Skip to main content
PMC home page
Virologica Sinica logoLink to Virologica Sinica
. 2017 Jan 23;32(1):32–43. doi: 10.1007/s12250-016-3899-x

Hantavirus infection: a global zoonotic challenge

Hong Jiang 1, Xuyang Zheng 1, Limei Wang 2, Hong Du 1, Pingzhong Wang 1,✉, Xuefan Bai 1,✉
PMCID: PMC6598904  PMID: 28120221

Abstract

Hantaviruses are comprised of tri-segmented negative sense single-stranded RNA, and are members of the Bunyaviridae family. Hantaviruses are distributed worldwide and are important zoonotic pathogens that can have severe adverse effects in humans. They are naturally maintained in specific reservoir hosts without inducing symptomatic infection. In humans, however, hantaviruses often cause two acute febrile diseases, hemorrhagic fever with renal syndrome (HFRS) and hantavirus cardiopulmonary syndrome (HCPS). In this paper, we review the epidemiology and epizootiology of hantavirus infections worldwide. graphic file with name 12250_2016_3899_Fig1_HTML.jpg

Keywords: hantavirus, Bunyaviridae, zoonosis, hemorrhagic fever with renal syndrome, hantavirus cardiopulmonary syndrome

Acknowledgments

The authors would like to thank Mr. An Yang from the Department of Foreign Languages, Fourth Military Medical University, China, for improving the English manuscript. This work was supported by the National Natural Science Foundation of China (No. 81373118) and the National Basic Research Programme of China (973 Programme No. 2012CB518905).

Footnotes

These authors contributed equally to this work.

ORCID: 0000-0002-4468-4729

ORCID: 0000-0003-4609-4877

Compliance with Ethical Guidelines

The authors declare that they have no conflict of interest. This article does not contain any studies with human or animal subjects performed by any of the authors.

Contributor Information

Pingzhong Wang, Email: wangpz63@126.com.

Xuefan Bai, Email: xfbai2011@163.com.

References

  1. Ali HS, Drewes S, Sadowska ET, Mikowska M, Groschup MH, Heckel G, Koteja P, Ulrich RG. First molecular evidence for Puumala hantavirus in Poland. Viruses. 2014;6:340–353. doi: 10.3390/v6010340. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arai S, Nguyen ST, Boldgiv B, Fukui D, Araki K, Dang CN, Ohdachi SD, Nguyen NX, Pham TD, Boldbaatar B, Satoh H, Yoshikawa Y, Morikawa S, Tanaka-Taya K, Yanagihara R, Oishi K. Novel bat-borne hantavirus, Vietnam. Emerg Infect Dis. 2013;19:1159–1161. doi: 10.3201/eid1907.121549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Arai S, Ohdachi SD, Asakawa M, Kang HJ, Mocz G, Arikawa J, Okabe N, Yanagihara R. Molecular phylogeny of a newfound hantavirus in the Japanese shrew mole (Urotrichus talpoides) Proc Natl Acad Sci U S A. 2008;105:16296–16301. doi: 10.1073/pnas.0808942105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ardalan M, Chinikar S, Mohajel Shoja M. Hemorrhagic Fever with renal syndrome and its history in Iran. Iran J Kidney Dis. 2014;8:438–442. [PubMed] [Google Scholar]
  5. Armien B, Pascale JM, Bayard V, Munoz C, Mosca I, Guerrero G, Armien A, Quiroz E, Castillo Z, Zaldivar Y, Gracia F, Hjelle B, Koster F. High seroprevalence of hantavirus infection on the Azuero peninsula of Panama. Am J Trop Med Hyg. 2004;70:682–687. [PubMed] [Google Scholar]
  6. Armien B, Pascale JM, Munoz C, Marinas J, Nunez H, Herrera M, Trujillo J, Sanchez D, Mendoza Y, Hjelle B, Koster F. Hantavirus fever without pulmonary syndrome in Panama. Am J Trop Med Hyg. 2013;89:489–494. doi: 10.4269/ajtmh.12-0334. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Atkinson B, Jameson LJ, Bovill BA, Aarons EJ, Clewlow J, Lumley S, Latham J, Jenkins MH, MacGowan AP, Simpson AJ, Ahmed J, Brooks TJ, Hewson R. A non-fatal case of hantavirus cardiopulmonary syndrome imported into the UK (ex Panama), July 2014. J Clin Virol. 2015;67:52–55. doi: 10.1016/j.jcv.2015.04.007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Avsic Zupanc T, Korva M, Markotic A. HFRS and hantaviruses in the Balkans/South-East Europe. Virus Res. 2014;187:27–33. doi: 10.1016/j.virusres.2013.12.042. [DOI] [PubMed] [Google Scholar]
  9. Blasdell K, Cosson JF, Chaval Y, Herbreteau V, Douangboupha B, Jittapalapong S, Lundqvist A, Hugot JP, Morand S, Buchy P. Rodent-borne hantaviruses in Cambodia, Lao PDR, and Thailand. Ecohealth. 2011;8:432–443. doi: 10.1007/s10393-011-0725-7. [DOI] [PubMed] [Google Scholar]
  10. Blasdell K, Morand S, Henttonen H, Tran A, Buchy P. Hantavirus seropositivity in rodents in relation to habitat heterogeneity in human-shaped landscapes of Southeast Asia. Spat Spatiotemporal Epidemiol. 2016;17:27–35. doi: 10.1016/j.sste.2016.04.002. [DOI] [PubMed] [Google Scholar]
  11. Botros BA, Sobh M, Wierzba T, Arthur RR, Mohareb EW, Frenck R, El Refaie A, Mahmoud I, Chapman GD, Graham RR. Prevalence of hantavirus antibody in patients with chronic renal disease in Egypt. Trans R Soc Trop Med Hyg. 2004;98:331–336. doi: 10.1016/S0035-9203(03)00063-4. [DOI] [PubMed] [Google Scholar]
  12. Brocato RL, Hammerbeck CD, Bell TM, Wells JB, Queen LA, Hooper JW. A lethal disease model for hantavirus pulmonary syndrome in immunosuppressed Syrian hamsters infected with Sin Nombre virus. J Virol. 2014;88:811–819. doi: 10.1128/JVI.02906-13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Chandy S, Boorugu H, Chrispal A, Thomas K, Abraham P, Sridharan G. Hantavirus infection: a case report from India. Indian J Med Microbiol. 2009;27:267–270. doi: 10.4103/0255-0857.53215. [DOI] [PubMed] [Google Scholar]
  14. Chandy S, Yoshimatsu K, Ulrich RG, Mertens M, Okumura M, Rajendran P, John GT, Balraj V, Muliyil J, Mammen J, Abraham P, Arikawa J, Sridharan G. Seroepidemiological study on hantavirus infections in India. Trans R Soc Trop Med Hyg. 2008;102:70–74. doi: 10.1016/j.trstmh.2007.09.016. [DOI] [PubMed] [Google Scholar]
  15. de Araujo J, Dure AI, Negrao R, Ometto T, Thomazelli LM, Durigon EL. Co-circulation in a single biome of the Juquitiba and Araraquara hantavirus detected in human sera in a sub-tropical region of Brazil. J Med Virol. 2015;87:725–732. doi: 10.1002/jmv.24118. [DOI] [PubMed] [Google Scholar]
  16. Demeester R, Bottieau E, Van Esbroeck M, Pourkarim MR, Maes P, Clement J. Hantavirus nephropathy as a pseudo-import pathology from Ecuador. Eur J Clin Microbiol Infect Dis. 2010;29:59–62. doi: 10.1007/s10096-009-0820-7. [DOI] [PubMed] [Google Scholar]
  17. Fang LQ, Goeijenbier M, Zuo SQ, Wang LP, Liang S, Klein SL, Li XL, Liu K, Liang L, Gong P, Glass GE, van Gorp E, Richardus JH, Ma JQ, Cao WC, de Vlas SJ. The association between hantavirus infection and selenium deficiency in mainland China. Viruses. 2015;7:333–351. doi: 10.3390/v7010333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Fang LZ, Zhao L, Wen HL, Zhang ZT, Liu JW, He ST, Xue ZF, Ma DQ, Zhang XS, Zhang Y, Yu XJ. Reservoir host expansion of hantavirus, China. Emerg Infect Dis. 2015;21:170–171. doi: 10.3201/eid2101.140960. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ferrer JF, Galligan D, Esteban E, Rey V, Murua A, Gutierrez S, Gonzalez L, Thakuri M, Feldman L, Poiesz B, Jonsson C. Hantavirus infection in people inhabiting a highly endemic region of the Gran Chaco territory, Paraguay: association with Trypanosoma cruzi infection, epidemiological features and haematological characteristics. Ann Trop Med Parasitol. 2003;97:269–280. doi: 10.1179/000349803235001903. [DOI] [PubMed] [Google Scholar]
  20. Figueiredo LT, Souza WM, Ferres M, Enria DA. Hantaviruses and cardiopulmonary syndrome in South America. Virus Res. 2014;187:43–54. doi: 10.1016/j.virusres.2014.01.015. [DOI] [PubMed] [Google Scholar]
  21. Firth C, Tokarz R, Simith DB, Nunes MR, Bhat M, Rosa ES, Medeiros DB, Palacios G, Vasconcelos PF, Lipkin WI. Diversity and distribution of hantaviruses in South America. J Virol. 2012;86:13756–13766. doi: 10.1128/JVI.02341-12. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Fontana-Binard L, Schultze D, Rojanavisut BS, Kruger DH, Dollenmaier G, Zanetti G, Meylan P. First case of nephropathia epidemica acquired in Switzerland. Rev Med Suisse. 2008;4:1572–1575. [PubMed] [Google Scholar]
  23. Gamage CD, Yasuda SP, Nishio S, Kularatne SA, Weerakoon K, Rajapakse J, Nwafor-Okoli C, Lee RB, Obayashi Y, Yoshimatsu K, Arikawa J, Tamashiro H. Serological evidence of Thailand virus-related hantavirus infection among suspected leptospirosis patients in Kandy, Sri Lanka. Jpn J Infect Dis. 2011;64:72–75. [PubMed] [Google Scholar]
  24. Ge XY, Yang WH, Pan H, Zhou JH, Han X, Zhu GJ, Desmond JS, Daszak P, Shi ZL, Zhang YZ. Fugong virus, a novel hantavirus harbored by the small oriental vole (Eothenomys eleusis) in China. Virol J. 2016;13:27. doi: 10.1186/s12985-016-0483-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. George J, Patnaik M, Bakshi E, Levy Y, Ben-David A, Ahmed A, Peter JB, Shoenfeld Y. Hantavirus seropositivity in Israeli patients with renal failure. Viral Immunol. 1998;11:103–108. doi: 10.1089/vim.1998.11.103. [DOI] [PubMed] [Google Scholar]
  26. Goeijenbier M, Aron G, Anfasa F, Lundkvist A, Verner-Carlsson J, Reusken CB, Martina BE, van Gorp EC, Resida L. Emerging Viruses in the Republic of Suriname: Retrospective and Prospective Study into Chikungunya Circulation and Suspicion of Human Hantavirus Infections, 2008–2012 and 2014. Vector Borne Zoonotic Dis. 2015;15:611–618. doi: 10.1089/vbz.2015.1798. [DOI] [PubMed] [Google Scholar]
  27. Groen J, Suharti C, Koraka P, van Gorp EC, Sutaryo J, Lundkvist A, Osterhaus AD. Serological evidence of human hantavirus infections in Indonesia. Infection. 2002;30:326–327. doi: 10.1007/s15010-002-2194-y. [DOI] [PubMed] [Google Scholar]
  28. Gu SH, Arai S, Yu HT, Lim BK, Kang HJ, Yanagihara R. Genetic variants of Cao Bang hantavirus in the Chinese mole shrew (Anourosorex squamipes) and Taiwanese mole shrew (Anourosorex yamashinai) Infect Genet Evol. 2016;40:113–118. doi: 10.1016/j.meegid.2016.01.031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Gubler DJ, Reiter P, Ebi KL, Yap W, Nasci R, Patz JA. Climate variability and change in the United States: potential impacts on vector-and rodent-borne diseases. Environ Health Perspect. 2001;109(2):223–233. doi: 10.1289/ehp.109-1240669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Guo G, Sheng J, Wu X, Wang Y, Guo L, Zhang X, Yao H. Seoul virus in the Brown Rat ( Rattus norvegicus ) from Urumqi, Xinjiang, Northwest of China. J Wildl Dis. 2016;52:705–708. doi: 10.7589/2015-08-210. [DOI] [PubMed] [Google Scholar]
  31. Guterres A, de Oliveira RC, Fernandes J, Schrago CG, de Lemos ER. Detection of different South American hantaviruses. Virus Res. 2015;210:106–113. doi: 10.1016/j.virusres.2015.07.022. [DOI] [PubMed] [Google Scholar]
  32. Hall PR, Leitao A, Ye C, Kilpatrick K, Hjelle B, Oprea TI, Larson RS. Small molecule inhibitors of hantavirus infection. Bioorg Med Chem Lett. 2010;20:7085–7091. doi: 10.1016/j.bmcl.2010.09.092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Hamidon BB, Saadiah S. Seoul hantavirus infection mimicking dengue fever. Med J Malaysia. 2003;58:786–787. [PubMed] [Google Scholar]
  34. Han SS, Kim S, Choi Y, Kim S, Kim YS. Air pollution and hemorrhagic fever with renal syndrome in South Korea: an ecological correlation study. BMC Public Health. 2013;13:347. doi: 10.1186/1471-2458-13-347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Heinemann P, Tia M, Alabi A, Anon JC, Auste B, Essbauer S, Gnionsahe A, Kigninlman H, Klempa B, Kraef C, Kruger N, Leendertz FH, Ndhatz-Sanogo M, Schaumburg F, Witkowski PT, Akoua-Koffi CG, Kruger DH. Human infections by non-rodent associated hantaviruses in Africa. J Infect Dis. 2016;214:1507–1511. doi: 10.1093/infdis/jiw401. [DOI] [PubMed] [Google Scholar]
  36. Heyman P, Ceianu CS, Christova I, Tordo N, Beersma M, Joao Alves M, Lundkvist A, Hukic M, Papa A, Tenorio A, Zelena H, Essbauer S, Visontai I, Golovljova I, Connell J, Nicoletti L, Van Esbroeck M, Gjeruldsen Dudman S, Aberle SW, Avsic-Zupanc T, Korukluoglu G, Nowakowska A, Klempa B, Ulrich RG, Bino S, Engler O, Opp M, Vaheri A. A five-year perspective on the situation of haemorrhagic fever with renal syndrome and status of the hantavirus reservoirs in Europe, 2005–2010. Euro Surveill. 2011;16:19961. doi: 10.2807/ese.16.36.19961-en. [DOI] [PubMed] [Google Scholar]
  37. Holsomback TS, Van Nice CJ, Clark RN, McIntyre NE, Abuzeineh AA, Salazar-Bravo J. Socio-ecology of the marsh rice rat (Oryzomys palustris) and the spatio-temporal distribution of Bayou virus in coastal Texas. Geospat Health. 2013;7:289–298. doi: 10.4081/gh.2013.87. [DOI] [PubMed] [Google Scholar]
  38. Hotez PJ, Woc-Colburn L, Bottazzi ME. Neglected tropical diseases in Central America and Panama: review of their prevalence, populations at risk and impact on regional development. Int J Parasitol. 2014;44:597–603. doi: 10.1016/j.ijpara.2014.04.001. [DOI] [PubMed] [Google Scholar]
  39. Huang LY, Zhou H, Yin WW, Wang Q, Sun H, Ding F, Man TF, Li Q, Feng ZJ. The current epidemic situation and surveillance regarding hemorrhagic fever with renal syndrome in China, 2010. Zhonghua Liu Xing Bing Xue Za Zhi. 2012;33:685–691. [PubMed] [Google Scholar]
  40. Huggins JW, Hsiang CM, Cosgriff TM, Guang MY, Smith JI, Wu ZO, LeDuc JW, Zheng ZM, Meegan JM, Wang QN, et al. Prospective, double-blind, concurrent, placebo-controlled clinical trial of intravenous ribavirin therapy of hemorrhagic fever with renal syndrome. J Infect Dis. 1991;164:1119–1127. doi: 10.1093/infdis/164.6.1119. [DOI] [PubMed] [Google Scholar]
  41. Huong VT, Yoshimatsu K, Luan VD, le Tuan V, Nhi L, Arikawa J, Nguyen TM. Hemorrhagic fever with renal syndrome, Vietnam. Emerg Infect Dis. 2010;16:363–365. doi: 10.3201/eid1602.091204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Ibrahim IN, Sudomo M, Morita C, Uemura S, Muramatsu Y, Ueno H, Kitamura T. Seroepidemiological survey of wild rats for Seoul virus in Indonesia. Jpn J Med Sci Biol. 1996;49:69–74. doi: 10.7883/yoken1952.49.69. [DOI] [PubMed] [Google Scholar]
  43. Jiang H, Du H, Wang LM, Wang PZ, Bai XF. Hemorrhagic Fever with Renal Syndrome: Pathogenesis and Clinical Picture. Front Cell Infect Microbiol. 2016;6:1. doi: 10.3389/fcimb.2016.00001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Jiang W, Wang PZ, Yu HT, Zhang Y, Zhao K, Du H, Bai XF. Development of a SYBR Green I based one-step real-time PCR assay for the detection of Hantaan virus. J Virol Methods. 2014;196:145–151. doi: 10.1016/j.jviromet.2013.11.004. [DOI] [PubMed] [Google Scholar]
  45. Johansson P, Yap G, Low HT, Siew CC, Kek R, Ng LC, Bucht G. Molecular characterization of two hantavirus strains from different rattus species in Singapore. Virol J. 2010;7:15. doi: 10.1186/1743-422X-7-15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Jonsson CB, Figueiredo LT, Vapalahti O. A global perspective on hantavirus ecology, epidemiology, and disease. Clin Microbiol Rev. 2010;23:412–441. doi: 10.1128/CMR.00062-09. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Kallio-Kokko H, Laakkonen J, Rizzoli A, Tagliapietra V, Cattadori I, Perkins SE, Hudson PJ, Cristofolini A, Versini W, Vapalahti O, Vaheri A, Henttonen H. Hantavirus and arenavirus antibody prevalence in rodents and humans in Trentino, Northern Italy. Epidemiol Infect. 2006;134:830–836. doi: 10.1017/S0950268805005431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Kang HJ, Kosoy MY, Shrestha SK, Shrestha MP, Pavlin JA, Gibbons RV, Yanagihara R. Short report: Genetic diversity of Thottapalayam virus, a Hantavirus harbored by the Asian house shrew (Suncus murinus) in Nepal. Am J Trop Med Hyg. 2011;85:540–545. doi: 10.4269/ajtmh.2011.11-0034. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Kariwa H, Yoshimatsu K, Arikawa J. Hantavirus infection in East Asia. Comp Immunol Microbiol Infect Dis. 2007;30:341–356. doi: 10.1016/j.cimid.2007.05.011. [DOI] [PubMed] [Google Scholar]
  50. Klempa B. Hantaviruses and climate change. Clin Microbiol Infect. 2009;15:518–523. doi: 10.1111/j.1469-0691.2009.02848.x. [DOI] [PubMed] [Google Scholar]
  51. Klempa B, Fichet-Calvet E, Lecompte E, Auste B, Aniskin V, Meisel H, Denys C, Koivogui L, ter Meulen J, Kruger DH. Hantavirus in African wood mouse, Guinea. Emerg Infect Dis. 2006;12:838–840. doi: 10.3201/eid1205.051487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Klempa B, Koivogui L, Sylla O, Koulemou K, Auste B, Kruger DH, ter Meulen J. Serological evidence of human hantavirus infections in Guinea, West Africa. J Infect Dis. 2010;201:1031–1034. doi: 10.1086/651169. [DOI] [PubMed] [Google Scholar]
  53. Klempa B, Meisel H, Rath S, Bartel J, Ulrich R, Kruger DH. Occurrence of renal and pulmonary syndrome in a region of northeast Germany where Tula hantavirus circulates. J Clin Microbiol. 2003;41:4894–4897. doi: 10.1128/JCM.41.10.4894-4897.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Klempa B, Tkachenko EA, Dzagurova TK, Yunicheva YV, Morozov VG, Okulova NM, Slyusareva GP, Smirnov A, Kruger DH. Hemorrhagic fever with renal syndrome caused by 2 lineages of Dobrava hantavirus, Russia. Emerg Infect Dis. 2008;14:617–625. doi: 10.3201/eid1404.071310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Klempa B, Witkowski PT, Popugaeva E, Auste B, Koivogui L, Fichet-Calvet E, Strecker T, Ter Meulen J, Kruger DH. Sangassou virus, the first hantavirus isolate from Africa, displays genetic and functional properties distinct from those of other murinae-associated hantaviruses. J Virol. 2012;86:3819–3827. doi: 10.1128/JVI.05879-11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Knust B, Rollin PE. Twenty-year summary of surveillance for human hantavirus infections, United States. Emerg Infect Dis. 2013;19:1934–1937. doi: 10.3201/eid1912.131217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Krautkramer E, Zeier M, Plyusnin A. Hantavirus infection: an emerging infectious disease causing acute renal failure. Kidney Int. 2013;83:23–27. doi: 10.1038/ki.2012.360. [DOI] [PubMed] [Google Scholar]
  58. Kruger DH, Schonrich G, Klempa B. Human pathogenic hantaviruses and prevention of infection. Hum Vaccin. 2011;7:685–693. doi: 10.4161/hv.7.6.15197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Kruger DH, Ulrich RG, Hofmann J. Hantaviruses as zoonotic pathogens in Germany. Dtsch Arztebl Int. 2013;110:461–467. doi: 10.3238/arztebl.2013.0461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Ksiazek TG, Peters CJ, Rollin PE, Zaki S, Nichol S, Spiropoulou C, Morzunov S, Feldmann H, Sanchez A, Khan AS, et al. Identification of a new North American hantavirus that causes acute pulmonary insufficiency. Am J Trop Med Hyg. 1995;52:117–123. doi: 10.4269/ajtmh.1995.52.117. [DOI] [PubMed] [Google Scholar]
  61. Lam SK, Chua KB, Myshrall T, Devi S, Zainal D, Afifi SA, Nerome K, Chu YK, Lee HW. Serological evidence of hantavirus infections in Malaysia. Southeast Asian J Trop Med Public Health. 2001;32:809–813. [PubMed] [Google Scholar]
  62. Latus J, Kitterer D, Segerer S, Artunc F, Alscher MD, Braun N. Severe thrombocytopenia in hantavirus-induced nephropathia epidemica. Infection. 2015;43:83–87. doi: 10.1007/s15010-014-0699-9. [DOI] [PubMed] [Google Scholar]
  63. Latus J, Schwab M, Tacconelli E, Pieper FM, Wegener D, Rettenmaier B, Schwab A, Hoffmann L, Dippon J, Muller S, Fritz P, Zakim D, Segerer S, Kitterer D, Kimmel M, Gussmann K, Priwitzer M, Mezger B, Walter-Frank B, Corea A, Wiedenmann A, Brockmann S, Pohlmann C, Alscher MD, Braun N. Acute kidney injury and tools for risk-stratification in 456 patients with hantavirus-induced nephropathia epidemica. Nephrol Dial Transplant. 2015;30:245–251. doi: 10.1093/ndt/gfu319. [DOI] [PubMed] [Google Scholar]
  64. Lee HW, Lee PW, Johnson KM. Isolation of the etiologic agent of Korean Hemorrhagic fever. J Infect Dis. 1978;137:298–308. doi: 10.1093/infdis/137.3.298. [DOI] [PubMed] [Google Scholar]
  65. Lee JG, Gu SH, Baek LJ, Shin OS, Park KS, Kim HC, Klein TA, Yanagihara R, Song JW. Muju virus, harbored by Myodes regulus in Korea, might represent a genetic variant of Puumala virus, the prototype arvicolid rodent-borne hantavirus. Viruses. 2014;6:1701–1714. doi: 10.3390/v6041701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Lee SH, Chung BH, Lee WC, Choi IS. Epidemiology of hemorrhagic fever with renal syndrome in Korea, 2001–2010. J Korean Med Sci. 2013;28:1552–1554. doi: 10.3346/jkms.2013.28.10.1552. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Lledo L, Gegundez MI, Martinez JC, Sanfeliu I. Epidemic nephropathy in Spain: first imported case. Med Clin (Barc) 2003;121:677. doi: 10.1016/s0025-7753(03)74058-5. [DOI] [PubMed] [Google Scholar]
  68. Lledo L, Klingstrom J, Gegundez MI, Plyusnina A, Vapalahti O, Saz JV, Beltran M, Sjolander KB, Vaheri A, Plyusnin A, Lundkvist A. Hantavirus infections in Spain: analysis of sera from the general population and from patients with pneumonia, renal disease and hepatitis. J Clin Virol. 2003;27:296–307. doi: 10.1016/s1386-6532(02)00228-7. [DOI] [PubMed] [Google Scholar]
  69. Lokugamage N, Kariwa H, Lokugamage K, Iwasa MA, Hagiya T, Yoshii K, Tachi A, Ando S, Fukushima H, Tsuchiya K, Iwasaki T, Araki K, Yoshimatsu K, Arikawa J, Mizutani T, Osawa K, Sato H, Takashima I. Epizootiological and epidemiological study of hantavirus infection in Japan. Microbiol Immunol. 2004;48:843–851. doi: 10.1111/j.1348-0421.2004.tb03616.x. [DOI] [PubMed] [Google Scholar]
  70. Mace G, Feyeux C, Mollard N, Chantegret C, Audia S, Rebibou JM, Spagnolo G, Bour JB, Denoyel GA, Sagot P, Reynes JM. Severe Seoul hantavirus infection in a pregnant woman, France, October 2012. Euro Surveill. 2013;18:20464. [PubMed] [Google Scholar]
  71. Maes P, Clement J, Gavrilovskaya I, Van Ranst M. Hantaviruses: immunology, treatment, and prevention. Viral Immunol. 2004;17:481–497. doi: 10.1089/vim.2004.17.481. [DOI] [PubMed] [Google Scholar]
  72. Maes P, Clement J, Van Ranst M. Recent approaches in hantavirus vaccine development. Expert Rev Vaccines. 2009;8:67–76. doi: 10.1586/14760584.8.1.67. [DOI] [PubMed] [Google Scholar]
  73. Manigold T, Vial P. Human hantavirus infections: epidemiology, clinical features, pathogenesis and immunology. Swiss Med Wkly. 2014;144:w13937. doi: 10.4414/smw.2014.13937. [DOI] [PubMed] [Google Scholar]
  74. Martinez-Valdebenito C, Calvo M, Vial C, Mansilla R, Marco C, Palma RE, Vial PA, Valdivieso F, Mertz G, Ferres M. Person-to-person household and nosocomial transmission of andes hantavirus, Southern Chile, 2011. Emerg Infect Dis. 2014;20:1629–1636. doi: 10.3201/eid2010.140353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. McElhinney L, Fooks AR, Featherstone C, Smith R, Morgan D. Hantavirus (Seoul virus) in pet rats: a zoonotic viral threat. Vet Rec. 2016;178:171–172. doi: 10.1136/vr.i817. [DOI] [PubMed] [Google Scholar]
  76. Mustonen J, Makela S, Outinen T, Laine O, Jylhava J, Arstila PT, Hurme M, Vaheri A. The pathogenesis of nephropathia epidemica: new knowledge and unanswered questions. Antiviral Res. 2013;100:589–604. doi: 10.1016/j.antiviral.2013.10.001. [DOI] [PubMed] [Google Scholar]
  77. Nelson R, Canate R, Pascale JM, Dragoo JW, Armien B, Armien AG, Koster F. Confirmation of Choclo virus as the cause of hantavirus cardiopulmonary syndrome and high serum antibody prevalence in Panama. J Med Virol. 2010;82:1586–1593. doi: 10.1002/jmv.21864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Newman EN, Johnstone P, Bridge H, Wright D, Jameson L, Bosworth A, Hatch R, Hayward-Karlsson J, Osborne J, Bailey MS, Green A, Ross D, Brooks T, Hewson R. Seroconversion for infectious pathogens among UK military personnel deployed to Afghanistan, 2008–2011. Emerg Infect Dis. 2014;20:2015–2022. doi: 10.3201/eid2012.131830. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Nikolic V, Stajkovic N, Stamenkovic G, Cekanac R, Marusic P, Siljic M, Gligic A, Stanojevic M. Evidence of recombination in Tula virus strains from Serbia. Infect Genet Evol. 2014;21:472–478. doi: 10.1016/j.meegid.2013.08.020. [DOI] [PubMed] [Google Scholar]
  80. Noh JY, Cheong HJ, Song JY, Kim WJ, Song KJ, Klein TA, Lee SH, Yanagihara R, Song JW. Clinical and molecular epidemiological features of hemorrhagic fever with renal syndrome in Korea over a 10-year period. J Clin Virol. 2013;58:11–17. doi: 10.1016/j.jcv.2013.06.027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Onishchenko GG, Ezhlova EB. Zh Mikrobiol Epidemiol Immunobiol. 2013. Epidemiologic surveillance and prophylaxis of hemorrhagic fever with renal syndrome in Russian Federation; pp. 23–32. [PubMed] [Google Scholar]
  82. Padula P, Della Valle MG, Alai MG, Cortada P, Villagra M, Gianella A. Andes virus and first case report of Bermejo virus causing fatal pulmonary syndrome. Emerg Infect Dis. 2002;8:437–439. doi: 10.3201/eid0804.010300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Papa A. Dobrava-Belgrade virus: phylogeny, epidemiology, disease. Antiviral Res. 2012;95:104–117. doi: 10.1016/j.antiviral.2012.05.011. [DOI] [PubMed] [Google Scholar]
  84. Papa A, Vaheri A, LeDuc JW, Kruger DH, Avsic-Zupanc T, Arikawa J, Song JW, Markotic A, Clement J, Liang M, Li D, Yashina LN, Jonsson CB, Schmaljohn CS. Meeting report: Tenth International Conference on Hantaviruses. Antiviral Res. 2016;133:234–241. doi: 10.1016/j.antiviral.2016.08.015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Pattamadilok S, Lee BH, Kumperasart S, Yoshimatsu K, Okumura M, Nakamura I, Araki K, Khoprasert Y, Dangsupa P, Panlar P, Jandrig B, Kruger DH, Klempa B, Jakel T, Schmidt J, Ulrich R, Kariwa H, Arikawa J. Geographical distribution of hantaviruses in Thailand and potential human health significance of Thailand virus. Am J Trop Med Hyg. 2006;75:994–1002. [PubMed] [Google Scholar]
  86. Peters CJ, Khan AS. Hantavirus pulmonary syndrome: the new American hemorrhagic fever. Clin Infect Dis. 2002;34:1224–1231. doi: 10.1086/339864. [DOI] [PubMed] [Google Scholar]
  87. Pettersson L, Boman J, Juto P, Evander M, Ahlm C. Outbreak of Puumala virus infection, Sweden. Emerg Infect Dis. 2008;14:808–810. doi: 10.3201/eid1405.071124. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Plyusnina A, Ferenczi E, Racz GR, Nemirov K, Lundkvist A, Vaheri A, Vapalahti O, Plyusnin A. Co-circulation of three pathogenic hantaviruses: Puumala, Dobrava, and Saaremaa in Hungary. J Med Virol. 2009;81:2045–2052. doi: 10.1002/jmv.21635. [DOI] [PubMed] [Google Scholar]
  89. Plyusnina A, Ibrahim IN, Plyusnin A. A newly recognized hantavirus in the Asian house rat (Rattus tanezumi) in Indonesia. J Gen Virol. 2009;90:205–209. doi: 10.1099/vir.0.006155-0. [DOI] [PubMed] [Google Scholar]
  90. Rawlings JA, Torrez-Martinez N, Neill SU, Moore GM, Hicks BN, Pichuantes S, Nguyen A, Bharadwaj M, Hjelle B. Cocirculation of multiple hantaviruses in Texas, with characterization of the small (S) genome of a previously undescribed virus of cotton rats (Sigmodon hispidus) Am J Trop Med Hyg. 1996;55:672–679. doi: 10.4269/ajtmh.1996.55.672. [DOI] [PubMed] [Google Scholar]
  91. Rhodes LV, 3rd, Huang C, Sanchez AJ, Nichol ST, Zaki SR, Ksiazek TG, Humphreys JG, Freeman JJ, Knecht KR. Hantavirus pulmonary syndrome associated with Monongahela virus, Pennsylvania. Emerg Infect Dis. 2000;6:616–621. doi: 10.3201/eid0606.000610. [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. Rollin PE, Nawrocka E, Rodhain F, Sureau P, McCormick JB. Serological data on hemorrhagic fever with renal syndrome in Southeast Asia. Bull Soc Pathol Exot Filiales. 1986;79:473–475. [PubMed] [Google Scholar]
  93. Rovida F, Percivalle E, Sarasini A, Chichino G, Baldanti F. Imported hantavirus cardiopulmonary syndrome in an Italian traveller returning from Cuba. New Microbiol. 2013;36:103–105. [PubMed] [Google Scholar]
  94. Sandmann S, Meisel H, Razanskiene A, Wolbert A, Pohl B, Kruger DH, Sasnauskas K, Ulrich R. Detection of human hantavirus infections in Lithuania. Infection. 2005;33:66–72. doi: 10.1007/s15010-005-4058-8. [DOI] [PubMed] [Google Scholar]
  95. Schmaljohn C, Hjelle B. Hantaviruses: a global disease problem. Emerg Infect Dis. 1997;3:95–104. doi: 10.3201/eid0302.970202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Song G. Epidemiological progresses of hemorrhagic fever with renal syndrome in China. Chin Med J (Engl) 1999;112:472–477. [PubMed] [Google Scholar]
  97. Spengler JR, Haddock E, Gardner D, Hjelle B, Feldmann H, Prescott J. Experimental Andes virus infection in deer mice: characteristics of infection and clearance in a heterologous rodent host. PLoS One. 2013;8:e55310. doi: 10.1371/journal.pone.0055310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  98. Spiropoulou CF, Albarino CG, Ksiazek TG, Rollin PE. Andes and Prospect Hill hantaviruses differ in early induction of interferon although both can downregulate interferon signaling. J Virol. 2007;81:2769–2776. doi: 10.1128/JVI.02402-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. Suharti C, van Gorp EC, Dolmans WM, Groen J, Hadisaputro S, Djokomoeljanto RJ, D MEO, van der Meer JW. Hanta virus infection during dengue virus infection outbreak in Indonesia. Acta Med Indones. 2009;41:75–80. [PubMed] [Google Scholar]
  100. Sunil-Chandra NP, Clement J, Maes P, DES HJ, VANE M, VANR M. Concomitant leptospirosis-hantavirus co-infection in acute patients hospitalized in Sri Lanka: implications for a potentially worldwide underestimated problem -ERRATUM. Epidemiol Infect. 2015;143:2094. doi: 10.1017/S0950268815000412. [DOI] [PMC free article] [PubMed] [Google Scholar]
  101. Suputthamongkol Y, Nitatpattana N, Chayakulkeeree M, Palabodeewat S, Yoksan S, Gonzalez JP. Hantavirus infection in Thailand: first clinical case report. Southeast Asian J Trop Med Public Health. 2005;36:700–703. [PubMed] [Google Scholar]
  102. Tervo L, Makela S, Syrjanen J, Huttunen R, Rimpela A, Huhtala H, Vapalahti O, Vaheri A, Mustonen J. Smoking is associated with aggravated kidney injury in Puumala hantavirus-induced haemorrhagic fever with renal syndrome. Nephrol Dial Transplant. 2015;30:1693–1698. doi: 10.1093/ndt/gfv273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  103. Torres-Perez F, Boric-Bargetto D, Palma Vasquez RE. Hantavirus in Chile: New rodents with potential epidemiological importance. Rev Med Chil. 2016;144:818. doi: 10.4067/S0034-98872016000600020. [DOI] [PubMed] [Google Scholar]
  104. Truong TT, Yoshimatsu K, Araki K, Lee BH, Nakamura I, Endo R, Shimizu K, Yasuda SP, Koma T, Taruishi M, Okumura M, Truong UN, Arikawa J. Molecular epidemiological and serological studies of hantavirus infection in northern Vietnam. J Vet Med Sci. 2009;71:1357–1363. doi: 10.1292/jvms.001357. [DOI] [PubMed] [Google Scholar]
  105. Vaheri A, Strandin T, Hepojoki J, Sironen T, Henttonen H, Makela S, Mustonen J. Uncovering the mysteries of hantavirus infections. Nat Rev Microbiol. 2013;11:539–550. doi: 10.1038/nrmicro3066. [DOI] [PubMed] [Google Scholar]
  106. Van Cuong N, Carrique-Mas J, Vo Be H, An NN, Tue NT, Anh NL, Anh PH, Phuc NT, Baker S, Voutilainen L, Jaaskelainen A, Huhtamo E, Utriainen M, Sironen T, Vaheri A, Henttonen H, Vapalahti O, Chaval Y, Morand S, Bryant JE. Rodents and risk in the Mekong Delta of Vietnam: seroprevalence of selected zoonotic viruses in rodents and humans. Vector Borne Zoonotic Dis. 2015;15:65–72. doi: 10.1089/vbz.2014.1603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  107. Vitarana T, Colombage G, Bandaranayake V, Lee HW. Hantavirus disease in Sri Lanka. Lancet. 1988;2:1263. [PubMed] [Google Scholar]
  108. Vollmar P, Lubnow M, Simon M, Muller T, Bergler T, Alois P, Thoma BR, Essbauer S. Hantavirus cardiopulmonary syndrome due to Puumala virus in Germany. J Clin Virol. 2016;84:42–47. doi: 10.1016/j.jcv.2016.10.004. [DOI] [PubMed] [Google Scholar]
  109. Wang J, Guo W, Du H, Yu H, Jiang W, Zhu T, Bai X, Wang P. Elevated soluble CD163 plasma levels are associated with disease severity in patients with hemorrhagic fever with renal syndrome. PLoS One. 2014;9:e112127. doi: 10.1371/journal.pone.0112127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  110. Wang W, Zhang Y, Li Y, Pan L, Bai L, Zhuang Y, Huang CX, Wang JP, Yu HT, Wei X, Jiang W, Nan YY, Yang DQ, Su WJ, Wang PZ, Bai XF. Dysregulation of the beta3 integrin-VEGFR2 complex in Hantaan virus-directed hyperpermeability upon treatment with VEGF. Arch Virol. 2012;157:1051–1061. doi: 10.1007/s00705-012-1245-7. [DOI] [PubMed] [Google Scholar]
  111. Weiss S, Witkowski PT, Auste B, Nowak K, Weber N, Fahr J, Mombouli JV, Wolfe ND, Drexler JF, Drosten C, Klempa B, Leendertz FH, Kruger DH. Hantavirus in bat, Sierra Leone. Emerg Infect Dis. 2012;18:159–161. doi: 10.3201/eid1801.111026. [DOI] [PMC free article] [PubMed] [Google Scholar]
  112. Witkowski PT, Klempa B, Ithete NL, Auste B, Mfune JK, Hoveka J, Matthee S, Preiser W, Kruger DH. Hantaviruses in Africa. Virus Res. 2014;187:34–42. doi: 10.1016/j.virusres.2013.12.039. [DOI] [PubMed] [Google Scholar]
  113. Witkowski PT, Leendertz SA, Auste B, Akoua-Koffi C, Schubert G, Klempa B, Muyembe-Tamfum JJ, Karhemere S, Leendertz FH, Kruger DH. Human seroprevalence indicating hantavirus infections in tropical rainforests of Cote d'Ivoire and Democratic Republic of Congo. Front Microbiol. 2015;6:518. doi: 10.3389/fmicb.2015.00518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  114. Wong TW, Chan YC, Lee HW. Haemorrhagic fever with renal syndrome in Singapore: a case report. Southeast Asian J Trop Med Public Health. 1985;16:525–527. [PubMed] [Google Scholar]
  115. Yao L, Kang Z, Liu Y, Song F, Zhang X, Cao X, Zhang Y, Yang Y, Sun X, Wang J, Hu K, Liu L, Chen W, Shao L, Xu B, Wang B. Seoul virus in rats (Rattus norvegicus), Hyesan, North Korea, 2009–2011. Emerg Infect Dis. 2013;19:1895–1896. doi: 10.3201/eid1911.130207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  116. Yao LS, Qin CF, Pu Y, Zhang XL, Liu YX, Liu Y, Cao XM, Deng YQ, Wang J, Hu KX, Xu BL. Complete genome sequence of Seoul virus isolated from Rattus norvegicus in the Democratic People's Republic of Korea. J Virol. 2012;86:13853. doi: 10.1128/JVI.02668-12. [DOI] [PMC free article] [PubMed] [Google Scholar]
  117. Yu H, Jiang W, Du H, Xing Y, Bai G, Zhang Y, Li Y, Jiang H, Zhang Y, Wang J, Wang P, Bai X. Involvement of the Akt/NF-kappaB pathways in the HTNV-mediated increase of IL-6, CCL5, ICAM-1, and VCAM-1 in HUVECs. PLoS One. 2014;9:e93810. doi: 10.1371/journal.pone.0093810. [DOI] [PMC free article] [PubMed] [Google Scholar]
  118. Yu HT, Jiang H, Zhang Y, Nan XP, Li Y, Wang W, Jiang W, Yang DQ, Su WJ, Wang JP, Wang PZ, Bai XF. Hantaan virus triggers TLR4-dependent innate immune responses. Viral Immunol. 2012;25:387–393. doi: 10.1089/vim.2012.0005. [DOI] [PubMed] [Google Scholar]
  119. Yu XJ, Tesh RB. The role of mites in the transmission and maintenance of Hantaan virus (Hantavirus: Bunyaviridae) J Infect Dis. 2014;210:1693–1699. doi: 10.1093/infdis/jiu336. [DOI] [PMC free article] [PubMed] [Google Scholar]
  120. Zelena H, Mrazek J, Kuhn T. Tula hantavirus infection in immunocompromised host, Czech Republic. Emerg Infect Dis. 2013;19:1873–1875. doi: 10.3201/eid1911.130421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  121. Zhang S, Wang S, Yin W, Liang M, Li J, Zhang Q, Feng Z, Li D. Epidemic characteristics of hemorrhagic fever with renal syndrome in China, 2006–2012. BMC Infect Dis. 2014;14:384. doi: 10.1186/1471-2334-14-384. [DOI] [PMC free article] [PubMed] [Google Scholar]
  122. Zhang WY, Wang LY, Liu YX, Yin WW, Hu WB, Magalhaes RJ, Ding F, Sun HL, Zhou H, Li SL, Haque U, Tong SL, Glass GE, Bi P, Clements AC, Liu QY, Li CY. Spatiotemporal transmission dynamics of hemorrhagic fever with renal syndrome in China, 2005–2012. PLoS Negl Trop Dis. 2014;8:e3344. doi: 10.1371/journal.pntd.0003344. [DOI] [PMC free article] [PubMed] [Google Scholar]
  123. Zhang Y, Liu BH, Lin F, Zhang YG, Si BY, Kang XP, Hu Y, Li J, Wu XY, Li YC, Zhu QY, Yang YH. The first complete genomic characterization of an Amur virus isolate from China. Arch Virol. 2013;158:2185–2188. doi: 10.1007/s00705-013-1633-7. [DOI] [PubMed] [Google Scholar]
  124. Zhang YZ. Discovery of hantaviruses in bats and insectivores and the evolution of the genus Hantavirus. Virus Res. 2014;187:15–21. doi: 10.1016/j.virusres.2013.12.035. [DOI] [PubMed] [Google Scholar]
  125. Zou LX, Chen MJ, Sun L. Haemorrhagic fever with renal syndrome: literature review and distribution analysis in China. Int J Infect Dis. 2016;43:95–100. doi: 10.1016/j.ijid.2016.01.003. [DOI] [PubMed] [Google Scholar]
  126. Zuo SQ, Fang LQ, Zhan L, Zhang PH, Jiang JF, Wang LP, Ma JQ, Wang BC, Wang RM, Wu XM, Yang H, Cao ZW, Cao WC. Geo-spatial hotspots of hemorrhagic fever with renal syndrome and genetic characterization of Seoul variants in Beijing, China. PLoS Negl Trop Dis. 2011;5:e945. doi: 10.1371/journal.pntd.0000945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  127. Zuo SQ, Gong ZD, Fang LQ, Jiang JF, Zhang JS, Zhao QM, Cao WC. A new hantavirus from the stripe-backed shrew (Sorex cylindricauda) in the People's Republic of China. Virus Res. 2014;184:82–86. doi: 10.1016/j.virusres.2014.02.004. [DOI] [PubMed] [Google Scholar]

Articles from Virologica Sinica are provided here courtesy of Wuhan Institute of Virology, Chinese Academy of Sciences

RESOURCES