Isolation and Characterization of Hantaviruses in Far East Russia and Etiology of Hemorrhagic Fever with Renal Syndrome in the Region

Hiroaki Kariwa Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Japan; Plague Control Station of Khabarovsk, Khabarovsk, Russia; Research Institute of Epidemiology and Microbiology, Siberian Branch of Russian Academy of Medical Sciences, Vladivostok, Russia; Far Eastern State Medical University, Khabarovsk, Russia; Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan; Graduate School of Medicine, Hokkaido University, Sapporo, Japan

Search for other papers by Hiroaki Kariwa in
Current site
Google Scholar
PubMed
Close
,
Keisuke Yoshikawa Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Japan; Plague Control Station of Khabarovsk, Khabarovsk, Russia; Research Institute of Epidemiology and Microbiology, Siberian Branch of Russian Academy of Medical Sciences, Vladivostok, Russia; Far Eastern State Medical University, Khabarovsk, Russia; Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan; Graduate School of Medicine, Hokkaido University, Sapporo, Japan

Search for other papers by Keisuke Yoshikawa in
Current site
Google Scholar
PubMed
Close
,
Yoichi Tanikawa Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Japan; Plague Control Station of Khabarovsk, Khabarovsk, Russia; Research Institute of Epidemiology and Microbiology, Siberian Branch of Russian Academy of Medical Sciences, Vladivostok, Russia; Far Eastern State Medical University, Khabarovsk, Russia; Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan; Graduate School of Medicine, Hokkaido University, Sapporo, Japan

Search for other papers by Yoichi Tanikawa in
Current site
Google Scholar
PubMed
Close
,
Takahiro Seto Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Japan; Plague Control Station of Khabarovsk, Khabarovsk, Russia; Research Institute of Epidemiology and Microbiology, Siberian Branch of Russian Academy of Medical Sciences, Vladivostok, Russia; Far Eastern State Medical University, Khabarovsk, Russia; Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan; Graduate School of Medicine, Hokkaido University, Sapporo, Japan

Search for other papers by Takahiro Seto in
Current site
Google Scholar
PubMed
Close
,
Takahiro Sanada Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Japan; Plague Control Station of Khabarovsk, Khabarovsk, Russia; Research Institute of Epidemiology and Microbiology, Siberian Branch of Russian Academy of Medical Sciences, Vladivostok, Russia; Far Eastern State Medical University, Khabarovsk, Russia; Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan; Graduate School of Medicine, Hokkaido University, Sapporo, Japan

Search for other papers by Takahiro Sanada in
Current site
Google Scholar
PubMed
Close
,
Ngonda Saasa Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Japan; Plague Control Station of Khabarovsk, Khabarovsk, Russia; Research Institute of Epidemiology and Microbiology, Siberian Branch of Russian Academy of Medical Sciences, Vladivostok, Russia; Far Eastern State Medical University, Khabarovsk, Russia; Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan; Graduate School of Medicine, Hokkaido University, Sapporo, Japan

Search for other papers by Ngonda Saasa in
Current site
Google Scholar
PubMed
Close
,
Leonid I. Ivanov Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Japan; Plague Control Station of Khabarovsk, Khabarovsk, Russia; Research Institute of Epidemiology and Microbiology, Siberian Branch of Russian Academy of Medical Sciences, Vladivostok, Russia; Far Eastern State Medical University, Khabarovsk, Russia; Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan; Graduate School of Medicine, Hokkaido University, Sapporo, Japan

Search for other papers by Leonid I. Ivanov in
Current site
Google Scholar
PubMed
Close
,
Raisa Slonova Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Japan; Plague Control Station of Khabarovsk, Khabarovsk, Russia; Research Institute of Epidemiology and Microbiology, Siberian Branch of Russian Academy of Medical Sciences, Vladivostok, Russia; Far Eastern State Medical University, Khabarovsk, Russia; Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan; Graduate School of Medicine, Hokkaido University, Sapporo, Japan

Search for other papers by Raisa Slonova in
Current site
Google Scholar
PubMed
Close
,
Tatyana A. Zakharycheva Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Japan; Plague Control Station of Khabarovsk, Khabarovsk, Russia; Research Institute of Epidemiology and Microbiology, Siberian Branch of Russian Academy of Medical Sciences, Vladivostok, Russia; Far Eastern State Medical University, Khabarovsk, Russia; Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan; Graduate School of Medicine, Hokkaido University, Sapporo, Japan

Search for other papers by Tatyana A. Zakharycheva in
Current site
Google Scholar
PubMed
Close
,
Ichiro Nakamura Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Japan; Plague Control Station of Khabarovsk, Khabarovsk, Russia; Research Institute of Epidemiology and Microbiology, Siberian Branch of Russian Academy of Medical Sciences, Vladivostok, Russia; Far Eastern State Medical University, Khabarovsk, Russia; Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan; Graduate School of Medicine, Hokkaido University, Sapporo, Japan

Search for other papers by Ichiro Nakamura in
Current site
Google Scholar
PubMed
Close
,
Kumiko Yoshimatsu Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Japan; Plague Control Station of Khabarovsk, Khabarovsk, Russia; Research Institute of Epidemiology and Microbiology, Siberian Branch of Russian Academy of Medical Sciences, Vladivostok, Russia; Far Eastern State Medical University, Khabarovsk, Russia; Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan; Graduate School of Medicine, Hokkaido University, Sapporo, Japan

Search for other papers by Kumiko Yoshimatsu in
Current site
Google Scholar
PubMed
Close
,
Jiro Arikawa Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Japan; Plague Control Station of Khabarovsk, Khabarovsk, Russia; Research Institute of Epidemiology and Microbiology, Siberian Branch of Russian Academy of Medical Sciences, Vladivostok, Russia; Far Eastern State Medical University, Khabarovsk, Russia; Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan; Graduate School of Medicine, Hokkaido University, Sapporo, Japan

Search for other papers by Jiro Arikawa in
Current site
Google Scholar
PubMed
Close
,
Kentaro Yoshii Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Japan; Plague Control Station of Khabarovsk, Khabarovsk, Russia; Research Institute of Epidemiology and Microbiology, Siberian Branch of Russian Academy of Medical Sciences, Vladivostok, Russia; Far Eastern State Medical University, Khabarovsk, Russia; Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan; Graduate School of Medicine, Hokkaido University, Sapporo, Japan

Search for other papers by Kentaro Yoshii in
Current site
Google Scholar
PubMed
Close
, and
Ikuo Takashima Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Japan; Plague Control Station of Khabarovsk, Khabarovsk, Russia; Research Institute of Epidemiology and Microbiology, Siberian Branch of Russian Academy of Medical Sciences, Vladivostok, Russia; Far Eastern State Medical University, Khabarovsk, Russia; Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan; Graduate School of Medicine, Hokkaido University, Sapporo, Japan

Search for other papers by Ikuo Takashima in
Current site
Google Scholar
PubMed
Close
Restricted access

Hemorrhagic fever with renal syndrome (HFRS) is a serious public health issue in Far East Russia. Two different hantaviruses were isolated from rodents captured in the Khabarovsk region: Amur virus (AMRV; Khekhtsir/AP209/2005 strain from Apodemus peninsulae) and Hantaan virus (HTNV; Galkino/AA57/2002 strain from A. agrarius). Genetic analysis of the new isolates revealed that the M and L segments were apparently different between AMRV and HTNV, but S segments of the two viruses were closer. The antigenicities of AMRV, HTNV, and Seoul virus (SEOV) were differentiated by cross-neutralization. Serological differential diagnoses of 67 HFRS patients in the Prymorsky and Khabarovsk regions of Far East Russia were conducted using a neutralization test. The results revealed that the major cause of HFRS varied with location in Far East Russia: SEOV for Vladivostok city in the Prymorsky region, AMRV in rural areas of the Primorsky region, and probably HTNV for the Khabarovsk region.

Author Notes

*Address correspondence to Hiroaki Kariwa, Graduate School of Veterinary Medicine, Hokkaido University, Kita-Ku, Kita-18, Nishi-9, Sapporo, Hokkaido, Japan, 060-0818. E-mail: kariwa@vetmed.hokudai.ac.jp

Financial support: This study was supported financially by grants-in-aid for scientific research (B) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan, a scientific grant for Research on Emerging and Re-emerging Infectious Diseases from the Ministry of Health, Welfare, and Labour of Japan, and a grant from the Program of Global Center of Excellence Program, Hokkaido University (“Establishment of International Collaboration Centers for Zoonosis Control”).

Authors’ addresses: Hiroaki Kariwa, Keisuke Yoshikawa, Yoichi Tanikawa, Takahiro Seto, Takahiro Sanada, Ngonda Saasa, Kentaro Yoshii, and Ikuo Takashima, Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Japan, E-mails: kariwa@vetmed.hokudai.ac.jp, canis-familiaris-l@k.vodafone.ne.jp, tanikawa.yf@om.asahi-kasei.co.jp, setotaka@vetmed.hokudai.ac.jp, sanada-t@vetmed.hokudai.ac.jp, nsaasa@yahoo.co.uk, kyoshii@vetmed.hokudai.ac.jp, and takasima@vetmed.hokudai.ac.jp. Leonid I. Ivanov, Plague Control Station of Khabarovsk, Khabarovsk, Russia, E-mail: chum@chum.khv.ru. Raisa Slonova, Research Institute of Epidemiology and Microbiology, Siberian Branch of Russian Academy of Medical Sciences, Vladivostok, Russia, E-mail: atavalk@inbox.ru. Tatyana A. Zakharycheva, Far Eastern State Medical University, Khabarovsk, Russia, E-mail: dolika@inbox.ru. Ichiro Nakamura, Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan, E-mail: inaka@czc.hokudai.ac.jp. Kumiko Yoshimatsu and Jiro Arikawa, Graduate School of Medicine, Hokkaido University, Sapporo, Japan, E-mails: yosimatu@med.hokudai.ac.jp and j_arika@med.hokudai.ac.jp.

  • 1.

    Krüger DH, Ulrich R, Lundkvist A, 2001. Hantavirus infections and their prevention. Microbes Infect 3: 11291144.

  • 2.

    Schmaljohn CS, Hjelle B, 1997. Hantaviruses: a global disease problem. Emerg Infect Dis 3: 95104.

  • 3.

    Jonsson CB, Schmaljohn CS, 2001. Replication of hantavirus. Schmaojohn CS, Nichol ST, eds. Hantavirus. Berlin, Germany: Springer-Verlag, 1532.

  • 4.

    Jonsson CB, Figueiredo LTM, Vapalahti O, 2010. A global perspective on hantavirus ecology, epidemiology, and disease. Clin Microbiol Rev 23: 412441.

  • 5.

    Elliot RM, Beaty BJ, Calisher CH, Goldbach RW, Nichol ST, Plyusnin A, Schmaljohn CS, 2005. Family Bunyaviridae. Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA, eds. Virus Taxonomy. London, United Kingdom: Elsevier Academic Press, 695715.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Zhang YZ, Zou Y, Fu ZF, Plyusnin A, 2010. Hantavirus infections in humans and animals, China. Emerg Infect Dis 16: 11951203.

  • 7.

    Song JY, Chun BC, Kim SD, Baek LJ, Kim SH, Sohn JW, Cheong HJ, Kim WJ, Park SC, Kim MJ, 2006. Epidemiology of hemorrhagic fever with renal syndrome in endemic area of the Republic of Korea, 1995–1998. J Korean Med Sci 21: 614620.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Kariwa H, Lokugamage K, Lokugamage N, Miyamoto H, Yoshii K, Nakauchi M, Yoshimatsu K, Arikawa J, Ivanov LI, Iwasaki T, Takashima I, 2007. A comparative epidemiological study of hantavirus infection in Japan and far east Russia. Jpn J Vet Res 54: 145161.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Kariwa H, Zhong CB, Araki K, Yoshimatsu K, Lokugamage K, Lokugamage N, Murphy ME, Mizutani T, Arikawa J, Fukushima H, Xiong H, Jiehua C, Takashima I, 2001. Epizootiological survey of hantavirus among rodent species in Ningxia Hui Autonomous Province, China. Jpn J Vet Res 49: 105114.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Song G, Hang CS, Liao HX, Fu JL, Gao GZ, Qiu HL, Zhang QF, 1984. Antigenic difference between viral strains causing classical and mild types of epidemic hemorrhagic fever with renal syndrome in China. J Infect Dis 150: 889894.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Lokugamage K, Kariwa H, Hayasaka D, Cui BZ, Iwasaki T, Lokugamage N, Ivanov LI, Volkov VI, Demenev VA, Slonova R, Kompanets G, Kushnaryova T, Kurata T, Maeda K, Araki K, Mizutani T, Yoshimatsu K, Arikawa J, Takashima I, 2002. Genetic characterization of hantaviruses transmitted by the Korean field mouse (Apodemus peninsulae), far east Russia. Emerg Infect Dis 8: 768776.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Miyamoto H, Kariwa H, Araki K, Lokugamage K, Hayasaka D, Cui BZ, Lokugamage N, Ivanov LI, Mizutani T, Iwasa MA, Yoshimatsu K, Arikawa J, Takashima I, 2003. Serological analysis of hemorrhagic fever with renal syndrome (HFRS) patients in far eastern Russia and identification of the causative hantavirus genotype. Arch Virol 148: 15431556.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Yashina LN, Patrushev NA, Ivanov LI, Slonova RA, Mishin VP, Kompanez GG, Zdanovskaya NI, Kuzina II, Safronov PF, Chizhikov VE, Schmaljohn C, Netesov SV, 2000. Genetic diversity of hantaviruses associated with hemorrhagic fever with renal syndrome in the far east of Russia. Virus Res 70: 3144.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Yashina L, Mishin V, Zdanovskaya N, Schmaljohn C, Ivanov L, 2001. A newly discovered variant of a hantavirus in Apodemus peninsulae, far eastern Russia. Emerg Infect Dis 7: 912913.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Lokugamage K, Kariwa H, Lokugamage N, Iwasa M, Hagiya T, Araki K, Tachi A, Mizutani T, Yoshimatsu K, Arikawa J, Iwasaki T, Takashima I, 2004. Comparison of virulence of various hantaviruses related to hemorrhagic fever with renal syndrome in newborn mouse model. Jpn J Vet Res 51: 143149.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Baek LJ, Kariwa H, Lokugamage K, Yoshimatsu K, Arikawa J, Takashima I, Kang JI, Moon SS, Chung SY, Kim EJ, Kang HJ, Song KJ, Klein TA, Yanagihara R, Song JW, 2006. Soochong virus: an antigenically and genetically distinct hantavirus isolated from Apodemus peninsulae in Korea. J Med Virol 78: 290297.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Garanina SB, Platonov AE, Zhuravlev VI, Murashkina AN, Yakimenko VV, Korneev AG, Shipulin GA, 2009. Genetic diversity and geographic distribution of hantaviruses in Russia. Zoonoses Public Health 56: 297309.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Ivanov LI, Liberova RN, Zdanovskaya NI, Denisov EA, Prosina NA, 1996. Contingents of people for specific prevention of hemorrhagic fever with renal syndrome in the Khabarovsk Territory and Jewish Autonomous Region of Russia. Far East Med J 4 (Suppl Vaccination): 4448.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Kompanets GG, Slonova RA, Kushnareva TV, Maksema IG, Pysina TV, Kraeva LS, 2006. Humoral immune response to hantaviruses in health people of the Maritime Territory of Russia. Zh Microbiol (Moscow) 3: (Suppl): 8487.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Lee HW, Lee PW, Johnson KM, 1978. Isolation of the etiologic agent of Korean Hemorrhagic fever. J Infect Dis 137: 298308.

  • 21.

    Wang H, Yoshimatsu K, Ebihara H, Ogino M, Araki K, Kariwa H, Wang Z, Luo Z, Li D, Hang C, Arikawa J, 2000. Genetic diversity of hantaviruses isolated in china and characterization of novel hantaviruses isolated from Niviventer confucianus and Rattus rattus. Virology 278: 332345.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Liang M, Li D, Xiao SY, Hang C, Rossi CA, Schmaljohn CS, 1994. Antigenic and molecular characterization of hantavirus isolates from China. Virus Res 31: 219233.

  • 23.

    Kitamura T, Morita C, Komatsu T, Sugiyama K, Arikawa J, Shiga S, Takeda H, Akao Y, Imaizumi K, Oya A, Hashimoto N, Urasawa S, 1983. Isolation of virus causing hemorrhagic fever with renal syndrome (HFRS) through a cell culture system. Jpn J Med Sci Biol 36: 1725.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Yoshimatsu K, Arikawa J, Tamura M, Yoshida R, Lundkvist A, Niklasson B, Kariwa H, Azuma I, 1996. Characterization of the nucleocapsid protein of Hantaan virus strain 76-118 using monoclonal antibodies. J Gen Virol 77: 695704.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Kariwa H, Arikawa J, Takashima I, Isegawa Y, Yamanishi K, Hashimoto N, 1994. Enhancement of infectivity of hantavirus in cell culture by centrifugation. J Virol Methods 49: 235244.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Nylander JAA, 2004. MrModeltest v2. Available at: http://www.abc.se/~nylander/mrmodeltest2/mrmodeltest2.html. Accessed May 22, 2008.

  • 27.

    Huelsenbeck JP, Ronquist F, 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754755.

  • 28.

    Lokugamage K, Kariwa H, Lokugamage N, Miyamoto H, Iwasa M, Hagiya T, Araki K, Tachi A, Mizutani T, Yoshimatsu K, Arikawa J, Takashima I, 2004. Genetic and antigenic characterization of the Amur virus associated with hemorrhagic fever with renal syndrome. Virus Res 101: 127134.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Shelby JH, 1973. The analysis of residuals in cross classified tables. Biometrics 29: 205220.

  • 30.

    Zou Y, Hu J, Wang ZX, Wang DM, Li MH, Ren GD, Duan ZX, Fu ZF, Plyusnin A, Zhang YZ, 2008. Molecular diversity and phylogeny of Hantaan virus in Guizhou, China: evidence for Guizhou as a radiation center of the present Hantaan virus. J Gen Virol 89: 19871997.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Razzauti M, Plyusnina A, Henttonen H, Plyusnin A, 2008. Accumulation of point mutations and reassortment of genomic RNA segments are involved in the microevolution of Puumala hantavirus in a bank vole (Myodes glareolus) population. J Gen Virol 89: 16491660.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Zou Y, Hu J, Wang ZX, Wang DM, Yu C, Zhou JZ, Fu ZF, Zhang YZ, 2008. Genetic characterization of hantaviruses isolated from Guizhou, China: evidence for spillover and reassortment in nature. J Med Virol 80: 10331041.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Rodriguez LL, Owens JH, Peters CJ, Nichol ST, 1998. Genetic reassortment among viruses causing hantavirus pulmonary syndrome. Virology 242: 99106.

  • 34.

    Klempa B, Schmidt HA, Ulrich R, Kaluz S, Labuda M, Meisel H, Hjelle B, Krüger DH, 2003. Genetic interaction between distinct Dobrava hantavirus subtypes in Apodemus agrarius and A. flavicollis in nature. J Virol 77: 804809.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Sibold C, Meisel H, Krüger DH, Labuda M, Lysy J, Kozuch O, Pejcoch M, Vaheri A, Plyusnin A, 1999. Recombination in Tula hantavirus evolution: analysis of genetic lineages from Slovakia. J Virol 73: 667675.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Ruo SL, Sanchez A, Elliott LH, Brammer LS, McCormick JB, Fisher-Hoch SP, 1991. Monoclonal antibodies to three strains of hantaviruses: Hantaan, R22, and Puumala. Arch Virol 119: 111.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Araki K, Yoshimatsu K, Ogino M, Ebihara H, Lundkvist A, Kariwa H, Takashima I, Arikawa J, 2001. Truncated hantavirus nucleocapsid proteins for serotyping Hantaan, Seoul, and Dobrava hantavirus infections. J Clin Microbiol 39: 23972404.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Nakamura I, Yoshimatsu K, Lee BH, Okumura M, Taruishi M, Araki K, Kariwa H, Takashima I, Arikawa J, 2008. Development of a serotyping ELISA system for Thailand virus infection. Arch Virol 153: 15371542.

    • PubMed
    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 456 430 57
Full Text Views 394 13 0
PDF Downloads 91 8 0
 
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save