1887

Abstract

Japanese patients with sporadic acute hepatitis E are infected with polyphyletic strains of hepatitis E virus (HEV). Hepatitis E is considered a zoonotic disease. Thus far in Japan, only three strains of swine HEV have been identified and an antibody study for HEV antibodies has not been done on Japanese pigs. To determine the prevalence of swine HEV infection in Japan and the extent of genetic variation among Japanese swine HEV strains, we tested serum samples obtained from 2500 pigs from 2 to 6 months of age at 25 commercial swine farms in Japan for the presence of IgG antibodies to HEV and swine HEV RNA. Anti-HEV antibodies were detected in 1448 pigs (58 %). One-hundred-and-thirteen (15 %) of the 750 3-month-old pigs and 24 (13 %) of the 180 4-month-old pigs were positive for swine HEV RNA. The nucleotide sequence of a 412 bp region within open reading frame 2 of the 137 swine HEV isolates was determined. Sequence analyses revealed that the 137 isolates shared 76·6–100 % nucleotide sequence identities and were classifiable into genotype III (93 %) or IV (7 %) and that the isolates from the same farm were ⩾97·1 % similar to each other. Phylogenetic analysis showed that the Japanese swine and human HEV isolates segregated into four clusters, with the highest nucleotide identity being 94·4–100 % between swine and human isolates in each cluster. These results indicate that swine HEV is widespread in the Japanese swine population and further support the hypothesis that swine serve as reservoirs for HEV infection.

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2003-04-01
2020-01-23
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References

  1. Arankalle, V. A., Chobe, L. P., Joshi, M. V., Chadha, M. S., Kundu, B. & Walimbe, A. M. ( 2002; ). Human and swine hepatitis E viruses from Western India belong to different genotypes. J Hepatol 36, 417–425.[CrossRef]
    [Google Scholar]
  2. Balayan, M. S. ( 1997; ). Epidemiology of hepatitis E virus infection. J Viral Hepat 4, 155–165.[CrossRef]
    [Google Scholar]
  3. Chandler, J. D., Riddell, M. A., Li, F., Love, R. J. & Anderson, D. A. ( 1999; ). Serological evidence for swine hepatitis E virus infection in Australian pig herds. Vet Microbiol 68, 95–105.[CrossRef]
    [Google Scholar]
  4. Clayson, E. T., Innis, B. L., Myint, K. W. A., Narupiti, S., Vaughn, D. W., Giri, S., Ranabhat, P. & Shrestha, M. P. ( 1995; ). Detection of hepatitis E virus infections among domestic swine in the Kathmandu Valley of Nepal. Am J Trop Med Hyg 53, 228–232.
    [Google Scholar]
  5. Erker, J. C., Desai, S. M., Schlauder, G. G., Dawson, G. J. & Mushahwar, I. K. ( 1999; ). A hepatitis E virus variant from the United States: molecular characterization and transmission in cynomolgus macaques. J Gen Virol 80, 681–690.
    [Google Scholar]
  6. Favorov, M. O., Nazarova, O. & Margolis, H. S. ( 1998; ). Is hepatitis E an emerging zoonotic disease? Am J Trop Med Hyg 59, 242.
    [Google Scholar]
  7. Favorov, M. O., Kosoy, M. Y., Tsarev, S. A., Childs, J. E. & Margolis, H. S. ( 2000; ). Prevalence of antibody to hepatitis E virus among rodents in the United States. J Infect Dis 181, 449–455.[CrossRef]
    [Google Scholar]
  8. Felsenstein, J. ( 1985; ). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.[CrossRef]
    [Google Scholar]
  9. Garkavenko, O., Obriadina, A., Meng, J., Anderson, D. A., Benard, H. J., Schroeder, B. A., Khudyakov, Y. E., Fields, H. A. & Croxson, M. C. ( 2001; ). Detection and characterization of swine hepatitis E virus in New Zealand. J Med Virol 65, 525–529.[CrossRef]
    [Google Scholar]
  10. Haqshenas, G., Shivaprasad, H. L., Woolcock, H. L., Read, D. H. & Meng, X. J. ( 2001; ). Genetic identification and characterization of a novel virus related to human hepatitis E virus from chickens with hepatitis–splenomegaly syndrome in the United States. J Gen Virol 82, 2449–2462.
    [Google Scholar]
  11. Harrison, T. J. ( 1999; ). Hepatitis E virus – an update. Liver 19, 171–176.
    [Google Scholar]
  12. Hartmann, W. J., Frosner, C. G. & Eichenlaub, D. ( 1998; ). Transmission of hepatitis E in Germany. Infection 26, 409.[CrossRef]
    [Google Scholar]
  13. Hsieh, S. Y., Meng, X. J., Wu, Y. H., Liu, S. T., Tam, A. W., Lin, D. Y. & Liaw, Y. F. ( 1999; ). Identity of a novel swine hepatitis E virus in Taiwan forming a monophyletic group with Taiwan isolates of human hepatitis E virus. J Clin Microbiol 37, 3828–3834.
    [Google Scholar]
  14. Huang, F. F., Haqshenas, G., Guenette, D. K., Halbur, P. G., Schommer, S. K., Pierson, F. W., Toth, T. E. & Meng, X. J. ( 2002a; ). Detection by reverse transcription-PCR and genetic characterization of field isolates of swine hepatitis E virus from pigs in different geographic regions of the United States. J Clin Microbiol 40, 1326–1332.[CrossRef]
    [Google Scholar]
  15. Huang, F. F., Haqshenas, G., Shivaprasad, H. L. & 7 other authors ( 2002b; ). Heterogeneity and seroprevalence of a newly identified avian hepatitis E virus from chickens in the United States. J Clin Microbiol 40, 4197–4202.[CrossRef]
    [Google Scholar]
  16. Ina, Y. ( 1994; ). ODEN: a program package for molecular evolutionary analysis and database search of DNA and amino acid sequences. Comput Appl Biosci 10, 11–12.
    [Google Scholar]
  17. Kabrane-Lazizi, Y., Fine, J. B., Elm, J. & 7 other authors ( 1999; ). Evidence for wide-spread infection of wild rats with hepatitis E virus in the United States. Am J Trop Med Hyg 61, 331–335.
    [Google Scholar]
  18. Kasorndorkbua, C., Halbur, P. G., Thomas, P. L., Guenette, D. K., Toth, T. E. & Meng, X. J. ( 2002; ). Use of a swine bioassay and a RT-PCR assay to assess the risk of transmission of swine hepatitis E virus in pigs. J Virol Methods 101, 71–78.[CrossRef]
    [Google Scholar]
  19. Kwok, S. & Higuchi, R. ( 1989; ). Avoiding false positives with PCR. Nature 339, 237–238.[CrossRef]
    [Google Scholar]
  20. Meng, X. J. ( 2000; ). Novel strains of hepatitis E virus identified from humans and other animal species: is hepatitis E a zoonosis? J Hepatol 33, 842–845.[CrossRef]
    [Google Scholar]
  21. Meng, X. J., Purcell, R. H., Halbur, P. G., Lehman, J. R., Webb, D. M., Tsareva, T. S., Haynes, J. S., Thacker, B. J. & Emerson, S. U. ( 1997; ). A novel virus in swine is closely related to the human hepatitis E virus. Proc Natl Acad Sci U S A 94, 9860–9865.[CrossRef]
    [Google Scholar]
  22. Meng, X. J., Halbur, P. G., Shapiro, M. S., Govindarajan, S., Bruna, J. D., Mushahwar, I. K., Purcell, R. H. & Emerson, S. U. ( 1998; ). Genetic and experimental evidence for cross-species infection by swine hepatitis E virus. J Virol 72, 9714–9721.
    [Google Scholar]
  23. Meng, X. J., Dea, S., Engle, R. E. & 10 other authors ( 1999; ). Prevalence of antibodies to the hepatitis E virus in pigs from countries where hepatitis E is common or is rare in the human population. J Med Virol 59, 297–302.[CrossRef]
    [Google Scholar]
  24. Meng, X. J., Wiseman, B., Elvinger, F., Guenette, D. K., Toth, T. E., Engle, R. E., Emerson, S. U. & Purcell, R. H. ( 2002; ). Prevalence of antibodies to hepatitis E virus in veterinarians working with swine and in normal blood donors in the United States and other countries. J Clin Microbiol 40, 117–122.[CrossRef]
    [Google Scholar]
  25. Mizuo, H., Suzuki, K., Takikawa, Y. & 8 other authors ( 2002; ). Polyphyletic strains of hepatitis E virus are responsible for sporadic cases of acute hepatitis in Japan. J Clin Microbiol 40, 3209–3218.[CrossRef]
    [Google Scholar]
  26. Okamoto, H., Takahashi, M., Nishizawa, T., Fukai, K., Muramatsu, U. & Yoshikawa, A. ( 2001; ). Analysis of the complete genome of indigenous swine hepatitis E virus isolated in Japan. Biochem Biophys Res Commun 289, 929–936.[CrossRef]
    [Google Scholar]
  27. Page, R. D. M. ( 1996; ). TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12, 357–358.
    [Google Scholar]
  28. Payne, C. J., Ellis, T. M., Plant, S. L., Gregory, A. R. & Wilcox, G. E. ( 1999; ). Sequence data suggesting big liver and spleen disease virus (BLSV) is genetically related to hepatitis E virus. Vet Microbiol 68, 119–125.[CrossRef]
    [Google Scholar]
  29. Pina, S., Buti, M., Cotrina, M., Piella, J. & Girones, R. ( 2000; ). HEV identified in serum from humans with acute hepatitis and in sewage of animal origin in Spain. J Hepatol 33, 826–833.[CrossRef]
    [Google Scholar]
  30. Purcell, R. H. & Emerson, S. U. ( 2001a; ). Hepatitis E virus. In Fields Virology, 4th edn, pp. 3051–3061. Edited by D. M. Knipe, P. M. Howley, D. E. Griffin, M. A. Martin, R. A. Lamb, B. Roizman & S. E. Straus. Philadelphia: Lippincott Williams and Wilkins.
  31. Purcell, R. H. & Emerson, S. U. ( 2001b; ). Animal models of hepatitis A and E. ILAR J 42, 161–177.[CrossRef]
    [Google Scholar]
  32. Reyes, G. R., Purdy, M. A., Kim, J. P., Luk, K. C., Young, L. M., Fry, K. E. & Bradley, D. W. ( 1990; ). Isolation of a cDNA from the virus responsible for enterically transmitted non-A, non-B hepatitis. Science 247, 1335–1339.[CrossRef]
    [Google Scholar]
  33. Saitou, N. & Nei, M. ( 1987; ). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406–425.
    [Google Scholar]
  34. Schlauder, G. G. & Mushahwar, I. K. ( 2001; ). Genetic heterogeneity of hepatitis E virus. J Med Virol 65, 282–292.[CrossRef]
    [Google Scholar]
  35. Schlauder, G. G., Dawson, G. J., Erker, J. C., Kwo, P. Y., Knigge, M. F., Smalley, D. L., Rosenblatt, J. E., Desai, S. M. & Mushahwar, I. K. ( 1998; ). The sequence and phylogenetic analysis of a novel hepatitis E virus isolated from a patient with acute hepatitis reported in the United States. J Gen Virol 79, 447–456.
    [Google Scholar]
  36. Schlauder, G. G., Desai, S. M., Zanetti, A. R., Tassopoulos, N. C. & Mushahwar, I. K. ( 1999; ). Novel hepatitis E virus (HEV) isolates from Europe: evidence for additional genotypes of HEV. J Med Virol 57, 243–251.[CrossRef]
    [Google Scholar]
  37. Schlauder, G. G., Frider, B., Sookoian, S., Castano, G. C. & Mushahwar, I. K. ( 2000; ). Identification of 2 novel isolates of hepatitis E virus in Argentina. J Infect Dis 182, 294–297.[CrossRef]
    [Google Scholar]
  38. Shrestha, S. M. ( 1987; ). Acute sporadic viral hepatitis in Nepal. Trop Gastroenterol 8, 99–105.
    [Google Scholar]
  39. Takahashi, K., Iwata, K., Watanabe, N., Hatahara, T., Ohta, Y., Baba, K. & Mishiro, S. ( 2001; ). Full-genome nucleotide sequence of a hepatitis E virus strain that may be indigenous to Japan. Virology 287, 9–12.[CrossRef]
    [Google Scholar]
  40. Takahashi, K., Kang, J. H., Ohnishi, S., Hino, K. & Mishiro, S. ( 2002a; ). Genetic heterogeneity of hepatitis E virus recovered from Japanese patients with acute sporadic hepatitis. J Infect Dis 185, 1342–1345.[CrossRef]
    [Google Scholar]
  41. Takahashi, M., Nishizawa, T., Yoshikawa, A., Sato, S., Isoda, N., Ido, K., Sugano, K. & Okamoto, H. ( 2002b; ). Identification of two distinct genotypes of hepatitis E virus in a Japanese patient with acute hepatitis who had not travelled abroad. J Gen Virol 83, 1931–1940.
    [Google Scholar]
  42. Tam, A. W., Smith, M. M., Guerra, M. E., Huang, C. C., Bradley, D. W., Fry, K. E. & Reyes, G. R. ( 1991; ). Hepatitis E virus (HEV): molecular cloning and sequencing of the full-length viral genome. Virology 185, 120–131.[CrossRef]
    [Google Scholar]
  43. Thompson, J. D., Higgins, D. G. & Gibson, T. J. ( 1994; ). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673–4680.[CrossRef]
    [Google Scholar]
  44. Tien, N. T., Clayson, H. T., Khiem, H. B., Sac, P. K., Corwin, A. L., Myint, K. S. & Vaughn, D. W. ( 1997; ). Detection of immunoglobulin G to the hepatitis E virus among several animal species in Vietnam. Am J Trop Med Hyg 57, 211.
    [Google Scholar]
  45. Wang, Y., Ling, R., Erker, J. C., Zhang, H., Li, H., Desai, S., Mushahwar, I. K. & Harrison, T. J. ( 1999; ). A divergent genotype of hepatitis E virus in Chinese patients with acute hepatitis. J Gen Virol 80, 169–177.
    [Google Scholar]
  46. Wang, Y., Zhang, H., Ling, R., Li, H. & Harrison, T. J. ( 2000; ). The complete sequence of hepatitis E virus genotype 4 reveals an alternative strategy for translation of open reading frames 2 and 3. J Gen Virol 81, 1675–1686.
    [Google Scholar]
  47. Wang, Y., Levine, D. F., Bendall, R. P., Teo, C. G. & Harrison, T. J. ( 2001; ). Partial sequence analysis of indigenous hepatitis E virus isolated in the United Kingdom. J Med Virol 65, 706–709.[CrossRef]
    [Google Scholar]
  48. Wang, Y., Zhang, H., Xia, N. & 11 other authors ( 2002; ). Prevalence, isolation, and partial sequence analysis of hepatitis E virus from domestic animals in China. J Med Virol 67, 516–521.[CrossRef]
    [Google Scholar]
  49. Worm, H. C., Schlauder, G. G., Wurzer, H. & Mushahwar, I. K. ( 2000; ). Identification of a novel variant of hepatitis E virus in Austria: sequence, phylogenetic and serological analysis. J Gen Virol 81, 2885–2890.
    [Google Scholar]
  50. Wu, J. C., Chen, C. M., Chiang, T. Y., Tsai, W. H., Jeng, W. J., Sheen, I. J., Kin, C. C. & Meng, X. J. ( 2002; ). Spread of hepatitis E virus among different-aged pigs: two-year survey in Taiwan. J Med Virol 66, 488–492.[CrossRef]
    [Google Scholar]
  51. Zanetti, A. R., Schlauder, G. G., Romano, L., Tanzi, E., Fabris, P., Dawson, G. J. & Mushahwar, I. K. ( 1999; ). Identification of a novel variant of hepatitis E virus in Italy. J Med Virol 57, 356–360.[CrossRef]
    [Google Scholar]
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