Hantaviruses

Charles F. Fulhorst; Michael D. Bowen

doi:10.1128/9781555816728.ch94

Chapter 94 : Hantaviruses

Authors: Charles F. Fulhorst, Michael D. Bowen

Content Type: Reference

Publication Year: 2011

Category: Clinical Microbiology

Book DOI: 10.1128/9781555816728

Chapter DOI: 10.1128/9781555816728.ch94

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:

Hantaviruses, Page 1 of 2

< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555816728/9781555814632_Chap94-1.gif /docserver/preview/fulltext/10.1128/9781555816728/9781555814632_Chap94-2.gif

Abstract:

The hemorrhagic fever with renal syndrome (HFRS) and hantavirus pulmonary syndrome (HPS) are rodent-borne zoonoses caused by certain members of the virus family Bunyaviridae, genus Hantavirus. Specific rodents (i.e., one or two closely related members of the order Rodentia) are the principal hosts of the hantaviruses known to cause human disease. The reverse transcription-PCR (RT-PCR) assays have been employed extensively to detect hantaviral RNA in clinical samples from HPS and HFRS patients and to obtain amplified products for viral characterization by DNA sequencing. Hantaviruses usually are extremely difficult to isolate from clinical materials. Thus, virus isolation is not commonly used for the diagnosis of hantaviral infections in humans. Neutralization of infectivity in vitro, immunofluorescent-antibody assays (IFAs), enzyme-linked immunosorbent assays (ELISAs), and a host of other serologic methods have been used to characterize hantaviruses isolated from clinical samples and rodents. The use of genetic sequence data to define taxonomic relationships within the genus Hantavirus has become increasingly important, in part because some hantaviruses have never been adapted to growth in cultured cells and because our knowledge of the serologic relationships among some of the hantaviral species is based on one strain per species. Early diagnosis is critical to the successful management of HFRS and HPS and, at least in the case of HPS caused by Andes virus, implementation of appropriate isolation procedures to prevent virus transmission to health care providers and other people.

Citation: Fulhorst C, Bowen M. 2011. Hantaviruses, p 1504-1513. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch94

Key Concept Ranking

Sin nombre virus: 0.57785004
Hemorrhagic Fever With Renal Syndrome: 0.44218794

0.57785004

Highlighted Text: Show | Hide

Full text loading...

Figures

Hantaviruses

[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555816728.chap94-1,webId=/content/author/10.1128/9781555816728.chap94-1,properties={foaf_givenname=Charles F., foaf_name=Charles F. Fulhorst, foaf_surname=Fulhorst}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555816728.chap94-2,webId=/content/author/10.1128/9781555816728.chap94-2,properties={foaf_givenname=Michael D., foaf_name=Michael D. Bowen, foaf_surname=Bowen}]]

/content/10.1128/9781555816728.chap94.fig94-1

FIGURE 1

Electron micrograph of negatively stained Sin Nombre virus (2% phosphotungstic acid stain, pH 6.5). Courtesy of Charles Humphrey, Centers for Disease Control and Prevention. Humans usually become infected with hantaviruses by inhalation of aerosolized droplets of urine, saliva, or respiratory secretions from infected rodents or inhalation of aerosolized particles of feces, dust, or other organic matter contaminated with secretions or excretions from infected rodents. The aerosol transmission of hantaviruses from rodents to humans has been well documented (49, 110). Other means of infection include contamination of cutaneous injuries with infectious virus, contact of infectious materials with mucous membranes, ingestion of food contaminated with infectious rodent secretions or excretions, laboratory-acquired infections ( 7 , 49 , 58 , 63 , 118 ), and—only in the case of Andes virus—contact with an HPS patient during the acute phase of illness ( 84 ). Note that person-to-person hantavirus transmission has never been documented in Europe, Asia, or North America.

10.1128/9781555816728/fig94-1_thmb.gif

10.1128/9781555816728/fig94-1.gif

FIGURE 1

/content/10.1128/9781555816728.chap94.fig94-2

FIGURE 2

Photomicrograph of human lung tissue showing hantaviral antigens in pulmonary microvasculature by using immunohistochemistry. Viral antigens are stained in red. Courtesy of Sherif Zaki, Centers for Disease Control and Prevention.

10.1128/9781555816728/fig94-2_thmb.gif

10.1128/9781555816728/fig94-2.gif

FIGURE 2

References

/content/book/10.1128/9781555816728.chap94

1. Aitichou, M.,, S. S. Saleh,, A. K. McElroy,, C. Schmaljohn,, and M. S. Ibrahim. 2005. Identification of Dobrava, Hantaan, Seoul, and Puumala viruses by one-step real-time RT-PCR. J. Virol. Methods 124: 21– 26.

2. Armstrong, L. R.,, S. R. Zaki,, M. J. Goldoft,, R. L. Todd,, A. S. Khan,, R. F. Khabbaz,, T. G. Ksiazek,, and C. J. Peters. 1995. Hantavirus pulmonary syndrome associated with entering or cleaning rarely used, rodent-infested structures. J. Infect. Dis. 172: 1166.

3. Bharadwaj, M.,, R. Nofchissey,, D. Goade,, F. Koster,, and B. Hjelle. 2000. Humoral immune responses in the hantavirus cardiopulmonary syndrome. J. Infect. Dis. 182: 43– 48.

4. Biel, S. S.,, O. Donoso Mantke,, K. Lemmer,, A. Vaheri,, A. Lundkvist,, P. Emmerich,, M. Hukic,, and M. Niedrig. 2003. Quality control measures for the serological diagnosis of hantavirus infections. J. Clin. Virol. 28: 248– 256.

5. Bostik, P.,, J. Winter,, T. G. Ksiazek,, P. E. Rollin,, F. Villinger,, S. R. Zaki,, C. J. Peters,, and A. A. Ansari. 2000. Sin Nombre virus (SNV) Ig isotype antibody response during acute and convalescent phases of hantavirus pulmonary syndrome. Emerg. Infect. Dis. 6: 184– 187.

6. Castillo, C.,, J. Naranjo,, A. Sepulveda,, G. Ossa,, and H. Levy. 2001. Hantavirus pulmonary syndrome due to Andes virus in Temuco, Chile: clinical experience with 16 adults. Chest 120: 548– 554.

7.Centers for Disease Control and Prevention. 1994. Laboratory management of agents associated with hantavirus pulmonary syndrome: interim biosafety guidelines. MMWR Recommend. Rep. 43: 1– 7.

8. Chapman, L. E.,, G. J. Mertz,, C. J. Peters,, H. M. Jolson,, A. S. Khan,, T. G. Ksiazek,, F. T. Koster,, K. F. Baum,, P. E. Rollin,, A. T. Pavia,, R. C. Holman,, J. C. Christenson,, P. J. Rubin,, R. E. Behrman,, L. J. Bell,, G. L. Simpson,, R. F. Sadek, and the Ribavirin Study Group. 1999. Intravenous ribavirin for hantavirus pulmonary syndrome: safety and tolerance during 1 year of open-label experience. Antivir. Ther. 4: 211– 219.

9. Cho, H. W.,, C. R. Howard,, and H. W. Lee. 2002. Review of an inactivated vaccine against hantaviruses . Intervirology 45: 328– 333.

10. Choi, Y.,, C. J. Ahn,, K. M. Seong,, M. Y. Jung,, and B. Y. Ahn. 2003. Inactivated Hantaan virus vaccine derived from suspension culture of Vero cells. Vaccine 21: 1867– 1873.

11. Chu, Y. K.,, G. Jennings,, A. Schmaljohn,, F. Elgh,, B. Hjelle,, H. W. Lee,, S. Jenison,, T. Ksiazek,, C. J. Peters,, P. Rollin,, and C. S. Schmaljohn. 1995. Cross-neutralization of hantaviruses with immune sera from experimentally infected animals and from hemorrhagic fever with renal syndrome and hantavirus pulmonary syndrome patients. J. Infect. Dis. 172: 1581– 1584.

12. Chu, Y. K.,, C. Rossi,, J. W. Leduc,, H. W. Lee,, C. S. Schmaljohn,, and J. M. Dalrymple. 1994. Serological relationships among viruses in the Hantavirus genus, family Bunyaviridae. Virology 198: 196– 204.

13. Clement, J.,, P. McKenna,, J. Groen,, A. Osterhaus,, P. Colson,, T. Vervoort,, G. Preventionen,, and H. W. Lee. 1995. Epidemiology and laboratory diagnosis of hantavirus (HTV) infections. Acta Clin. Belg. 50: 9– 19.

14. Clement, J.,, and P. McKenna,. 1998. Hantaviruses, p. 331– 351. In S. R. Palmer,, E. J. L. Soulsby,, and D. I. H. Simpson (ed.), Zoonoses, Biology, Clinical Practice and Public Health Control. Oxford University Press, New York, NY.

15. Crowcroft, N. S.,, A. Infuso,, D. Ilef,, B. Le Guenno,, J. C. Desenclos,, F. Van Loock,, and J. Clement. 1999. Risk factors for human hantavirus infection: Franco-Belgian collaborative case-control study during 1995-6 epidemic. Br. Med. J. 318: 1737– 1738.

16. Custer, D. M.,, E. Thompson,, C. S. Schmaljohn,, T. G. Ksiazek,, and J. W. Hooper. 2003. Active and passive vaccination against hantavirus pulmonary syndrome with Andes virus M genome segment-based DNA vaccine. J. Virol. 77: 9894– 9905.

16a.. Department of Health and Human Services. 2009. Biosafety in Microbiological and Biomedical Laboratories, 5th ed. U.S. Government Printing Office, Washington, DC. http://www. cdc.gov/biosafety/publications/bmbl5/BMBL.pdf.

17. Duchin, J. S.,, F. T. Koster,, C. J. Peters,, G. L. Simpson,, B. Tempest,, S. R. Zaki,, T. G. Ksiazek,, P. E. Rollin,, S. Nichol,, E. T. Umland,, R. L. Moolenaar,, S. E. Reef,, K. B. Nolte,, M. M. Gallaher,, J. C. Butler,, R. F. Breiman, and The Hantavirus Study Group. 1994. Hantavirus pulmonary syndrome: a clinical description of 17 patients with a newly recognized disease. N. Engl. J. Med. 330: 949– 955.

18. Dzagurova, T. K.,, B. Klempa,, E. A. Tkachenko,, G. P. Slyusareva,, V. G. Morozov,, B. Auste,, and D. H. Kruger. 2009. Molecular diagnostics of hemorrhagic fever with renal syndrome during a Dobrava virus infection outbreak in the European part of Russia. J. Clin. Microbiol. 47: 4029– 4036.

19. Elgh, F.,, M. Linderholm,, G. Wadell,, A. Tarnvik,, and P. Juto. 1998. Development of humoral cross-reactivity to the nucleocapsid protein of heterologous hantaviruses in nephropathia epidemica. FEMS Immunol. Med. Microbiol. 22: 309– 315.

20. Elgh, F.,, G. Wadell,, and P. Juto. 1995. Comparison of the kinetics of Puumala virus specific IgM and IgG antibody responses in nephropathia epidemica as measured by a recombinant antigen-based enzyme-linked immunosorbent assay and an immunofluorescence test. J. Med.Virol. 45: 146– 150.

21. Evander, M.,, I. Eriksson,, L. Pettersson,, P. Juto,, C. Ahlm,, G. E. Olsson,, G. Bucht,, and A. Allard. 2007. Puumala hantavirus viremia diagnosed by real-time reverse transcriptase PCR using samples from patients with hemorrhagic fever and renal syndrome. J. Clin. Microbiol. 45: 2491– 2497.

22. Fabbri, M.,, and M. J. Maslow. 2001. Hantavirus pulmonary syndrome in the United States. Curr. Infect. Dis. Rep. 3: 258– 265.

22a.. Federal Register. 2002. Hazardous materials: revision to standards for infectious substances, final rule. Fed. Regist. 67: 53118– 53144.

22b.. Federal Register. 2006. Hazardous materials: infectious substances; harmonization with the United Nations Recommendations, final rule. Fed. Regist. 71: 32244– 32263.

23. Feldmann, H.,, A. Sanchez,, S. Morzunov,, C. F. Spiropoulou,, P. E. Rollin,, T. G. Ksiazek,, C. J. Peters,, and S. T. Nichol. 1993. Utilization of autopsy RNA for the synthesis of the nucleocapsid antigen of a newly recognized virus associated with hantavirus pulmonary syndrome. Virus Res. 30: 351– 367.

24. Galeno, H.,, J. Mora,, E. Villagra,, J. Fernandez,, J. Hernandez,, G. J. Mertz,, and E. Ramirez. 2002. First human isolate of Hantavirus (Andes virus) in the Americas. Emerg. Infect. Dis. 8: 657– 661.

25. Garin, D.,, C. Peyrefitte,, J. M. Crance,, A. Le Faou,, A. Jouan,, and M. Bouloy. 2001. Highly sensitive Taqman PCR detection of Puumala hantavirus. Microbes Infect. 3: 739– 745.

26. Gavrilovskaya, I. N.,, M. Shepley,, R. Shaw,, M. H. Ginsberg,, and E. R. Mackow. 1998. ?3 Integrins mediate the cellular entry of hantaviruses that cause respiratory failure. Proc. Natl. Acad. Sci. USA 95: 7074– 7079.

27. Godoy, P.,, D. Marsac,, E. Stefas,, P. Ferrer,, N. D. Tischler,, K. Pino,, P. Ramdohr,, P. Vial,, P. D. Valenzuela,, M. Ferres,, F. Veas,, and M. Lopez-Lastra. 2009. Andes virus antigens are shed in urine of patients with acute hantavirus cardiopulmonary syndrome. J. Virol. 83: 5046– 5055.

28. Gott, P.,, R. Stohwasser,, P. Schnitzler,, G. Darai,, and E. K. Bautz. 1993. RNA binding of recombinant nucleocapsid proteins of hantaviruses. Virology 194: 332– 337.

29. Groen, J.,, J. Dalrymple,, S. Fisher-Hoch,, J. G. Jordans,, J. P. Clement,, and A. D. Osterhaus. 1992. Serum antibodies to structural proteins of Hantavirus arise at different times after infection. J. Med. Virol. 37: 283– 287.

30. Heider, H.,, B. Ziaja,, C. Priemer,, A. Lundkvist,, J. Neyts,, D. H. Kruger,, and R. Ulrich. 2001. A chemiluminescence detection method of hantaviral antigens in neutralisation assays and inhibitor studies. J. Virol. Methods 96: 17– 23.

31. Henderson, W. W.,, M. C. Monroe,, S. C. St. Jeor,, W. P. Thayer,, J. E. Rowe,, C. J. Peters,, and S. T. Nichol. 1995. Naturally occurring Sin Nombre virus genetic reassortants. Virology 214: 602– 610.

32. Hjelle, B. 2002. Vaccines against hantaviruses. Expert Rev. Vaccines 1: 373– 384.

33. Hjelle, B.,, F. Chavez-Giles,, N. Torrez-Martinez,, T. Yamada,, J. Sarisky,, M. Ascher,, and S. Jenison. 1994. Dominant glycoprotein epitope of Four Corners hantavirus is conserved across a wide geographical area. J. Gen. Virol. 75: 2881– 2888.

34. Hjelle, B.,, S. Jenison,, N. Torrez-Martinez,, T. Yamada,, K. Nolte,, R. Zumwalt,, K. MacInnes,, and G. Myers. 1994. A novel hantavirus associated with an outbreak of fatal respiratory disease in the southwestern United States: evolutionary relationships to known hantaviruses. J. Virol. 68: 592– 596.

35. Horling, J.,, A. Lundkvist,, J. W. Huggins,, and B. Niklasson. 1992. Antibodies to Puumala virus in humans determined by neutralization test. J. Virol. Methods 39: 139– 147.

36. Horling, J.,, A. Lundkvist,, K. Persson,, M. Mullaart,, T. Dzagurova,, A. Dekonenko,, E. Tkachenko,, and B. Niklasson. 1995. Detection and subsequent sequencing of Puumala virus from human specimens by PCR. J. Clin. Microbiol. 33: 277– 282.

37. Huggins, J. W.,, C. M. Hsiang,, T. M. Cosgriff,, M. Y. Guang,, J. I. Smith,, Z. O. Wu,, J. W. LeDuc,, Z. M. Zheng,, J. M. Meegan,, Q. N. Wang,, D. D. Oland,, X. E. Gui,, P. H. Gibbs,, G. H. Yuan,, and T. M. Zhang. 1991. Prospective, double-blind, concurrent, placebo-controlled clinical trial of intravenous ribavirin therapy of hemorrhagic fever with renal syndrome. J. Infect. Dis. 164: 1119– 1127.

38. Huggins, J. W.,, G. R. Kim,, O. M. Brand,, and K. T. McKee, Jr. 1986. Ribavirin therapy for Hantaan virus infection in suckling mice. J. Infect. Dis. 153: 489– 497.

39. Hujakka, H.,, V. Koistinen,, I. Kuronen,, P. Eerikainen,, M. Parviainen,, A. Lundkvist,, A. Vaheri,, O. Vapalahti,, and A. Narvanen. 2003. Diagnostic rapid tests for acute hantavirus infections: specific tests for Hantaan, Dobrava and Puumala viruses versus a hantavirus combination test. J. Virol. Methods 108: 117– 122.

40. Hung, T.,, J. Y. Zhou,, Y. M. Tang,, T. X. Zhao,, L. J. Baek,, and H. W. Lee. 1992. Identification of Hantaan virus-related structures in kidneys of cadavers with haemorrhagic fever with renal syndrome. Arch. Virol. 122: 187– 199.

41. Ivanov, A.,, O. Vapalahti,, H. Lankinen,, E. Tkachenko,, A. Vaheri,, B. Niklasson,, and A. Lundkvist. 1996. Biotinlabeled antigen: a novel approach for detection of Puumala virus-specific IgM. J. Virol. Methods 62: 87– 92.

42. Iversson, L. B.,, A. P. da Rosa,, M. D. Rosa,, A. V. Lomar,, G. Sasaki Mda,, and J. W. LeDuc. 1994. Human infection by Hantavirus in southern and southeastern Brazil. Rev. Assoc. Med. Bras. 40: 85– 92. (In Portuguese.)

43. Jaaskelainen, K. M.,, P. Kaukinen,, E. S. Minskaya,, A. Plyusnina,, O. Vapalahti,, R. M. Elliott,, F. Weber,, A. Vaheri,, and A. Plyusnin. 2007. Tula and Puumala hantavirus NSs ORFs are functional and the products inhibit activation of the interferon-beta promoter. J. Med. Virol. 79: 1527– 1536.

44. Jenison, S.,, T. Yamada,, C. Morris,, B. Anderson,, N. Torrez- Martinez,, N. Keller,, and B. Hjelle. 1994. Characterization of human antibody responses to Four Corners hantavirus infections among patients with hantavirus pulmonary syndrome. J. Virol. 68: 3000– 3006.

45. Johnson, A. M.,, M. D. Bowen,, T. G. Ksiazek,, R. J. Williams,, R. T. Bryan,, J. N. Mills,, C. J. Peters,, and S. T. Nichol. 1997. Laguna Negra virus associated with HPS in western Paraguay and Bolivia. Virology 238: 115– 127.

46. Kallio-Kokko, H.,, R. Leveelahti,, M. Brummer-Korvenkontio,, A. Lundkvist,, A. Vaheri,, and O. Vapalahti. 2001. Human immune response to Puumala virus glycoproteins and nucleocapsid protein expressed in mammalian cells. J. Med. Virol. 65: 605– 613.

47. Kallio-Kokko, H.,, A. Lundkvist,, A. Plyusnin,, T. Avsic- Zupanc,, A. Vaheri,, and O. Vapalahti. 2000. Antigenic properties and diagnostic potential of recombinant Dobrava virus nucleocapsid protein. J. Med. Virol. 61: 266– 274.

48. Kang, H. J.,, S. N. Bennett,, L. Sumibcay,, S. Arai,, A. G. Hope,, G. Mocz,, J. W. Song,, J. A. Cook,, and R. Yanagihara. 2009. Evolutionary insights from a genetically divergent hantavirus harbored by the European common mole (Talpa europaea). PLoS One 4: e6149.

49. Kawamata, J.,, T. Yamanouchi,, K. Dohmae,, H. Miyamoto,, M. Takahaski,, K. Yamanishi,, T. Kurata,, and H. W. Lee. 1987. Control of laboratory acquired hemorrhagic fever with renal syndrome (HFRS) in Japan. Lab. Anim. Sci. 37: 431– 436.

50. Khan, A. S.,, M. Gaviria,, P. E. Rollin,, W. G. Hlady,, T. G. Ksiazek,, L. R. Armstrong,, R. Greenman,, E. Ravkov,, M. Kolber,, H. Anapol,, E. D. Sfakianaki,, S. T. Nichol,, C. J. Peters,, and R. F. Khabbaz. 1996. Hantavirus pulmonary syndrome in Florida: association with the newly identified Black Creek Canal virus. Am. J. Med. 100: 46– 48.

51. Khan, A. S.,, C. F. Spiropoulou,, S. Morzunov,, S. R. Zaki,, M. A. Kohn,, S. R. Nawas,, L. McFarland,, and S. T. Nichol. 1995. Fatal illness associated with a new hantavirus in Louisiana. J. Med. Virol. 46: 281– 286.

52. Kitsutani, P. T.,, R. W. Denton,, C. L. Fritz,, R. A. Murray,, R. L. Todd,, W. J. Pape,, J. Wyatt Frampton,, J. C. Young,, A. S. Khan,, C. J. Peters,, and T. G. Ksiazek. 1999. Acute Sin Nombre hantavirus infection without pulmonary syndrome, United States. Emerg. Infect. Dis. 5: 701– 705.

53. Koster, F.,, K. Foucar,, B. Hjelle,, A. Scott,, Y. Y. Chong,, R. Larson,, and M. McCabe. 2001. Rapid presumptive diagnosis of hantavirus cardiopulmonary syndrome by peripheral blood smear review. Am. J. Clin. Pathol. 116: 665– 672.

54. Koster, F. T.,, and H. Levy. 2007. Hantavirus Cardiopulmonary Syndrome: a New Twist to an Established Pathogen. Springer, New York, NY.

55. Kraus, A. A.,, C. Priemer,, H. Heider,, D. H. Kruger,, and R. Ulrich. 2005. Inactivation of Hantaan virus-containing samples for subsequent investigations outside biosafety level 3 facilities. Intervirology 48: 255– 261.

56. Ksiazek, T. G.,, C. J. Peters,, P. E. Rollin,, S. Zaki,, S. Nichol,, C. Spiropoulou,, S. Morzunov,, H. Feldmann,, A. Sanchez,, A. S. Khan,, B. W. J. Mahy,, K. Wachsmuth,, and J. C. Butler. 1995. Identification of a new North American hantavirus that causes acute pulmonary insufficiency. Am. J. Trop. Med. Hyg. 52: 117– 123.

57. LeDuc, J. W.,, T. G. Ksiazek,, C. A. Rossi,, and J. M. Dalrymple. 1990. A retrospective analysis of sera collected by the Hemorrhagic Fever Commission during the Korean Conflict. J. Infect. Dis. 162: 1182– 1184.

58. Lee, H. W.,, and K. M. Johnson. 1982. Laboratory-acquired infections with Hantaan virus, the etiologic agent of Korean hemorrhagic fever. J. Infect. Dis. 146: 645– 651.

59. Lee, H. W.,, and G. van der Groen. 1989. Hemorrhagic fever with renal syndrome. Prog. Med. Virol. 36: 62– 102.

60. Lee, P. W.,, C. J. Gibbs, Jr.,, D. C. Gajdusek,, and R. Yanagihara. 1985. Serotypic classification of hantaviruses by indirect immunofluorescent antibody and plaque reduction neutralization tests. J. Clin. Microbiol. 22: 940– 944.

61. Li, D.,, A. L. Schmaljohn,, K. Anderson,, and C. S. Schmaljohn. 1995. Complete nucleotide sequences of the M and S segments of two hantavirus isolates from California: evidence for reassortment in nature among viruses related to hantavirus pulmonary syndrome. Virology 206: 973– 983.

62. Linderholm, M.,, and F. Elgh. 2001. Clinical characteristics of hantavirus infections on the Eurasian continent. Curr. Top. Microbiol. Immunol. 256: 135– 151.

63. Lloyd, G.,, and N. Jones. 1986. Infection of laboratory workers with hantavirus acquired from immunocytomas propagated in laboratory rats. J. Infect. 12: 117– 125.

64. Lopez, N.,, P. Padula,, C. Rossi,, M. E. Lazaro,, and M. T. Franze-Fernandez. 1996. Genetic identification of a new hantavirus causing severe pulmonary syndrome in Argentina. Virology 220: 223– 226.

65. Lu, Q.,, Z. Zhu,, and J. Weng. 1996. Immune responses to inactivated vaccine in people naturally infected with hantaviruses. J. Med. Virol. 49: 333– 335.

66. Lukes, R. 1954. The pathology of thirty-nine fatal cases of epidemic hemorrhagic fever. Am. J. Med. 16: 639– 650.

67. Lundkvist, A.,, S. Bjorsten,, and B. Niklasson. 1993. Immunoglobulin G subclass responses against the structural components of Puumala virus. J. Clin. Microbiol. 31: 368– 372.

68. Lundkvist, A.,, M. Hukic,, J. Horling,, M. Gilljam,, S. Nichol,, and B. Niklasson. 1997. Puumala and Dobrava viruses cause hemorrhagic fever with renal syndrome in Bosnia-Herzegovina: evidence of highly cross-neutralizing antibody responses in early patient sera. J. Med. Virol. 53: 51– 59.

69. Lundkvist, A.,, D. Wiger,, J. Horling,, K. B. Sjolander,, A. Plyusnina,, R. Mehl,, A. Vaheri,, and A. Plyusnin. 1998. Isolation and characterization of Puumala hantavirus from Norway: evidence for a distinct phylogenetic sublineage. J. Gen. Virol. 79( Pt. 11): 2603– 2614.

70. Maes, P.,, J. Clement,, and M. Van Ranst. 2009. Recent approaches in hantavirus vaccine development. Expert Rev. Vaccines 8: 67– 76.

71. Maes, P.,, E. Keyaerts,, J. Clement,, V. Bonnet,, A. Robert,, and M. Van Ranst. 2004. Detection of Puumala hantavirus antibody with ELISA using a recombinant truncated nucleocapsid protein expressed in Escherichia coli. Viral Immunol. 17: 315– 321.

72. Maes, P.,, B. Klempa,, J. Clement,, J. Matthijnssens,, D. C. Gajdusek,, D. H. Kruger,, and M. Van Ranst. 2009. A proposal for new criteria for the classification of hantaviruses, based on S and M segment protein sequences. Infect. Genet. Evol. 9: 813– 820.

73. Maes, P.,, S. Li,, J. Verbeeck,, E. Keyaerts,, J. Clement,, and M. Van Ranst. 2007. Evaluation of the efficacy of disinfectants against Puumala hantavirus by real-time RT-PCR. J. Virol. Methods 141: 111– 115.

74. Martin, M. L.,, H. Lindsey-Regnery,, D. R. Sasso,, J. B. McCormick,, and E. Palmer. 1985. Distinction between Bunyaviridae genera by surface structure and comparison with Hantaan virus using negative stain electron microscopy. Arch. Virol. 86: 17– 28.

75. Mills, J. N.,, B. R. Amman,, and G. E. Glass. 2010. Ecology of hantaviruses and their hosts in North America. Vector Borne Zoonotic Dis. 10: 563– 574.

76. Mills, J. N.,, A. Corneli,, J. C. Young,, L. E. Garrison,, A. S. Khan,, and T. G. Ksiazek. 2002. Hantavirus pulmonary syndrome—United States: updated recommendations for risk reduction. MMWR Recommend. Rep. 51: 1– 12.

77. Monroe, M. C.,, S. P. Morzunov,, A. M. Johnson,, M. D. Bowen,, H. Artsob,, T. Yates,, C. J. Peters,, P. E. Rollin,, T. G. Ksiazek,, and S. T. Nichol. 1999. Genetic diversity and distribution of Peromyscus-borne hantaviruses in North America. Emerg. Infect. Dis. 5: 75– 86.

78. Morzunov, S. P.,, J. E. Rowe,, T. G. Ksiazek,, C. J. Peters,, S. C. St. Jeor,, and S. T. Nichol. 1998. Genetic analysis of the diversity and origin of hantaviruses in Peromyscus leucopus mice in North America. J. Virol. 72: 57– 64.

79. Nichol, S. T.,, B. J. Beaty,, R. M. Elliott,, R. Goldbach,, A. Plyusnin,, C. S. Schmaljohn,, and R. B. Tesh,. 2005. Family Bunyaviridae, p. 695– 716. In C. M. Fauquet,, M. A. Mayo,, J. Maniloff,, U. Desselberger,, and L. A. Ball (ed.), Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, San Diego, CA.

80. Nichol, S. T.,, C. F. Spiropoulou,, S. Morzunov,, P. E. Rollin,, T. G. Ksiazek,, H. Feldmann,, A. Sanchez,, J. Childs,, S. Zaki,, and C. J. Peters. 1993. Genetic identification of a hantavirus associated with an outbreak of acute respiratory illness. Science 262: 914– 917.

81. Niklasson, B.,, M. Jonsson,, A. Lundkvist,, J. Horling,, and E. Tkachenko. 1991. Comparison of European isolates of viruses causing hemorrhagic fever with renal syndrome by a neutralization test. Am. J. Trop. Med. Hyg. 45: 660– 665.

82. Niklasson, B.,, and T. Kjelsson. 1988. Detection of nephropathia epidemica (Puumala virus)-specific immunoglobulin M by enzyme-linked immunosorbent assay. J. Clin. Microbiol. 26: 1519– 1523.

83. Nolte, K. B.,, R. M. Feddersen,, K. Foucar,, S. R. Zaki,, F. T. Koster,, D. Madar,, T. L. Merlin,, P. J. McFeeley,, E. T. Umland,, and R. E. Zumwalt. 1995. Hantavirus pulmonary syndrome in the United States: a pathological description of a disease caused by a new agent. Hum. Pathol. 26: 110– 120.

84. Padula, P. J.,, A. Edelstein,, S. D. Miguel,, N. M. Lopez,, C. M. Rossi,, and R. D. Rabinovich. 1998. Hantavirus pulmonary syndrome outbreak in Argentina: molecular evidence for person-to-person transmission of Andes virus. Virology 241: 323– 330.

85. Padula, P. J.,, C. M. Rossi,, M. O. Della Valle,, P. V. Martinez,, S. B. Colavecchia,, A. Edelstein,, S. D. Miguel,, R. D. Rabinovich,, and E. L. Segura. 2000. Development and evaluation of a solid-phase enzyme immunoassay based on Andes hantavirus recombinant nucleoprotein. J. Med. Microbiol. 49: 149– 155.

86. Papa, A.,, H. Zelena,, D. Barnetova,, and L. Petrousova. 2010. Genetic detection of Dobrava/Belgrade virus in a Czech patient with haemorrhagic fever with renal syndrome. Clin. Microbiol. Infect. 16: 1187– 1190.

87. Park, K.,, C. S. Kim,, and K. T. Moon. 2004. Protective effectiveness of hantavirus vaccine. Emerg. Infect. Dis. 10: 2218– 2220.

88. Plyusnin, A. 2002. Genetics of hantaviruses: implications to taxonomy. Arch. Virol. 147: 665– 682.

89. Plyusnin, A.,, Y. Cheng,, O. Vapalahti,, M. Pejcoch,, J. Unar,, Z. Jelinkova,, H. Lehvaslaiho,, A. Lundkvist,, and A. Vaheri. 1995. Genetic variation in Tula hantaviruses: sequence analysis of the S and M segments of strains from Central Europe. Virus Res. 39: 237– 250.

90. Plyusnin, A.,, and S. P. Morzunov. 2001. Virus evolution and genetic diversity of hantaviruses and their rodent hosts. Curr. Top. Microbiol. Immunol. 256: 47– 75

91. Plyusnin, A.,, A. Vaheri,, and A. Lundkvist. 2006. Saaremaa hantavirus should not be confused with its dangerous relative, Dobrava virus. J. Clin. Microbiol. 44:1608-1609. (Author’s reply, 44: 1609– 1611.)

92. Plyusnin, A.,, O. Vapalahti,, and A. Vaheri. 1996. Hantaviruses: genome structure, expression and evolution. J. Gen. Virol. 77: 2677– 2687.

93. Puerta, H.,, C. Cantillo,, J. Mills,, B. Hjelle,, J. Salazar-Bravo,, and S. Mattar. 2006. The new-world hantaviruses. Ecology and epidemiology of an emerging virus in Latin America. Medicina (Buenos Aires) 66: 343– 356. (In Spanish.)

94. Ramsden, C.,, E. C. Holmes,, and M. A. Charleston. 2009. Hantavirus evolution in relation to its rodent and insectivore hosts: no evidence for codivergence. Mol. Biol. Evol. 26: 143– 153.

95. Richmond, J. Y.,, and R. W. McKinney (ed.). 1999. Biosafety in Microbiological and Biomedical Laboratories, 4th ed. U.S. Government Printing Office, Washington, DC.

96. Riquelme, R.,, M. Riquelme,, A. Torres,, M. L. Rioseco,, J. A. Vergara,, L. Scholz,, and A. Carriel. 2003. Hantavirus pulmonary syndrome, southern Chile. Emerg. Infect. Dis. 9: 1438– 1443.

97. Rusnak, J. M.,, W. R. Byrne,, K. N. Chung,, P. H. Gibbs,, T. T. Kim,, E. F. Boudreau,, T. Cosgriff,, P. Pittman,, K. Y. Kim,, M. S. Erlichman,, D. F. Rezvani,, and J. W. Huggins. 2009. Experience with intravenous ribavirin in the treatment of hemorrhagic fever with renal syndrome in Korea. Antivir. Res. 81: 68– 76.

98. Saksida, A.,, D. Duh,, M. Korva,, and T. Avsic-Zupanc. 2008. Dobrava virus RNA load in patients who have hemorrhagic fever with renal syndrome. J. Infect. Dis. 197: 681– 685.

99. Saluzzo, J. F.,, B. Leguenno,, and G. van der Groen. 1988. Use of heat inactivated viral haemorrhagic fever antigens in serological assays. J. Virol. Methods 22: 165– 172.

100. Schmaljohn, C. 2009. Vaccines for hantaviruses. Vaccine 27( Suppl. 4): D61– D64.

101. Schmidt, J.,, B. Jandrig,, B. Klempa,, K. Yoshimatsu,, J. Arikawa,, H. Meisel,, M. Niedrig,, C. Pitra,, D. H. Kruger,, and R. Ulrich. 2005. Nucleocapsid protein of cell culture-adapted Seoul virus strain 80-39: analysis of its encoding sequence, expression in yeast and immuno-reactivity. Virus Genes 30: 37– 48.

102. Schwarz, T. F.,, S. R. Zaki,, S. Morzunov,, C. J. Peters,, and S. T. Nichol. 1995. Detection and sequence confirmation of Sin Nombre virus RNA in paraffin-embedded human tissues using one-step RT-PCR. J. Virol. Methods 51: 349– 356.

103. Severson, W. E.,, C. S. Schmaljohn,, A. Javadian,, and C. B. Jonsson. 2003. Ribavirin causes error catastrophe during Hantaan virus replication. J. Virol. 77: 481– 488.

104. Sibold, C.,, H. Meisel,, D. H. Kruger,, M. Labuda,, J. Lysy,, O. Kozuch,, M. Pejcoch,, A. Vaheri,, and A. Plyusnin. 1999. Recombination in Tula hantavirus evolution: analysis of genetic lineages from Slovakia. J. Virol. 73: 667– 675.

105. Sironen, T.,, A. Vaheri,, and A. Plyusnin. 2001. Molecular evolution of Puumala hantavirus. J. Virol. 75: 11803– 11810.

106. Sjolander, K. B.,, and A. Lundkvist. 1999. Dobrava virus infection: serological diagnosis and cross-reactions to other hantaviruses. J. Virol. Methods 80: 137– 143.

107. Sohn, Y. M.,, H. O. Rho,, M. S. Park,, J. S. Kim,, and P. L. Summers. 2001. Primary humoral immune responses to formalin inactivated hemorrhagic fever with renal syndrome vaccine (Hantavax): consideration of active immunization in South Korea. Yonsei Med. J. 42: 278– 284.

108. Song, G.,, Y. C. Huang,, C. S. Hang,, F. Y. Hao,, D. X. Li,, X. L. Zheng,, W. M. Liu,, S. L. Li,, Z. W. Huo,, L. J. Huei,, and Q. F. Zhang. 1992. Preliminary human trial of inactivated golden hamster kidney cell (GHKC) vaccine against haemorrhagic fever with renal syndrome (HFRS). Vaccine 10: 214– 216.

109. Song, J. W.,, L. J. Baek,, C. S. Schmaljohn,, and R. Yanagihara. 2007. Thottapalayam virus, a prototype shrewborne hantavirus. Emerg. Infect. Dis. 13: 980– 985.

110. Tsai, T. F. 1987. Hemorrhagic fever with renal syndrome: mode of transmission to humans. Lab. Anim. Sci. 37: 428– 430.

111. Vaheri, A.,, O. Vapalahti,, and A. Plyusnin. 2008. How to diagnose hantavirus infections and detect them in rodents and insectivores. Rev. Med. Virol. 18: 277– 288.

112. Valdivieso, F.,, P. Vial,, M. Ferres,, C. Ye,, D. Goade,, A. Cuiza,, and B. Hjelle. 2006. Neutralizing antibodies in survivors of Sin Nombre and Andes hantavirus infection. Emerg. Infect. Dis. 12: 166– 168.

113. Van Loock, F.,, I. Thomas,, J. Clement,, S. Ghoos,, and P. Colson. 1999. A case-control study after a hantavirus infection outbreak in the south of Belgium: who is at risk? Clin. Infect. Dis. 28: 834– 839.

114. Vapalahti, O.,, 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,, and A. Plyusnin. 1999. Isolation and characterization of a hantavirus from Lemmus sibiricus: evidence for host switch during hantavirus evolution. J. Virol. 73: 5586– 5592.

115. Vapalahti, O.,, J. Mustonen,, A. Lundkvist,, H. Henttonen,, A. Plyusnin,, and A. Vaheri. 2003. Hantavirus infections in Europe. Lancet Infect. Dis. 3: 653– 661.

116. Weidmann, M.,, P. Schmidt,, M. Vackova,, K. Krivanec,, P. Munclinger,, and F. T. Hufert. 2005. Identification of genetic evidence for Dobrava virus spillover in rodents by nested reverse transcription (RT)-PCR and TaqMan RTPCR. J. Clin. Microbiol. 43: 808– 812.

117. Wells, R. M.,, S. Sosa Estani,, Z. E. Yadon,, D. Enria,, P. Padula,, N. Pini,, J. N. Mills,, C. J. Peters,, E. L. Segura, and the Hantavirus Pulmonary Syndrome Study Group for Patagonia. 1997. An unusual hantavirus outbreak in southern Argentina: person-to-person transmission? Emerg. Infect. Dis. 3: 171– 174.

118. Wong, T. W.,, Y. C. Chan,, E. H. Yap,, Y. G. Joo,, H. W. Lee,, P. W. Lee,, R. Yanagihara,, C. J. Gibbs, Jr.,, and D. C. Gajdusek. 1988. Serological evidence of hantavirus infection in laboratory rats and personnel. Int. J. Epidemiol. 17: 887– 890.

119. Woods, C.,, R. Palekar,, P. Kim,, D. Blythe,, O. de Senarclens,, K. Feldman,, E. C. Farnon,, P. E. Rollin,, C. G. Albarino,, S. T. Nichol,, and M. Smith. 2009. Domestically acquired Seoul virus causing hemorrhagic fever with renal syndrome—Maryland, 2008. Clin. Infect. Dis. 49: e109– e112.

120. Xiao, R.,, S. Yang,, F. Koster,, C. Ye,, C. Stidley,, and B. Hjelle. 2006. Sin Nombre viral RNA load in patients with hantavirus cardiopulmonary syndrome. J. Infect. Dis. 194: 1403– 1409.

121. Xiao, S. Y.,, Y. K. Chu,, F. K. Knauert,, R. Lofts,, J. M. Dalrymple,, and J. W. LeDuc. 1992. Comparison of hantavirus isolates using a genus-reactive primer pair polymerase chain reaction. J. Gen. Virol. 73: 567– 573.

122. Xiao, S. Y.,, J. W. Leduc,, Y. K. Chu,, and C. S. Schmaljohn. 1994. Phylogenetic analyses of virus isolates in the genus Hantavirus, family Bunyaviridae. Virology 198: 205– 217.

123. Yamanishi, K.,, O. Tanishita,, M. Tamura,, H. Asada,, K. Kondo,, M. Takagi,, I. Yoshida,, T. Konobe,, and K. Fukai. 1988. Development of inactivated vaccine against virus causing haemorrhagic fever with renal syndrome. Vaccine 6: 278– 282.

124. Yashina, L. N.,, N. A. Patrushev,, L. I. Ivanov,, R. A. Slonova,, V. P. Mishin,, G. G. Kompanez,, N. I. Zdanovskaya,, I. I. Kuzina,, P. F. Safronov,, V. E. Chizhikov,, C. Schmaljohn,, and S. V. Netesov. 2000. Genetic diversity of hantaviruses associated with hemorrhagic fever with renal syndrome in the far east of Russia. Virus Res. 70: 31– 44.

125. Ye, C.,, J. Prescott,, R. Nofchissey,, D. Goade,, and B. Hjelle. 2004. Neutralizing antibodies and Sin Nombre virus RNA after recovery from hantavirus cardiopulmonary syndrome. Emerg. Infect. Dis. 10: 478– 482.

126. Zaki, S. R.,, P. W. Greer,, L. M. Coffield,, C. S. Goldsmith,, K. B. Nolte,, K. Foucar,, R. M. Feddersen,, R. E. Zumwalt,, G. L. Miller,, A. S. Khan,, P. E. Rollin,, T. G. Ksiazek,, S. T. Nichol,, B. W. J. Mahy,, and C. J. Peters. 1995. Hantavirus pulmonary syndrome. Pathogenesis of an emerging infectious disease. Am. J. Pathol. 146: 552– 579.

127. Zaki, S. R.,, A. S. Khan,, R. A. Goodman,, L. R. Armstrong,, P. W. Greer,, L. M. Coffield,, T. G. Ksiazek,, P. E. Rollin,, C. J. Peters,, and R. F. Khabbaz. 1996. Retrospective diagnosis of hantavirus pulmonary syndrome, 1978-1993: implications for emerging infectious diseases. Arch. Pathol. Lab. Med. 120: 134– 139.

Tables

Hantaviruses

/content/10.1128/9781555816728.chap94.tab94-1

TABLE 1

Hantaviral species associated with human disease a

a Adapted from references 54 , 79 , 91 , 93 , and 124 . Amur virus has been associated with HFRS in eastern Russia; Apodemus peninsulae is the natural host. Additional hantaviruses associated with HPS include Monongahela virus in the United States; Central Plata virus in Uruguay; Choclo virus in Panama; Bermejo, Lechiguanas, and Oran viruses in Argentina; and Anajatuba, Araraquara, Castelo dos Sonhos, and Juquitiba viruses in Brazil. Monongahela virus is a strain of Sin Nombre virus, and Bermejo, Lechiguanas, and Oran viruses are considered strains of Andes virus. Sigmodontine rodents are the natural hosts of Anajatuba, Araraquara, Bermejo, Central Plata, Choclo, Juquitiba, Lechiguanas, and Oran viruses. The natural host of Castelo dos Sonhos virus is not known.

b Murinae, Old World rats and mice; Arvicolinae, voles and lemmings; Sigmodontinae and Neotominae, New World rats and mice.

10.1128/9781555816728/tab94-1_thmb.gif

10.1128/9781555816728/tab94-1.gif

TABLE 1

Hantaviral species associated with human disease a

b Murinae, Old World rats and mice; Arvicolinae, voles and lemmings; Sigmodontinae and Neotominae, New World rats and mice.