1887

Abstract

(HEV) is a zoonotic pathogen of which pigs are reservoirs. To determine the presence of HEV RNA in commercial pig livers sold in local grocery stores in the USA, 127 packages of commercial pig liver were purchased and tested by a universal RT-PCR assay capable of detecting all four known HEV genotypes. Among the 127 livers tested, 14 were positive for HEV RNA. Sequence and phylogenetic analyses revealed that the 14 isolates all belonged to genotype 3. An animal study was subsequently conducted in pigs to determine whether the PCR-positive pig livers still contained infectious virus. The results showed that pigs inoculated with two of the three PCR-positive pig-liver homogenates became infected, as evidenced by the detection of faecal virus shedding, viraemia and seroconversion. The data demonstrated that commercial pig livers sold in grocery stores are contaminated by HEV and that the contaminating virus remains infectious, thus raising a public-health concern for food-borne HEV infection.

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2007-03-01
2019-11-13
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References

  1. Arankalle, V. A., Chadha, M. S., Tsarev, S. A., Emerson, S. U., Risbud, A. R., Banerjee, K. & Purcell, R. H. ( 1994; ). Seroepidemiology of water-borne hepatitis in India and evidence for a third enterically-transmitted hepatitis agent. Proc Natl Acad Sci U S A 91, 3428–3432.[CrossRef]
    [Google Scholar]
  2. Banks, M., Heath, G. S., Grierson, S. S., King, D. P., Gresham, A., Girones, R., Widen, F. & Harrison, T. J. ( 2004; ). Evidence for the presence of hepatitis E virus in pigs in the United Kingdom. Vet Rec 154, 223–227.[CrossRef]
    [Google Scholar]
  3. Caron, M., Enouf, V., Than, S. C., Dellamonica, L., Buisson, Y. & Nicand, E. ( 2006; ). Identification of genotype 1 hepatitis E virus in samples from swine in Cambodia. J Clin Microbiol 44, 3440–3442.[CrossRef]
    [Google Scholar]
  4. Cooper, K., Huang, F. F., Batista, L., Rayo, C. D., Bezanilla, J. C., Toth, T. E. & Meng, X. J. ( 2005; ). Identification of genotype 3 hepatitis E virus (HEV) in serum and fecal samples from pigs in Thailand and Mexico, where genotype 1 and 2 HEV strains are prevalent in the respective human populations. J Clin Microbiol 43, 1684–1688.[CrossRef]
    [Google Scholar]
  5. Drobeniuc, J., Favorov, M. O., Shapiro, C. N., Bell, B. P., Mast, E. E., Dadu, A., Culver, D., Iarovoi, P., Robertson, B. H. & Margolis, H. S. ( 2001; ). Hepatitis E virus antibody prevalence among persons who work with swine. J Infect Dis 184, 1594–1597.[CrossRef]
    [Google Scholar]
  6. Emerson, S. U. & Purcell, R. H. ( 2003; ). Hepatitis E virus. Rev Med Virol 13, 145–154.[CrossRef]
    [Google Scholar]
  7. Emerson, S. U., Zhang, M., Meng, X. J., Nguyen, H., Huang, Y. K. & Purcell, R. H. ( 2001; ). Recombinant hepatitis E virus genomes infectious for primates: importance of capping and discovery of a cis-reactive element. Proc Natl Acad Sci U S A 98, 15270–15275.[CrossRef]
    [Google Scholar]
  8. Emerson, S. U., Anderson, D., Arankalle, A., Meng, X.-J., Purdy, M., Schlauder, G. G. & Tsarev, S. A. ( 2004; ). Genus Hepevirus. In Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses, pp. 853–857. Edited by C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger & L. A. Ball. London: Elsevier/Academic Press.
  9. Emerson, S. U., Arankalle, V. A. & Purcell, R. H. ( 2005; ). Thermal stability of hepatitis E virus. J Infect Dis 192, 930–933.[CrossRef]
    [Google Scholar]
  10. Halbur, P. G., Kasorndorkbua, C., Gilbert, C., Guenette, D., Potters, M. B., Purcell, R. H., Emerson, S. U., Toth, T. E. & Meng, X. J. ( 2001; ). Comparative pathogenesis of infection of pigs with hepatitis E virus recovered from a pig and a human. J Clin Microbiol 39, 918–923.[CrossRef]
    [Google Scholar]
  11. Hamid, S. S., Jafri, S. M., Khan, H., Shah, H., Abbas, Z. & Fields, H. ( 1996; ). Fulminant hepatic failure in pregnant women: acute fatty liver or acute viral hepatitis? J Hepatol 25, 20–27.[CrossRef]
    [Google Scholar]
  12. Haqshenas, G., Shivaprasad, H. L., Woolcock, P. R., 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]
  13. Harrison, T. J. ( 1999; ). Hepatitis E virus – an update. Liver 19, 171–176.
    [Google Scholar]
  14. 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]
  15. Huang, C. C., Nguyen, D., Fernandez, J., Yun, K. Y., Fry, K. E., Bradley, D. W., Tam, A. W. & Reyes, G. R. ( 1992; ). Molecular cloning and sequencing of the Mexico isolate of hepatitis E virus (HEV). Virology 191, 550–558.[CrossRef]
    [Google Scholar]
  16. Huang, F. F., Haqshenas, G., Guenette, D. K., Halbur, P. G., Schommer, S. K., Pierson, F. W., Toth, T. E. & Meng, X. J. ( 2002; ). 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]
  17. Huang, F. F., Sun, Z. F., Emerson, S. U., Purcell, R. H., Shivaprasad, H. L., Pierson, F. W., Toth, T. E. & Meng, X. J. ( 2004; ). Determination and analysis of the complete genomic sequence of avian hepatitis E virus (avian HEV) and attempts to infect rhesus monkeys with avian HEV. J Gen Virol 85, 1609–1618.[CrossRef]
    [Google Scholar]
  18. Mast, E. E., Kuramoto, I. K., Favorov, M. O., Schoening, V. R., Burkholder, B. T., Shapiro, C. N. & Holland, P. V. ( 1997; ). Prevalence of and risk factors for antibody to hepatitis E virus seroreactivity among blood donors in Northern California. J Infect Dis 176, 34–40.[CrossRef]
    [Google Scholar]
  19. Matsuda, H., Okada, K., Takahashi, K. & Mishiro, S. ( 2003; ). Severe hepatitis E virus infection after ingestion of uncooked liver from a wild boar. J Infect Dis 188, 944.[CrossRef]
    [Google Scholar]
  20. Meng, X. J. ( 2000a; ). Zoonotic and xenozoonotic risks of the hepatitis E virus. Infect Dis Rev 2, 35–41.
    [Google Scholar]
  21. Meng, X. J. ( 2000b; ). 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]
  22. Meng, X. J. ( 2003; ). Swine hepatitis E virus: cross-species infection and risk in xenotransplantation. Curr Top Microbiol Immunol 278, 185–216.
    [Google Scholar]
  23. Meng, X.-J. ( 2005; ). Hepatitis E as a zoonotic disease. In Viral Hepatitis, 3rd edn, pp. 611–623. Edited by H. Thomas, S. Lemon & A. J. Zuckermann. Oxford: Blackwell Publishing.
  24. Meng, X. J. & Halbur, P. G. ( 2005; ). Swine hepatitis E virus. In Diseases of Swine, 9th edn, pp. 537–545. Edited by B. E. Straw, J. J. Zimmerman, S. D'Allaire & D. J. Taylor. Ames, IA: Blackwell Publishing/Iowa State University Press.
  25. 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]
  26. Meng, X. J., Halbur, P. G., Shapiro, M. S., Govindarajan, S., Bruna, J. D., Mushahwar, I. K., Purcell, R. H. & Emerson, S. U. ( 1998a; ). Genetic and experimental evidence for cross-species infection by swine hepatitis E virus. J Virol 72, 9714–9721.
    [Google Scholar]
  27. Meng, X. J., Halbur, P. G., Haynes, J. S., Tsareva, T. S., Bruna, J. D., Royer, R. L., Purcell, R. H. & Emerson, S. U. ( 1998b; ). Experimental infection of pigs with the newly identified swine hepatitis E virus (swine HEV), but not with human strains of HEV. Arch Virol 143, 1405–1415.[CrossRef]
    [Google Scholar]
  28. 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]
  29. 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]
  30. Purcell, R. H. ( 1996; ). Hepatitis E virus. In Fields Virology, 3rd edn, pp. 2831–2843. Edited by B. N. Fields, D. M. Knipe & P. M. Howley. Philadelphia, PA: Lippincott–Raven.
  31. 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]
  32. Sun, Z. F., Larsen, C. T., Huang, F. F., Billam, P., Pierson, F. W., Toth, T. E. & Meng, X. J. ( 2004; ). Generation and infectivity titration of an infectious stock of avian hepatitis E virus (HEV) in chickens and cross-species infection of turkeys with avian HEV. J Clin Microbiol 42, 2658–2662.[CrossRef]
    [Google Scholar]
  33. Takahashi, M., Nishizawa, T., Miyajima, H., Gotanda, Y., Iita, T., Tsuda, F. & Okamoto, H. ( 2003; ). Swine hepatitis E virus strains in Japan form four phylogenetic clusters comparable with those of Japanese isolates of human hepatitis E virus. J Gen Virol 84, 851–862.[CrossRef]
    [Google Scholar]
  34. Tam, A. W., Smith, M. M., Guerra, M. E., Huang, C. C., Bradley, D. W., Fry, K. E. & Reyes, G. R. ( 1991; ). Molecular cloning and sequencing of the full-length viral genome. Virology 185, 120–131.[CrossRef]
    [Google Scholar]
  35. Tei, S., Kitajima, N., Takahashi, K. & Mishiro, S. ( 2003; ). Zoonotic transmission of hepatitis E virus from deer to human beings. Lancet 362, 371–373.[CrossRef]
    [Google Scholar]
  36. Tei, S., Kitajima, N., Ohara, S., Inoue, Y., Miki, M., Yamatani, T., Yamabe, H., Mishiro, S. & Kinoshita, Y. ( 2004; ). Consumption of uncooked deer meat as a risk factor for hepatitis E virus infection: an age- and sex-matched case-control study. J Med Virol 74, 67–70.[CrossRef]
    [Google Scholar]
  37. Thomas, D. L., Yarbough, P. O., Vlahov, D., Tsarev, S. A., Nelson, K. E., Saah, A. J. & Purcell, R. H. ( 1997; ). Seroreactivity to hepatitis E virus in areas where the disease is not endemic. J Clin Microbiol 35, 1244–1247.
    [Google Scholar]
  38. van der Poel, W. H., Verschoor, F., van der Heide, R., Herrera, M. I., Vivo, A., Kooreman, M. & de Roda Husman, A. M. ( 2001; ). Hepatitis E virus sequences in swine related to sequences in humans, The Netherlands. Emerg Infect Dis 7, 970–976.[CrossRef]
    [Google Scholar]
  39. 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]
  40. Withers, M. R., Correa, M. T., Morrow, M., Stebbins, M. E., Seriwatana, J., Webster, W. D., Boak, M. B. & Vaughn, D. W. ( 2002; ). Antibody levels to hepatitis E virus in North Carolina swine workers, non-swine workers, swine, and murids. Am J Trop Med Hyg 66, 384–388.
    [Google Scholar]
  41. Yazaki, Y., Mizuo, H., Takahashi, M., Nishizawa, T., Sasaki, N., Gotanda, Y. & Okamoto, H. ( 2003; ). Sporadic acute or fulminant hepatitis E in Hokkaido, Japan, may be food-borne, as suggested by the presence of hepatitis E virus in pig liver as food. J Gen Virol 84, 2351–2357.[CrossRef]
    [Google Scholar]
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