Mode of infection of Hokkaido virus (genus Hantavirus) among grey red-backed voles, Myodes rufocanus, in Hokkaido, Japan

Microbiology and Immunology

Volumn 51, Issue 11, 2007, Pages 1081-1090

  Abu Daud, Nur Hardy ^a   Kariwa, Hiroaki ^a   Tanikawa, Yoich ^a   Nakamura, Ichiro ^a   Seto, Takahiro ^a   Miyashita, Daisuke ^a   Yoshii, Kentaro ^a   Nakauchi, Mina ^a   Yoshimatsu, Kumiko ^b   Arikawa, Jiro ^b   Takashima, Ikuo ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Epidemiology; Hantavirus; Rodent

Indexed keywords

VIRUS RNA;

ANTIBODY BLOOD LEVEL; ARTICLE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HANTAVIRUS; HEALTH SURVEY; HUMAN; JAPAN; MALE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; SEROPREVALENCE; VIRUS INFECTION;

ANIMALIA; BUNYAVIRIDAE; CLETHRIONOMYS; HANTAVIRUS; RODENTIA;

EID: 36349019909     PISSN: 03855600     EISSN: 13480421     Source Type: Journal    
DOI: 10.1111/j.1348-0421.2007.tb04003.x     Document Type: Article

References (61)

1. Abbott, K.D., Ksiazek, T.G., and Mills, J.N. 1999. Longterm hantavirus persistence in rodent populations in central Arizona. Emerg. Infect. Dis. 5: 102-112.
2. Arikawa, J., Schmaljohn, A.L., Dalrymple, J.M., and Schmaljohn, C.S. 1989. Characterization of Hantaan virus envelope glycoprotein antigenic determinants defined by monoclonal antibodies. J. Gen. Virol. 70: 615-624.
3. Arikawa, J., Yoshimatsu, K., and Kariwa, H. 2001. Epidemiology and epizootiology of hantavirus infection in Japan. Jpn. J. Infect. Dis. 54: 95-102.
4. Avsic-Zupanc, T., Xiao, S.Y., Stojanovic, R., Gligic, A., van der Groen, G., and LeDuc, J.W. 1992. Characterization of Dobrava virus: a Hantavirus from Slovenia, Yugoslavia. J. Med. Virol. 38: 132-137.
5. Bernshtein, A.D., Apekina, N.S., Mikhailova, T.V., Myasnikov, Y.A., Khlyap, L.A., Korotkov, Y.S., and Gavrilovskaya, I.N. 1999. Dynamics of Puumala hantavirus infection in naturally infected bank voles (Clethrionomys glareolus). Arch. Virol. 144: 2415-2428.
6. Bharadwaj, M., Botten, J., Torrez-Martinez, N., and Hjelle, B. 1997. Rio Mamore virus: genetic characterization of a newly recognized hantavirus of the pygmy rice rat, Oligoryzomys microtis, from Bolivia. Am. J. Trop. Med. Hyg. 57: 368-374.
7. Boone, J.D., Otteson, E.W., McGwire, K.C., Villard, P., Rowe, J.E., and St. Jeor, S.C. 1998. Ecology and demographics of hantavirus infections in rodent populations in the Walker River Basin of Nevada and California. Am. J. Trop. Med. Hyg. 59: 445-451.
8. Calderon, G., Pini, N., Bolpe, J., Levis, S., Mills, J., Segura, E., Guthmann, N., Cantoni, G., Becker, J., Fonollat, A., Ripoll, C., Bortman, M., Benedetti, R., Sabattini, M., and Enria, D. 1999. Hantavirus reservoir hosts associated with peridomestic habitats in Argentina. Emerg. Infect. Dis. 5: 792-797.
9. Calisher, C.H., Root, J.J., Mills, J.N., Rowe, J.E., Reeder, S.A., Jentes, E.S., Wagoner, K., and Beaty, B.J. 2005. Epizootiology of Sin Nombre and El Moro Canyon hantaviruses, southeastern Colorado, 1995-2000. J. Wildl. Dis. 41: 1-11.
10. Childs, J.E., Glass, G.E., Korch, G.W., and Leduc, J.W. 1989. Effects of hantaviral infection on survival, growth and fertility in wild rat (Rattus norvegicus) populations of Baltimore, Maryland. J. Wildl. Dis. 25: 469-476.
11. Childs, J.E., Ksiazek, T.G., Spiropoulou, C.F., Krebs, J.W., Morzunov, S., Maupin, G.O., Gage, K.L., Rollin, P.E., Sarisky, J., Enscore, R.E., Frey, J.K., Peters, C.J., and Nichol, S.T. 1994. Serologic and genetic identification of Peromyscus maniculatus as the primary rodent reservoir for a new hantavirus in the southwestern United States. J. Infect. Dis. 169: 1271-1280.
12. Duchin, J.S., Koster, F.T., Peters, C.J., Simpson, G.L., Tempest, B., Zaki, S.R., Ksiazek, T.G., Rollin, P.E., Nichol, S., Umland, E.T., Moolenaar, R.L., Reef, S.E., Nolte, K.B., Gallaher, M.M., Butler, J.C., and Breimen, R.F. 1994. Hantavirus pulmonary syndrome: a clinical description of 17 patients with a newly recognized disease. N. Engl. J. Med. 330: 949-955.
13. Enria, D., Padula, P., Segura, E.L., Pini, N., Edelstein, A., Posse, C.R., and Weissenbacher, M.C. 1996. Hantavirus pulmonary syndrome in Argentina. Possibility of person to person transmission. Medicina (B Aires) 56: 709-711.
14. Escutenaire, S., Chalon, P., De Jaegere, F., Karelle-Bui, L., Mees, G., Brochier, B., Rozenfeld, F., and Pastoret, P.P. 2002. Behavioral, physiologic, and habitat influences on the dynamics of Puumala virus infection in bank voles (Clethrionomys glareolus). Emerg. Infect. Dis. 8: 930-936.
15. Escutenaire, S., Chalon, P., Verhagen, R., Heyman, P., Thomas, I., Karelle-Bui, L., Avsic-Zupanc, T., Lundkvist, A., Plyusnin, A., and Pastoret, P.P. 2000. Spatial and temporal dynamics of Puumala hantavirus infection in red bank vole (Clethrionomys glareolus) population in Belgium. Virus Res. 67: 91-107.
16. Gavrilovskaya, I., Apekina, N., Okulova, N., Demina, V., Bernshtein, A., and Myasnikov, Y. 1993. IgG avidity assay for estimation of the time after onset of hantavirus infection in colonized and wild bank voles. Arch. Virol. 132: 359-367.
17. Glass, G.E., Childs, J.E., Korch, G.W., and LeDuc, J.W. 1988. Association of intraspecific wounding with hantaviral infection in wild rats (Rattus norvegicus). Epidemiol. Infect. 101: 459-472.
18. Hinson, E.R., Shone, S.M., Zink, M.C., Glass, G.E., and Klein, S.L. 2004. Wounding: the primary mode of Seoul virus transmission among male Norway rats. Am. J. Trop. Med. Hyg. 70: 310-317.
19. Hutchinson, K.L., Rollin, P.E., and Peters, C.J. 1998. Pathogenesis of a North American hantavirus, Black Creek Canal virus, in experimentally infected Sigmodon hispidus. Am. J. Trop. Med. Hyg. 59: 58-65.
20. Iwasa, M.A., Kariwa, H., Cui, B.Z., Lokugamage, K., Lokugamage, N., Hagiya, T., Mizutani, T., and Takashima, I. 2004. Modes of hantavirus transmission in a population of Clethrionomys rufocanus bedfordiae inferred from mitochondrial and microsatellite DNA analyses. Arch. Virol. 149: 929-941.
21. Johnson, A.M., Bowen, M.D., Ksiazek, T.G., Williams, R.J., Bryan, R.T., Mills, J.N., Peters, C.J., and Nichol, S.T. 1997. Laguna Negra virus associated with HPS in western Paraguay and Bolivia. Virology 238: 115-127.
22. Kariwa, H., Isegawa, Y., Arikawa, J., Takashima, I., Ueda, S., Yamanishi, K., and Hashimoto, N. 1994. Comparison of nucleotide sequences of M genome segments among Seoul virus strains isolated from eastern Asia. Virus Res. 33: 27-38.
23. Kariwa, H., Kimura, M., Yoshizumi, S., Arikawa, J., Yoshimatsu, K., Takashima, I., and Hashimoto, N. 1996. Modes of Seoul virus infections: persistency in newborn rats and transiency in adult rats. Arch. Virol. 141: 2327-2338.
24. Kariwa, H., Yoshimatsu, K., Araki, K., Chayama, K., Kumada, H., Ogino, M., Ebihara, H., Murphy, M.E., Mizutani, T., Takashima, I., and Arikawa, J. 2000. Detection of hantaviral antibodies among patients with hepatitis of unknown etiology in Japan. Microbiol. Immunol. 44: 357-362.
25. Kariwa, H., Yoshimatsu, K., Sawabe, J., Yokota, E., Arikawa, J., Takashima, I., Fukushima, H., Lundkvist, A., Shubin, F.N., Isachkova, L.M., Slonova, R.A., Leonova, G.N., and Hashimoto, N. 1999. Genetic diversities of hantaviruses among rodents in Hokkaido, Japan and Far East Russia. Virus Res. 59: 219-228.
26. Kariwa, H., Yoshizumi, S., Arikawa, J., Yoshimatsu, K., Takahashi, K., Takashima, I., and Hashimoto, N. 1995. Evidence for the existence of Puumula-related virus among Clethrionomys rufocanus in Hokkaido, Japan. Am. J. Trop. Med. Hyg. 53: 222-227.
27. Kawamata, J., Yamanouchi, T., Dohmae, K., Miyamoto, H., Takahaski, M., Yamanishi, K., Kurata, T., and Lee, H.W. 1987. Control of laboratory acquired hemorrhagic fever with renal syndrome (HFRS) in Japan. Lab. Anim. Sci. 37: 431-436.
28. Klein, S.L., Bird, B.H., and Glass, G.E. 2000. Sex differences in Seoul virus infection are not related to adult sex steroid concentrations in Norway rats. J. Virol. 74: 8213-8217.
29. Ksiazek, T.G., Nichol, S.T., Mills, J.N., Groves, M.G., Wozniak, A., McAdams, S., Monroe, M.C., Johnson, A.M., Martin, M.L., Peters, C.J., and Rollin, P.E. 1997. Isolation, genetic diversity, and geographic distribution of Bayou virus (Bunyaviridae: hantavirus). Am. J. Trop. Med. Hyg. 57: 445-448.
30. Lee, H.W., Baek, L.J., and Johnson, K.M. 1982. Isolation of Hantaan virus, the etiologic agent of Korean hemorrhagic fever, from wild urban rats. J. Infect. Dis. 146: 638-644.
31. Lee, H.W., Lee, P.W., Baek, L.J., Song, C.K., and Seong, I.W. 1981. Intraspecific transmission of Hantaan virus, etiologic agent of Korean hemorrhagic fever, in the rodent Apodemus agrarius. Am. J. Trop. Med. Hyg. 30: 1106-1112.
32. Lee, H.W., Lee, P.W., and Johnson, K.M. 1978. Isolation of the etiologic agent of Korean hemorrhagic fever. J. Infect. Dis. 137: 298-308.
33. Lee, H.W., Lee, P.W., Tamura, M., Tamura, T., and Okuno, Y. 1979. Etiological relation between Korean hemorrhagic fever and epidemic hemorrhagic fever in Japan. Biken J. 22: 41-45.
34. Lokugamage, N., Kariwa, H., Lokugamage, K., Hagiya, T., Miyamoto, H., Iwasa, M.A., Araki, K., Yoshimatsu, K., Arikawa, J., Mizutani, T., and Takashima, I. 2003. Development of an efficient method for recovery of Puumala and Puumala-related viruses by inoculation of Mongolian gerbils. J. Vet. Med. Sci. 65: 1189-1194.
35. Lokugamage, N., Kariwa, H., Lokugamage, K., Iwasa, M.A., 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., and Takashima, I. 2004. Epizootiological and epidemiological study of hantavirus infection in Japan. Microbiol. Immunol. 48: 843-851.
36. LeDuc, J.W. 1987. Epidemiology of Hantaan and related viruses. Lab. Anim. Sci. 37: 413-418.
37. Lundkvist, A., Fatouros, A., and Niklasson, B. 1991. Antigenic variation of European haemorrhagic fever with renal syndrome virus strains characterized using bank vole monoclonal antibodies. J. Gen. Virol. 72: 2097-2103.
38. Mills, J.N., Ksiazek, T.G., Ellis, B.A., Rollin, P.E., Nichol, S.T., Yates, T.L., Gannon, W.L., Levy, C.E., Engelthaler, D.M., Davis, T., Tanda, D.T., Frampton, J.W., Nichols, C.R., Peters, C.J., and Childs, J.E. 1997. Patterns of association with host and habitat: antibody reactive with Sin Nombre virus in small mammals in the major biotic communities of the southwestern United States. Am. J. Trop. Med. Hyg. 56: 273-284.
39. Miyamoto, H., Kariwa, H., Araki, K., Lokugamage, K., Hayasaka, D., Cui, B.Z., Lokugamage, N., Ivanov, L.I., Mizutani, T., Iwasa, M.A., Yoshimatsu, K., Arikawa, J., and 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: 1543-1556.
40. Morzunov, S.P., Rowe, J.E., Ksiazek, T.G., Peters, C.J., St. Jeor, S.C., and Nichol, S.T. 1998. Genetic analysis of the diversity and origin of hantaviruses in Peromyscus leucopus mice in North America. J. Virol. 72: 57-64.
41. Muranyi, W., Bahr, U., Zeier, M., and van der Woude, F.J. 2005. Hantavirus infection. J. Am. Soc. Nephrol. 16: 3669-3679.
42. Netski, D., Thran, B.H., and St Jeor, S.C. 1999. Sin Nombre virus pathogenesis in Peromyscus maniculatus. J. Virol. 73: 585-591.
43. Nichol, S.T., Spiropoulou, C.F., Morzunov, S., Rollin, P.E., Ksiazek, T.G., Feldmann, H., Sanchez, A., Childs, J., Zaki, S., and Peters, C.J. 1993. Genetic identification of a hantavirus associated with an outbreak of acute respiratory illness. Science 262: 914-917.
44. Niklasson, B., Hornfeldt, B., Lundkvist, A., Bjorsten, S., and Leduc, J. 1995. Temporal dynamics of Puumala virus antibody prevalence in voles and of nephropathia epidemica incidence in humans. Am. J. Trop. Med. Hyg. 53: 134-140.
45. Olsson, G.E., White, N., Ahlm, C., Elgh, F., Verlemyr, A.C., Juto, P., and Palo, R.T. 2002. Demographic factors associated with hantavirus infection in bank voles (Clethrionomys glareolus). Emerg. Infect. Dis. 8: 924-929.
46. Padula, P., Figueroa, R., Navarrete, M., Pizarro, E., Cadiz, R., Bellomo, C., Jofre, C., Zaror, L., Rodriguez, E., and Murua, R. 2004. Transmission study of Andes hantavirus infection in wild sigmodontine rodents. J. Virol. 78: 11972-11979.
47. Padula, P.J., Edelstein, A., Miguel, S.D., Lopez, N.M., Rossi, C.M., and Rabinovich, R.D. 1998. Hantavirus pulmonary syndrome outbreak in Argentina: molecular evidence for person-to-person transmission of Andes virus. Virology 241: 323-330.
48. Peters, C.J., Simpson, G.L., and Levy, H. 1999. Spectrum of hantavirus infection: hemorrhagic fever with renal syndrome and hantavirus pulmonary syndrome. Annu. Rev. Med. 50: 531-545.
49. Plyusnin, A., Vapalahti, O., Lankinen, H., Lehvaslaiho, H., Apekina, N., Myasnikov, Y., Kallio-Kokko, H., Henttonen, H., Gavrilovskaya, I., and Vaheri, A. 1994. Tula virus: a newly detected hantavirus carried by European common voles. J. Virol. 68: 7833-7839.
50. Ravkov, E.V., Rollin, P.E., Ksiazek, T.G., Peters, C.J., and Nichols, S.T. 1995. Genetic and serologic analysis of Black Creek Canal virus and its association with human disease and Sigmodon hispidus infection. Virology 210: 482-489.
51. Rollin, P.E., Ksiazek, T.G., Elliott, L.H., Ravkov, E.V., Martin, M.L., Morzunov, S., Livingstone, W., Monroe, M., Glass, G., Ruo, S., Khan, A.S., Childs, J.E., Nichols, S.T., and Peters, C.J. 1995. Isolation of black creek canal virus, a new hantavirus from Sigmodon hispidus in Florida. J. Med. Virol. 46: 35-39.
52. Schmaljohn, C.S., Hasty, S.E., Harrison, S.A., and Dalrymple, J.M. 1983. Characterization of Hantaan virions, the prototype virus of hemorrhagic fever with renal syndrome. J. Infect. Dis. 148: 1005-1012.
53. Song, J.W., Baek, L.J., Gajdusek, D.C., Yanagihara, R., Gavrilovskaya, I., Luft, B.J., Mackow, E.R., and Hjelle, B. 1994. Isolation of pathogenic hantavirus from white-footed mouse (Peromyscus leucopus). Lancet 344: 1637.
54. Tamura, M. 1964. Occurrence of epidemic hemorrhagic fever in Osaka city: first cases found in Japan with characteristic feature of marked proteinuria. Biken J. 7: 79-94.
55. Torrez-Martinez, N., Bharadwaj, M., Goade, D., Delury, J., Moran, P., Hicks, B., Nix, B., Davis, J.L., and Hjelle, B. 1998. Bayou virus-associated hantavirus pulmonary syndrome in Eastern Texas: identification of the rice rat, Oryzomys palustris, as reservoir host. Emerg. Infect. Dis. 4: 105-111.
56. Tsai, T.F. 1987. Hemorrhagic fever with renal syndrome: mode of transmission to humans. Lab. Anim. Sci. 37: 428-430.
57. Umenai, T., Lee, H.W., Lee, P.W., Saito, T., Toyoda, T., Hongo, M., Yoshinaga, K., Nobunaga, T., Horiuchi, T., and Ishida, N. 1979. Korean haemorrhagic fever in staff in an animal laboratory. Lancet 1: 1314-1316.
58. Verhagen, R., Leirs, H., Tkachenko, E., and Van Der Groen, G. 1986. Ecological and epidemiological data on hantavirus in bank vole population in Belgium. Arch. Virol. 91: 193-205.
59. Yanagihara, R., Amyx, H.L., and Gajdusek, D.C. 1985. Experimental infection with Puumala virus, the etiologic agent of nephropathia epidemica, in bank voles (Clethrionomys glareolus). J. Virol. 55: 34-38.
60. Yanagihara, R., Svedmyr, A., Amyx, H.L., Lee, P., Goldgaber, D., Gajdusek, D.C., Gibbs, C.J., Jr., and Nystrom, K. 1984. Isolation and propagation of nephropathia epidemica virus in bank voles. Scand. J. Infect. Dis. 16: 225-228.
61. Zeier, M., Handermann, M., Bahr, U., Rensch, B., Muller, S., Kehm, R., Muranyi, W., and Darai, G. 2005. New ecological aspects of hantavirus infection: a change of a paradigm and a challenge of prevention - a review. Virus Genes 30: 157-180.