. Ruo Y.L. Li Z. Tong Q.R. Ma Z.L. Liu Y.W. Tang K.L. Ye J.B. McCormick S.P. Fisher-Hoch Z.Y. Xu (1994) J Infect Dis 170 527–534

    Google Scholar 

  • J. Klingstrom P. Heyman S. Escutenaire K.B. Sjolander F. De Jeagere H. Henttonen A. Lundkvist (2002) J Med Virol 68 581–588

    Google Scholar 

  • J.A. Lednicky (2003) Arch Pathol Lab Med 127 30–35

    Google Scholar 

  • M. Brummer-Korvenkontio A. Vaheri T. Hovi C.-H. von Bonsdorff J. Vuorimies T. Manni K. Penttinen N. Oker-Blom J. Lähdevirta (1980) J Infect Dis 141 131–134

    Google Scholar 

  • B. Klempa H. Meisel S. Rath J. Bartel R. Ulrich D.H. Kruger (2003) J. Clin. Microbiol 41 4894–4897

    Google Scholar 

  • Hjelle B., Emerging Viruses Research Center. Home page. <http://hsc.unm.edu/pathology/HjelleLab/>. Accessed 2004 July 9.

  • E. Bridson J Br (2001) Biomed Sci 58 1–6

    Google Scholar 

  • Harper T.K. Hantavirus: Description, Vector, Mechanisms, Symptoms, etc. Website. <http://www.tarakharper.com/v_hanta.htm>. Accessed 2004 July 9.

  • 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.

  • K. Stuhlfault (1943) Dtsch Med Wochenschr 69, 439–443 474–477

    Google Scholar 

  • G.R. French R.S. Foulke O.A. Brand G.A. Eddy H.W. Lee P.W. Lee (1981) Science 211 1046–1048

    Google Scholar 

  • E. Pon K.T. McKee B.M. Diniega B. Merrell A. Corwin T.G. Ksiazek (1990) Am J Trop Med Hyg 42 612–619

    Google Scholar 

  • S. Hawes J.P. Seabolt (2003) Clin Lab Sci 16 39–42

    Google Scholar 

  • L.H. Elliott T.G. Ksiazek P.E. Rollin C.F. Spiropoulou S. Morzunov M. Monroe C.S. Goldsmith C.D. Humphrey S.R. Zaki J.W. Krebs (1994) J.W. Am J Trop Med Hyg 51 102–108

    Google Scholar 

  • R.J. Williams R.T. Bryan J.N. Mills R.E. Palma I. Vera F. De Velasquez E. Baez W.E. Schmidt R.E. Figueroa C.J. Peters S.R. Zaki A.S. Khan T.G. Ksiazek (1997) Am J Trop Med Hyg 57 274–282

    Google Scholar 

  • J. Toro J.D. Vega A.S. Khan J.N. Mills P. Padula W. Terry Z. Yadon R. Valderrama B.A. Ellis C. Pavletic R. Cerda S. Zaki W.J. Shieh R. Meyer M. Tapia C. Mansilla M. Baro J.A. Vergara M. Concha G. Calderon D. Enria C.J. Peters T.G. Ksiazek (1997) Emerg Infect Dis 4 687–694

    Google Scholar 

  • 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.

  • P.J. Padula A.J. Sanchez A. Edelstein S.T. Nichol (2002) J Gen Virol 83 2117–2122

    Google Scholar 

  • O.V. Suarez G.R. Cueto R. Cavia I.E. Gomez Villafane D.N. Bilenca A. Edelstein P. Martinez S. Miguel C. Bellomo K. Hodara P.J. Padula M. Busch (2003) Mem Inst Oswaldo Cruz 98 727–732

    Google Scholar 

  • N. Pini S. Levis G. Calderon J. Ramirez D. Bravo E. Lozano C. Ripoll S. St Jeor T.G. Ksiazek R.M. Barquez D. Enria (2003) Emerg Infect Dis 9 1070–1076

    Google Scholar 

  • J.F. Ferrer D. Galligan E. Esteban V. Rey A. Murua S. Gutierrez L. Gonzalez M. Thakuri L. Feldman B. Poiesz C. Jonsson (2003) Ann Trop Med Parasitol 97 269–280

    Google Scholar 

  • Y.W. Tang Z.Y. Xu Z.Y. Zhu T.F. Tsai (1985) Lancet 1 513–514

    Google Scholar 

  • M.N. Pensiero J.B. Sharefkin J. Hay (1992) J Virol 66 5929–5936

    Google Scholar 

  • I.M. Davidovich (1990) Ter Arkh 62 68–71

    Google Scholar 

  • A.A. Kraus M.J. Raftery T. Giese R. Ulrich R. Zawatzky S. Hippenstiel N. Suttorp D.H. Krüger G. Schönrich (2004) J Virol 78 6143–6150

    Google Scholar 

  • E.R. Mackow I.N. Gavrilovskaya (2001) Curr Top Microbiol Immunol 256 91–115

    Google Scholar 

  • M.J. Raftery A.A. Kraus R. Ulrich D.H. Krüger G. Schönrich (2002) J Virol 76 10724–10733

    Google Scholar 

  • 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.

  • B. Singh N. Rawlings A. Kaur (2001) Histol Histopathol 16 1037–1046

    Google Scholar 

  • J.W. LeDuc T.G. Ksiazek C.A. Rossi J.M. Dalrymple (1990) J Infect Dis 162 1182–1184

    Google Scholar 

  • T. Avsic-Zupanc A. Toney K. Anderson Y.K. Chu C. Schmaljohn (1995) J Gen Virol 76 2801–2808

    Google Scholar 

  • R.A. Slonova E.A. Tkachenko E.L. Kushnarev T.K. Dzagurova T.I. Astakova (1992) Acta Virol 36 493

    Google Scholar 

  • K.M. Johnson J.V. Lange P.A. Webb F.A. Murphy (1977) Lancet 1 569–571

    Google Scholar 

  • J.P. Gonzalez R. Josse E.D. Johnson M. Merlin A.J. Abandja J. Georges M. Danyod E. Delaporte A. Dupont A Ghogomu (1989) Res Virol 140 319–331

    Google Scholar 

  • A. Corwin M. Habib J. Olson D. Scott T. Ksiazek D.M. Watts (1992) Trans R Soc Trop Med Hyg 86 677–679

    Google Scholar 

  • 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 

  • A. Corwin M. Habib D. Watts M. Darwish J. Olson B. Botros R. Hibbs M. Kleinosky H.W. Lee R. Shope M. Kilpatrick (1993) Am J Trop Med Hyg 48 776–783

    Google Scholar 

  • G. Rodier A.K. Soliman J. Bouloumie D. Kremer (1993) Trans R Soc Trop Med Hyg 87 160–161

    Google Scholar 

  • E. Nakounne B. Selekon J. Morvan (2000) Bull Soc Pathol Exot 93 340–347

    Google Scholar 

  • Z. Xu L. Wei H. Wang S. Jiang (2002) Biochem Biophys Res commun 298 552–558

    Google Scholar 

  • H.W. Cho C.R. Howard H.W. Lee (2002) Intervirology 45 328–333

    Google Scholar 

  • Y. Choi C.J. Ahn K.M. Seong M.Y. Jung B.Y. Ahn (2003) Vaccine 21 1867–1873

    Google Scholar 

  • M. Bharadwaj C.R. Lyons I.A. Wortman B. Hjelle (1999) Vaccine 17 2836–2843

    Google Scholar 

  • K.I. Kamrud J.W. Hooper F. Elgh C.S. Schmaljohn (1999) Virology 263 209–219

    Google Scholar 

  • D. Koletzki R. Schirmbeck A. Lundkvist H. Meisel D.H. Kruger R. Ulrich (2001) J Biotechnol 84 73–78

    Google Scholar 

  • J.W. Hooper D.M. Custer E. Thompson C.S. Schmaljohn (2001) J Virol 75 8469–8477

    Google Scholar 

  • P. Johansson T. Lindgren M. Lundstrom A. Holmstrom F. Elgh G. Bucht (2002) Vaccine 20 3379–3388

    Google Scholar 

  • M. Bharadwaj K. Mirowsky C. Ye J. Botten B. Masten J. Yee C.R. Lyons B. Hjelle (2002) J Gen Virol 83 1745–1751

    Google Scholar 

  • D.M. Custer E. Thompson C.S. Schmaljohn T.G. Ksiazek J.W. Hooper (2003) J Virol 77 9894–9905

    Google Scholar 

  • C.S. Schmaljohn Y.K. Chu A.L. Schmaljohn J.M. Dalrymple (1990) J Virol 64 3162–3170

    Google Scholar 

  • C.S. Schmaljohn S.E. Hasty J.M. Dalrymple (1992) Vaccine 10 10–13

    Google Scholar 

  • A. Lundkvist H. Kalli-Kokko K.B. Sjolander H. Lankinen B. Niklasson A. Vaheri O. Vapalahti (1996) Virology 216 397–406

    Google Scholar 

  • R. Ulrich A. Lundkvist H. Meisel D. Koletzki K. Brus H.R. Sjölander H.R. Gelderblom G. Borisova P. Schnitzler G. Darai D.H. Krüger (1998) Vaccine 16 272–280

    Google Scholar 

  • T.M. Welzel R. Kehm C.A. Tidona W. Muranyi G. Darai (1998) Virus Genes 17 185–198

    Google Scholar 

  • C. De Carvalho Nicacio M. Gonzalez Della Valle P. Padula E. Bjorling A. Plyusnin A. Lundkvist (2002) J Virol 76 6669–6677

    Google Scholar 

  • A. Zanskiene J. Schmidt A. Geldmacher A. Ritzi M. Niedrig A. Lundkvist D.H. Kruger H. Meisel K. Sasnauskas R. Ulrich (2004) J Biotechnol 111 319–333

    Google Scholar 

  • A. Gedvilaite A. Zvirbliene J. Staniulis K. Sasnauskas D.H. Kruger R. Ulrich (2004) Viral Immunol 17 51–68

    Google Scholar 

  • R. Kehm N.J. Jakob T.M. Welzel E. Tobiasch O. Viczian S. Jock K. Geider S. Sule G. Darai (2001) Virus Genes 22 73–83

    Google Scholar 

  • S. Khattak G. Darai A. Rösen-Wolff (2004) Virus Genes 29 109–116

    Google Scholar 

  • J. Koch M. Liang I. Queitsch A.A. Kraus E.K. Bautz (2003) Virology 308 64–73

    Google Scholar 

  • M. Liang M. Mahler J. Koch Y. Ji D. Li C. Schmaljohn E.K. Bautz (2003) J Med Virol 69 99–107

    Google Scholar 

  • J.W. Huggins G.R. Kim O.M. Brand K.T. McKee (1986) J Infect Dis 153 489–497

    Google Scholar 

  • W.E. Severson C.S. Schmaljohn A. Javadian C.B. Jonsson (2003) J Virol 77 481–488 Occurrence Handle10.1128/JVI.77.1.481-488.2003 Occurrence Handle1:CAS:528:DC%2BD3sXkt1Cl Occurrence Handle12477853

    Article  CAS  PubMed  Google Scholar 

  • D.J. Gubler P. Reiter K.L. Ebi W. Yap R. Nasci J.A. Path (2001) Environ Health Perspect 109 223–233

    Google Scholar 

  • J. Mustonen J. Partanen M. Kanerva K. Pietilä O. Vapalahti A. Pasternack A. Vaheri (1996) Kidney Int 49 217–221

    Google Scholar 

  • A. Plyusnin O. Vapalahti A. Vaheri (1996) J Gen Virol 77 2677–2687

    Google Scholar 

  • X. Zhao J. Hay (1997) Immunol Invest 26 191–197

    Google Scholar 

  • X. Coulaud E. Chouaib A.J. Georges P. Rollin J.P. Gonzales (1987) Trans R Soc Trop Med Hyg 81 686

    Google Scholar 

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Zeier, M., Handermann, M., Bahr, U. et al. New Ecological Aspects of Hantavirus Infection: A Change of A Paradigm and a Challenge of Prevention- A Review. Virus Genes 30, 157–180 (2005). https://doi.org/10.1007/s11262-004-5625-2

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