The Syrian hamster model of hantavirus pulmonary syndrome

Antiviral Research

Volumn 95, Issue 3, 2012, Pages 282-292

  Safronetz, David ^a   Ebihara, Hideki ^a   Feldmann, Heinz ^a   Hooper, Jay W ^b  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b UNITED STATES ARMY MEDICAL RESEARCH INSTITUTE OF INFECTIOUS DISEASES   (United States)

Author keywords

Andes virus; Animal model; Bunyavirus; Hamster; Hantavirus pulmonary syndrome

Indexed keywords

DNA VACCINE; HANTAVIRUS PULMONARY SYNDROME VACCINE; NUCLEOPROTEIN; RIBAVIRIN; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; VIRUS VACCINE;

CELLULAR IMMUNITY; DISEASE COURSE; DYSPNEA; EXPERIMENTAL MODEL; HANTAVIRUS PULMONARY SYNDROME; IMMUNOMODULATION; INCUBATION TIME; LUNG; LUNG EDEMA; NONHUMAN; PHYLOGENY; PLEURA EFFUSION; PRIORITY JOURNAL; RESPIRATORY DISTRESS; REVIEW; SYRIAN HAMSTER;

ANIMALS; CRICETINAE; DISEASE MODELS, ANIMAL; HANTAVIRUS; HANTAVIRUS PULMONARY SYNDROME; HUMANS; MESOCRICETUS;

ANDES VIRUS; ANIMALIA; CRICETINAE; HANTAVIRUS; MESOCRICETUS AURATUS; ORTHOBUNYAVIRUS;

EID: 84865299409     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2012.06.002     Document Type: Review

References (97)

1. Arikawa J., Yao J.S., Yoshimatsu K., Takashima I., Hashimoto N. Protective role of antigenic sites on the envelope protein of Hantaan virus defined by monoclonal antibodies. Arch. Virol. 1992, 126:271-281.
2. Bharadwaj M., Nofchissey R., Goade D., Koster F., Hjelle B. Humoral immune responses in the hantavirus cardiopulmonary syndrome. J. Infect. Dis. 2000, 182:43-48.
3. Billings A.N., Rollin P.E., Milazzo M.L., Molina C.P., Eyzaguirre E.J., Livingstone W., Ksiazek T.G., Fulhorst C.F. Pathology of Black Creek Canal virus infection in juvenile hispid cotton rats (Sigmodon hispidus). Vector Borne Zoonotic Dis. 2010, 10:621-628.
4. Borges A.A., Campos G.M., Moreli M.L., Souza R.L., Aquino V.H., Saggioro F.P., Figueiredo L.T. Hantavirus cardiopulmonary syndrome: immune response and pathogenesis. Microbes Infect. 2006, 8:2324-2330.
5. Borges A.A., Campos G.M., Moreli M.L., Moro Souza R.L., Saggioro F.P., Figueiredo G.G., Livonesi M.C., Moraes Figueiredo L.T. Role of mixed Th1 and Th2 serum cytokines on pathogenesis and prognosis of hantavirus pulmonary syndrome. Microbes Infect. 2008, 10:1150-1157.
6. Boroja M., Barrie J.R., Raymond G.S. Radiographic findings in 20 patients with hantavirus pulmonary syndrome correlated with clinical outcome. AJR Am. J. Roentgenol. 2002, 178:159-163.
7. Botten J., Mirowsky K., Kusewitt D., Bharadwaj M., Yee J., Ricci R., Feddersen R.M., Hjelle B. Experimental infection model for Sin Nombre hantavirus in the deer mouse (Peromyscus maniculatus). Proc. Natl. Acad. Sci. USA 2000, 97:10578-10583.
8. Boudreau E.F., Josleyn M., Ullman D., Fisher D., Dalrymple L., Sellers-Myers K., Loudon P., Rusnak J., Rivard R., Schmaljohn C., Hooper J.W. A Phase 1 clinical trial of hantaan virus and puumala virus M-segment DNA vaccines for hemorrhagic fever with renal syndrome. Vaccine 2012, 30:1951-1958.
9. Brocato R., Josleyn M., Ballantyne J., Vial P., Hooper J.W. DNA vaccine-generated duck polyclonal antibodies as a postexposure prophylactic to prevent hantavirus pulmonary syndrome (HPS). PLoS One 2012, 7:e35996.
10. Brown K.S., Safronetz D., Marzi A., Ebihara H., Feldmann H. Vesicular stomatitis virus-based vaccine protects hamsters against lethal challenge with Andes virus. J. Virol. 2011, 85:12781-12791.
11. Buys K.K., Jung K.H., Smee D.F., Furuta Y., Gowen B.B. Maporal virus as a surrogate for pathogenic New World hantaviruses and its inhibition by favipiravir. Antivir. Chem. Chemother. 2011, 21:193-200.
12. Campen M.J., Milazzo M.L., Fulhorst C.F., Obot Akata C.J., Koster F. Characterization of shock in a hamster model of hantavirus infection. Virology 2006, 356:45-49.
13. Castillo C., Naranjo J., Sepulveda A., Ossa G., Levy H. Hantavirus pulmonary syndrome due to Andes virus in Temuco, Chile: clinical experience with 16 adults. Chest 2001, 120:548-554.
14. CDC, 2010. Hantavirus pulmonary syndrome (hantavirus disease) (HPS) 2010 case definition, http://www.cdc.gov/osels/ph_surveillance/nndss/print/hantaviruscurrent.htm.
15. Chapman L.E., Mertz G.J., Peters C.J., Jolson H.M., Khan A.S., Ksiazek T.G., Koster F.T., Baum K.F., Rollin P.E., Pavia A.T., Holman R.C., Christenson J.C., Rubin P.J., Behrman R.E., Bell L.J., Simpson G.L., Sadek R.F. Intravenous ribavirin for hantavirus pulmonary syndrome: safety and tolerance during 1 year of open-label experience. Ribavirin Study Group. Antivir. Ther. 1999, 4:211-219.
16. Custer D.M., Thompson E., Schmaljohn C.S., Ksiazek T.G., Hooper J.W. Active and passive vaccination against hantavirus pulmonary syndrome with Andes virus M genome segment-based DNA vaccine. J. Virol. 2003, 77:9894-9905.
17. Dietl C.A., Wernly J.A., Pett S.B., Yassin S.F., Sterling J.P., Dragan R., Milligan K., Crowley M.R. Extracorporeal membrane oxygenation support improves survival of patients with severe hantavirus cardiopulmonary syndrome. J. Thorac. Cardiovasc. Surg. 2008, 135:579-584.
18. Duchin J.S., Koster F.T., Peters C.J., Simpson G.L., Tempest B., Zaki S.R., Ksiazek T.G., Rollin P.E., Nichol S., Umland E.T., et al. Hantavirus pulmonary syndrome: a clinical description of 17 patients with a newly recognized disease. The Hantavirus Study Group. N. Engl. J. Med. 1994, 330:949-955.
19. Easterbrook J.D., Zink M.C., Klein S.L. Regulatory T cells enhance persistence of the zoonotic pathogen seoul virus in its reservoir host. Proc. Natl. Acad. Sci. USA 2007, 104:15502-15507.
20. Ebihara H., Yoshimatsu K., Ogino M., Araki K., Ami Y., Kariwa H., Takashima I., Li D., Arikawa J. Pathogenicity of Hantaan virus in newborn mice. genetic reassortant study demonstrating that a single amino acid change in glycoprotein G1 is related to virulence. J. Virol. 2000, 74:9245-9255.
21. Enria D.A., Briggiler A.M., Pini N., Levis S. Clinical manifestations of New World hantaviruses. Curr. Top Microbiol. Immunol. 2001, 256:117-134.
22. Enria D.A., Briggiler A.M., Sanchez Z. Treatment of Argentine hemorrhagic fever. Antiviral Res. 2008, 78:132-139.
23. Eyzaguirre E.J., Milazzo M.L., Koster F.T., Fulhorst C.F. Choclo virus infection in the Syrian golden hamster. Am. J. Trop. Med. Hyg. 2008, 78:669-674.
24. FDA, 2009. Guidance for Industry: Animal Model- Essential Elements to Address Efficacy Under the Animal Rule. January 2009, http://www.fda.gov/downloads/Drugs/GuidanceComplianceRegulatoryInformation/Guidances/ucm078923.pdf.
25. Fulhorst C.F., Milazzo M.L., Duno G., Salas R.A. Experimental infection of the Sigmodon alstoni cotton rat with Cano Delgadito virus, a South American hantavirus. Am. J. Trop. Med. Hyg. 2002, 67:107-111.
26. Gavrilovskaya I.N., Shepley M., Shaw R., Ginsberg M.H., Mackow E.R. Beta3 Integrins mediate the cellular entry of hantaviruses that cause respiratory failure. Proc. Natl. Acad. Sci. USA 1998, 95:7074-7079.
27. Gavrilovskaya I.N., Brown E.J., Ginsberg M.H., Mackow E.R. Cellular entry of hantaviruses which cause hemorrhagic fever with renal syndrome is mediated by beta3 integrins. J. Virol. 1999, 73:3951-3959.
28. Gorbunova E., Gavrilovskaya I.N., Mackow E.R. Pathogenic hantaviruses andes virus and hantaan virus induce adherens junction disassembly by directing vascular endothelial cadherin internalization in human endothelial cells. J. Virol. 2010, 84:7405-7411.
29. Gorbunova E.E., Gavrilovskaya I.N., Pepini T., Mackow E.R. VEGFR2 and Src kinase inhibitors suppress andes virus-induced endothelial cell permeability. J. Virol. 2011, 85:2296-2303.
30. Gowen B.B., Holbrook M.R. Animal models of highly pathogenic RNA viral infections: hemorrhagic fever viruses. Antiviral Res. 2008, 78:79-90.
31. Gowen B.B., Julander J.G., London N.R., Wong M.H., Larson D., Morrey J.D., Li D.Y., Bray M. Assessing changes in vascular permeability in a hamster model of viral hemorrhagic fever. Virol. J. 2010, 7:240.
32. Hammerbeck C.D., Hooper J.W. Hantavirus vaccines. New Generation Vaccines 2010, 905-913. Informa Healthcare, New York. fourth ed. M.M. Levin (Ed.).
33. Hammerbeck C.D., Hooper J.W. T cells are not required for pathogenesis in the Syrian hamster model of hantavirus pulmonary syndrome. J. Virol. 2011, 85:9929-9944.
34. Hooper J.W., Kamrud K.I., Elgh F., Custer D., Schmaljohn C.S. DNA vaccination with hantavirus M segment elicits neutralizing antibodies and protects against seoul virus infection. Virology 1999, 255:269-278.
35. Hooper J.W., Larsen T., Custer D.M., Schmaljohn C.S. A lethal disease model for hantavirus pulmonary syndrome. Virology 2001, 289:6-14.
36. Hooper J.W., Custer D.M., Smith J., Wahl-Jensen V. Hantaan/andes virus DNA vaccine elicits a broadly cross-reactive neutralizing antibody response in nonhuman primates. Virology 2006, 347:208-216.
37. Hooper J.W., Ferro A.M., Wahl-Jensen V. Immune serum produced by DNA vaccination protects hamsters against lethal respiratory challenge with andes virus. J. Virol. 2008, 82:1332-1338.
38. Huggins J.W., Kim G.R., Brand O.M., McKee K.T. Ribavirin therapy for hantaan virus infection in suckling mice. J. Infect. Dis. 1986, 153:489-497.
39. Hutchinson K.L., Rollin P.E., Peters C.J. Pathogenesis of a North American hantavirus, Black Creek Canal virus, in experimentally infected Sigmodon hispidus. Am. J. Trop. Med. Hyg. 1998, 59:58-65.
40. ICTV, 2009. Virus Taxonomy, http://ictvonline.org/virusTaxonomy.asp.
41. Jonsson C.B., Hooper J., Mertz G. Treatment of hantavirus pulmonary syndrome. Antiviral Res. 2008, 78:162-169.
42. Jonsson C.B., Figueiredo L.T., Vapalahti O. A global perspective on hantavirus ecology, epidemiology, and disease. Clin. Microbiol. Rev. 2010, 23:412-441.
43. Kamrud K.I., Hooper J.W., Elgh F., Schmaljohn C.S. Comparison of the protective efficacy of naked DNA, DNA-based Sindbis replicon, and packaged Sindbis replicon vectors expressing Hantavirus structural genes in hamsters. Virology 1999, 263:209-219.
44. Klein S.L., Bird B.H., Glass G.E. Sex differences in immune responses and viral shedding following seoul virus infection in Norway rats. Am. J. Trop. Med. Hyg. 2001, 65:57-63.
45. Klingstrom J., Plyusnin A., Vaheri A., Lundkvist A. Wild-type puumala hantavirus infection induces cytokines, C-reactive protein, creatinine, and nitric oxide in cynomolgus macaques. J. Virol. 2002, 76:444-449.
46. Klingstrom J., Hardestam J., Lundkvist A. Dobrava, but not saaremaa, hantavirus is lethal and induces nitric oxide production in suckling mice. Microbes Infect. 2006, 8:728-737.
47. Kurata T., Tsai T.F., Bauer S.P., McCormick J.B. Immunofluorescence studies of disseminated hantaan virus infection of suckling mice. Infect. Immun. 1983, 41:391-398.
48. Lee H.W., Lee P.W., Baek L.J., Song C.K., Seong I.W. Intraspecific transmission of hantaan virus, etiologic agent of Korean hemorrhagic fever, in the rodent Apodemus agrarius. Am. J. Trop. Med. Hyg. 1981, 30:1106-1112.
49. Lee P.W., Yanagihara R., Gibbs C.J., Gajdusek D.C. Pathogenesis of experimental hantaan virus infection in laboratory rats. Arch. Virol. 1986, 88:57-66.
50. Lundkvist A., Kallio-Kokko H., Sjolander K.B., Lankinen H., Niklasson B., Vaheri A., Vapalahti O. Characterization of puumala virus nucleocapsid protein: identification of B-cell epitopes and domains involved in protective immunity. Virology 1996, 216:397-406.
51. Macneil A., Nichol S.T., Spiropoulou C.F. Hantavirus pulmonary syndrome. Virus Res. 2011, 162:138-147.
52. Martinez V.P., Bellomo C., San Juan J., Pinna D., Forlenza R., Elder M., Padula P.J. Person-to-person transmission of andes virus. Emerg. Infect. Dis. 2005, 11:1848-1853.
53. Martinez V.P., Padula P.J. Induction of protective immunity in a Syrian hamster model against a cytopathogenic strain of andes virus. J. Med. Virol. 2012, 84:87-95.
54. Matthys V.S., Gorbunova E.E., Gavrilovskaya I.N., Mackow E.R. Andes virus recognition of human and Syrian hamster beta3 integrins is determined by an L33P substitution in the PSI domain. J. Virol. 2010, 84:352-360.
55. McElroy A.K., Bray M., Reed D.S., Schmaljohn C.S. Andes virus infection of cynomolgus macaques. J. Infect. Dis. 2002, 186:1706-1712.
56. McElroy A.K., Smith J.M., Hooper J.W., Schmaljohn C.S. Andes virus M genome segment is not sufficient to confer the virulence associated with andes virus in Syrian hamsters. Virology 2004, 326:130-139.
57. McKee K.T., Kim G.R., Green D.E., Peters C.J. Hantaan virus infection in suckling mice: virologic and pathologic correlates. J. Med. Virol. 1985, 17:107-117.
58. McNees A.L., Vilchez R.A., Heard T.C., Sroller V., Wong C., Herron A.J., Hamilton M.J., Davis W.C., Butel J.S. SV40 lymphomagenesis in Syrian golden hamsters. Virology 2009, 384:114-124.
59. Medina R.A., Mirowsky-Garcia K., Hutt J., Hjelle B. Ribavirin, human convalescent plasma and anti-beta3 integrin antibody inhibit infection by Sin Nombre virus in the deer mouse model. J. Gen. Virol. 2007, 88:493-505.
60. Mertz G.J., Miedzinski L., Goade D., Pavia A.T., Hjelle B., Hansbarger C.O., Levy H., Koster F.T., Baum K., Lindemulder A., Wang W., Riser L., Fernandez H., Whitley R.J. Placebo-controlled, double-blind trial of intravenous ribavirin for the treatment of hantavirus cardiopulmonary syndrome in North America. Clin. Infect. Dis. 2004, 39:1307-1313.
61. Milazzo M.L., Eyzaguirre E.J., Molina C.P., Fulhorst C.F. Maporal viral infection in the Syrian golden hamster: a model of hantavirus pulmonary syndrome. J. Infect. Dis. 2002, 186:1390-1395.
62. Mori M., Rothman A.L., Kurane I., Montoya J.M., Nolte K.B., Norman J.E., Waite D.C., Koster F.T., Ennis F.A. High levels of cytokine-producing cells in the lung tissues of patients with fatal hantavirus pulmonary syndrome. J. Infect. Dis. 1999, 179:295-302.
63. Murphy M.E., Kariwa H., Mizutani T., Tanabe H., Yoshimatsu K., Arikawa J., Takashima I. Characterization of in vitro and in vivo antiviral activity of lactoferrin and ribavirin upon hantavirus. J. Vet. Med. Sci. 2001, 63:637-645.
64. Neumann K., Michaux J., Lebedev V., Yigit N., Colak E., Ivanova N., Poltoraus A., Surov A., Markov G., Maak S., Neumann S., Gattermann R. Molecular phylogeny of the Cricetinae subfamily based on the mitochondrial cytochrome b and 12S rRNA genes and the nuclear vWF gene. Mol. Phylogenet. Evol. 2006, 39:135-148.
65. Padula P.J., Edelstein A., Miguel S.D., Lopez N.M., Rossi C.M., Rabinovich R.D. Hantavirus pulmonary syndrome outbreak in Argentina: molecular evidence for person-to-person transmission of andes virus. Virology 1998, 241:323-330.
66. Rockx B., Brining D., Kramer J., Callison J., Ebihara H., Mansfield K., Feldmann H. Clinical outcome of henipavirus infection in hamsters is determined by the route and dose of infection. J. Virol. 2011, 85:7658-7671.
67. Safronetz D., Hegde N.R., Ebihara H., Denton M., Kobinger G.P., St Jeor S., Feldmann H., Johnson D.C. Adenovirus vectors expressing hantavirus proteins protect hamsters against lethal challenge with andes virus. J. Virol. 2009, 83:7285-7295.
68. Safronetz D., Haddock E., Feldmann F., Ebihara H., Feldmann H. In vitro and in vivo activity of ribavirin against andes virus infection. PLoS One 2011, 6:e23560.
69. Safronetz D., Zivcec M., Lacasse R., Feldmann F., Rosenke R., Long D., Haddock E., Brining D., Gardner D., Feldmann H., Ebihara H. Pathogenesis and host response in Syrian hamsters following intranasal infection with andes virus. PLoS Pathog. 2011, 7:e1002426.
70. Saggioro F.P., Rossi M.A., Duarte M.I., Martin C.C., Alves V.A., Moreli M.L., Figueiredo L.T., Moreira J.E., Borges A.A., Neder L. Hantavirus infection induces a typical myocarditis that may be responsible for myocardial depression and shock in hantavirus pulmonary syndrome. J. Infect. Dis. 2007, 195:1541-1549.
71. Sanada T., Kariwa H., Nagata N., Tanikawa Y., Seto T., Yoshimatsu K., Arikawa J., Yoshii K., Takashima I. Puumala virus infection in Syrian hamsters (Mesocricetus auratus) resembling hantavirus infection in natural rodent hosts. Virus Res. 2011, 160:108-119.
72. Schmaljohn C. Vaccines for hantaviruses. Vaccine 2009, 27(Suppl. 4):D61-D64.
73. Schmaljohn C.S., Chu Y.K., Schmaljohn A.L., Dalrymple J.M. Antigenic subunits of hantaan virus expressed by baculovirus and vaccinia virus recombinants. J. Virol. 1990, 64:3162-3170.
74. Schountz T., Prescott J., Cogswell A.C., Oko L., Mirowsky-Garcia K., Galvez A.P., Hjelle B. Regulatory T cell-like responses in deer mice persistently infected with Sin Nombre virus. Proc. Natl. Acad. Sci. USA 2007, 104:15496-15501.
75. Seto T., Nagata N., Yoshikawa K., Ichii O., Sanada T., Saasa N., Ozaki Y., Kon Y., Yoshii K., Takashima I., Kariwa H. Infection of hantaan virus strain AA57 leading to pulmonary disease in laboratory mice. Virus Res. 2012, 163:284-290.
76. Shrivastava-Ranjan P., Rollin P.E., Spiropoulou C.F. Andes virus disrupts the endothelial cell barrier by induction of vascular endothelial growth factor and downregulation of VE-cadherin. J. Virol. 2010, 84:11227-11234.
77. Sironen T., Klingstrom J., Vaheri A., Andersson L.C., Lundkvist A., Plyusnin A. Pathology of puumala hantavirus infection in macaques. PLoS One 2008, 3:e3035.
78. St Jeor S.C. Three-week incubation period for hantavirus infection. Pediatr. Infect. Dis. J. 2004, 23:974-975.
79. Taddei A., Giampietro C., Conti A., Orsenigo F., Breviario F., Pirazzoli V., Potente M., Daly C., Dimmeler S., Dejana E. Endothelial adherens junctions control tight junctions by VE-cadherin-mediated upregulation of claudin-5. Nat. Cell Biol. 2008, 10:923-934.
80. Tamura M., Asada H., Kondo K., Tanishita O., Kurata T., Yamanishi K. Pathogenesis of Hantaan virus in mice. J. Gen. Virol. 1989, 70(Pt. 11):2897-2906.
81. Terajima M., Ennis F.A. T cells and pathogenesis of hantavirus cardiopulmonary syndrome and hemorrhagic fever with renal syndrome. Viruses 2011, 3:1059-1073.
82. 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. An outbreak of hantavirus pulmonary syndrome, Chile, 1997. Emerg. Infect. Dis. 1998, 4:687-694.
83. Torres-Perez F., Wilson L., Collinge S.K., Harmon H., Ray C., Medina R.A., Hjelle B. Sin Nombre virus infection in field workers, Colorado, USA. Emerg. Infect. Dis. 2010, 16:308-310.
84. Vial P.A., Valdivieso F., Mertz G., Castillo C., Belmar E., Delgado I., Tapia M., Ferres M. Incubation period of hantavirus cardiopulmonary syndrome. Emerg. Infect. Dis. 2006, 12:1271-1273.
85. Wahl-Jensen V., Chapman J., Asher L., Fisher R., Zimmerman M., Larsen T., Hooper J.W. Temporal analysis of Andes virus and Sin Nombre virus infections of Syrian hamsters. J. Virol. 2007, 81:7449-7462.
86. Wichmann D., Grone H.J., Frese M., Pavlovic J., Anheier B., Haller O., Klenk H.D., Feldmann H. Hantaan virus infection causes an acute neurological disease that is fatal in adult laboratory mice. J. Virol. 2002, 76:8890-8899.
87. Xiao R., Yang S., Koster F., Ye C., Stidley C., Hjelle B. Sin Nombre viral RNA load in patients with hantavirus cardiopulmonary syndrome. J. Infect. Dis. 2006, 194:1403-1409.
88. Xu X., Ruo S.L., McCormick J.B., Fisher-Hoch S.P. Immunity to Hantavirus challenge in Meriones unguiculatus induced by vaccinia-vectored viral proteins. Am. J. Trop. Med. Hyg. 1992, 47:397-404.
89. Xu Z., Wei L., Wang L., Wang H., Jiang S. The in vitro and in vivo protective activity of monoclonal antibodies directed against hantaan virus: potential application for immunotherapy and passive immunization. Biochem. Biophys. Res. Commun. 2002, 298:552-558.
90. Yanagihara R., Amyx H.L., Gajdusek D.C. Experimental infection with puumala virus, the etiologic agent of nephropathia epidemica, in bank voles (Clethrionomys glareolus). J. Virol. 1985, 55:34-38.
91. Yanagihara R., Amyx H.L., Lee P.W., Asher D.M., Gibbs C.J., Gajdusek D.C. Experimental hantavirus infection in nonhuman primates. Arch. Virol. 1988, 101:125-130.
92. Yoo Y.C., Yoshimatsu K., Yoshida R., Tamura M., Azuma I., Arikawa J. Comparison of virulence between seoul virus strain SR-11 and hantaan virus strain 76-118 of hantaviruses in newborn mice. Microbiol. Immunol. 1993, 37:557-562.
93. Yoshimatsu K., Arikawa J., Tamura M., Yoshida R., Lundkvist A., Niklasson B., Kariwa H., Azuma I. Characterization of the nucleocapsid protein of hantaan virus strain 76-118 using monoclonal antibodies. J. Gen. Virol. 1996, 77(Pt 4):695-704.
94. Young J.C., Hansen G.R., Graves T.K., Deasy M.P., Humphreys J.G., Fritz C.L., Gorham K.L., Khan A.S., Ksiazek T.G., Metzger K.B., Peters C.J. The incubation period of hantavirus pulmonary syndrome. Am. J. Trop. Med. Hyg. 2000, 62:714-717.
95. Zaki S.R., Greer P.W., Coffield L.M., Goldsmith C.S., Nolte K.B., Foucar K., Feddersen R.M., Zumwalt R.E., Miller G.L., Khan A.S., et al. Hantavirus pulmonary syndrome. Pathogenesis of an emerging infectious disease. Am. J. Pathol. 1995, 146:552-579.
96. Zhang X.K., Takashima I., Hashimoto N. Characteristics of passive immunity against hantavirus infection in rats. Arch. Virol. 1989, 105:235-246.
97. Zivcec M., Safronetz D., Haddock E., Feldmann H., Ebihara H. Validation of assays to monitor immune responses in the Syrian golden hamster (Mesocricetus auratus). J. Immunol. Methods 2011, 368:24-35.