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

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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

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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

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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

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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

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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

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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

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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

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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

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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

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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

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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

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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

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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

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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.

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