1887

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Volume 85, Issue 3

Genetic identification of avian hepatitis E virus (HEV) from healthy chicken flocks and characterization of the capsid gene of 14 avian HEV isolates from chickens with hepatitis–splenomegaly syndrome in different geographical regions of the United States Free

Abstract

Avian hepatitis E virus (HEV), a novel virus identified from chickens with hepatitis–splenomegaly (HS) syndrome, is genetically and antigenically related to human HEV. Recently, it was found that avian HEV antibody is also prevalent in healthy chickens. A prospective study was done on a known seropositive but healthy chicken farm to identify avian HEV isolates from healthy chickens. Fourteen chickens were randomly selected, tagged and monitored under natural conditions for 19 weeks. All 14 chickens were seronegative at the beginning of the study at 12 weeks of age. By 21 weeks of age, all 14 chickens had seroconverted to avian HEV antibody. None of the chickens had any sign of HS syndrome. Partial helicase gene and capsid gene sequences of avian HEV isolates recovered from a healthy chicken were determined and found to share 75–97 % nucleotide sequence identity with the corresponding regions of avian HEV isolates from chickens with HS syndrome. Thus far, only one strain of avian HEV from a chicken with HS syndrome has been genetically characterized for its capsid gene, therefore the capsid gene region of an additional 14 isolates from chickens with HS syndrome were also characterized. The capsid genes of avian HEV isolates from chickens with HS syndrome were found to be heterogeneic, sharing 76–100 % nucleotide sequence identity with each other. This study indicates that avian HEV is enzootic in chicken flocks and spreads subclinically among chickens in the United States and that the virus is heterogeneic.

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2004-03-01
2024-04-18
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References

  1. Aggarwal R., Krawczynski K. 2000; Hepatitis E: an overview and recent advances in clinical and laboratory research. J Gastroenterol Hepatol 15:9–20
     [Google Scholar]
  2. 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
     [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
     [Google Scholar]
  4. Clemente-Casares P., Pina S., Buti M., Jardi R., Martin M., Bofill-Mas S., Girones R. 2003; Hepatitis E virus epidemiology in industrialized countries. Emerg Infect Dis 9:448–454
     [Google Scholar]
  5. Emerson S. U., Zhang M., Meng X. J., Nguyen H., Huang Y., 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
     [Google Scholar]
  6. 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]
  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 184:449–455
     [Google Scholar]
  8. Garkavenko O., Obriadina A., Meng J., Anderson D. A., Benard H. J., Schroeder B. A., Khudaakov 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
     [Google Scholar]
  9. 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 viruses recovered from a pig and a human. J Clin Microbiol 39:918–923
     [Google Scholar]
  10. Haqshenas G., Meng X. J. 2001; Determination of the nucleotide sequences at the extreme 5′ and 3′ ends of swine hepatitis E virus genome. Arch Virol 146:2461–2467
     [Google Scholar]
  11. 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]
  12. Haqshenas G., Huang F. F., Fenaux M., Guenette D. K., Pierson F. W., Larsen C. T., Shivaprasad H. L., Toth T. E., Meng X. J. 2002; The putative capsid protein of the newly identified avian hepatitis E virus shares antigenic epitopes with that of swine and human hepatitis E viruses and chicken big liver and spleen disease virus. J Gen Virol 83:2201–2209
     [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 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
     [Google Scholar]
  15. Huang F. F., Haqshenas G., Shivaprasad H. L. 7 other authors 2002a; Heterogeneity and seroprevalence of the newly identified avian hepatitis E virus from chickens in the United States. J Clin Microbiol 40:4197–4202
     [Google Scholar]
  16. Huang F. F., Haqshenas G., Guenette D. K., Halbur P. G., Schommer S., Pierson F. W., Toth T. E., Meng X. J. 2002b; Detection by RT-PCR and genetic characterization of field isolates of swine hepatitis E virus from pigs in different geographic regions of the US. J Clin Microbiol 40:1326–1332
     [Google Scholar]
  17. Hussaini S. H., Skidmore S. J., Richardson P., Sherratt L. M., Cooper B. T., O'Grady J. G. 1997; Severe hepatitis E infection during pregnancy. J Viral Hepat 4:51–54
     [Google Scholar]
  18. 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]
  19. Kasorndorkbua C., Halbur P. G., 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
     [Google Scholar]
  20. McCrudden R., O'Connell S., Farrant T., Beaton S., Iredale J. P., Fine D. 2000; Sporadic acute hepatitis E in the United Kingdom: an underdiagnosed phenomenon?. Gut 46:732–733
     [Google Scholar]
  21. 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
     [Google Scholar]
  22. Meng X. J. 2000a; Zoonotic and xenozoonotic risks of hepatitis E virus. Infect Dis Rev 2:35–41
     [Google Scholar]
  23. 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
     [Google Scholar]
  24. Meng X. J. 2003; Swine hepatitis E virus: cross-species infection and risk in xenotransplantation. Curr Top Microbiol Immunol 278:185–216
     [Google Scholar]
  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
     [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. 1998; Genetic and experimental evidence for cross-species infection by the swine hepatitis E virus. J Virol 72:9714–9721
     [Google Scholar]
  27. 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 58:297–302
     [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 the 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
     [Google Scholar]
  29. Nishizawa T., Takahashi M., Mizuo H., Miyajima H., Gotanda Y., Okamoto H. 2003; Characterization of Japanese swine and human hepatitis E virus isolates of genotype IV with 99% identity over the entire genome. J Gen Virol 84:1245–1251
     [Google Scholar]
  30. 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
     [Google Scholar]
  31. Payne C. J., Ellis T. M., Plant S. L., Gregory A. R., Wilcox G. E. 1999; Sequence data suggests big liver and spleen disease virus (BLSV) is genetically related to hepatitis E virus. Vet Microbiol 68:119–125
     [Google Scholar]
  32. 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
     [Google Scholar]
  33. Purcell R. H. 1996; Hepatitis E virus. In Field Virology . , 3rd edn. vol 2 pp  2831–2843 Edited by Fields B. N., Knipe D. M., Howley P. M. Philadelphia: Lippincott–Raven;
  34. Reyes G. R. 1997; Overview of the epidemiology and biology of the hepatitis E virus. In Viral Hepatitis pp  239–258 Edited by Willson R. A. New York: Marcel Dekker;
     [Google Scholar]
  35. Riddell C. 1997 Hepatitis–splenomegaly syndrome. In Diseases of Poultry , p. 1041 Edited by Calnek B. W., Barnes H. J., Beard C. W., McDougald L. R., Saif Y. M. Ames, IA: Iowa State University Press;
     [Google Scholar]
  36. Ritchie S. J., Riddell C. 1991; “Hepatitis–splenomegaly” syndrome in commercial egg laying hens. Can Vet J 32:500–501
     [Google Scholar]
  37. 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]
  38. 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
     [Google Scholar]
  39. Shivaprasad H. L., Woolcock P. R. 1995; Necrohemorrhagic hepatitis in broiler breeders. In Proceedings of the 44th Western Poultry Diseases Conference 5–7 March, 1995 p– 6 Sacramento, CA, USA:
     [Google Scholar]
  40. Sun Z. F., Huang F. F., Halbur P. G., Schommer S. K., Pierson F. W., Toth T. E., Meng X. J. 2003; Use of heteroduplex mobility assays (HMA) for pre-sequencing screening and identification of variant strains of avian and swine hepatitis E viruses. Vet Microbiol 96:165–176
     [Google Scholar]
  41. 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
     [Google Scholar]
  42. Takahashi K., Kang J. H., Ohnishi S., Mishiro S. 2002; Genetic heterogeneity of hepatitis E virus recovered from Japanese patients with acute sporadic hepatitis. J Infect Dis 185:1342–1345
     [Google Scholar]
  43. Takahashi M., Nishizawa T., Miyajima H., Gotanda Y., Iita T., Tsuda F., Okamoto H. 2003a; 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
     [Google Scholar]
  44. Takahashi M., Nishizawa T., Okamoto H. 2003b; Identification of a genotype III swine hepatitis E virus that was isolated from a Japanese pig born in 1990 and that is most closely related to Japanese isolates of human hepatitis E virus. J Clin Microbiol 41:1342–1343
     [Google Scholar]
  45. Tei S., Kitajima N., Takahashi K., Mishiro S. 2003; Zoonotic transmission of hepatitis E virus from deer to human beings. Lancet 362:371–373
     [Google Scholar]
  46. 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]
  47. Tsarev S. A., Emerson S. U., Reyes G. R., Tsareva T. S., Legters L. J., Malik I. A., Iqbal M., Purcell R. H. 1992; Characterization of a prototype strain of hepatitis E virus. Proc Natl Acad Sci U S A 89:559–563
     [Google Scholar]
  48. Tsarev S. A., Tsareva T. S., Emerson S. U., Yarbough P. O., Legters L. J., Moskal T., Purcell R. H. 1994; Infectivity titration of a prototype strain of hepatitis E virus in cynomolgus monkeys. J Med Virol 43:135–142
     [Google Scholar]
  49. 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
     [Google Scholar]
  50. 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]
  51. 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]
  52. Wang Y. C., Zhang H. Y., Xia N. S. 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
     [Google Scholar]
  53. Williams T. P. E., Kasorndorkbua C., Halbur P. G., Haqshenas G., Guenette D. K., Toth T. E., Meng X. J. 2001; Evidence of extrahepatic sites of replication of the hepatitis E virus in a swine model. J Clin Microbiol 39:3040–3046
     [Google Scholar]
  54. Wu J. C., Chen C. M., Chiang T. Y., Tsai W. H., Jeng W. J., Sheen I. J., Lin 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
     [Google Scholar]
  55. 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
     [Google Scholar]
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Genetic identification of avian hepatitis E virus (HEV) from healthy chicken flocks and characterization of the capsid gene of 14 avian HEV isolates from chickens with hepatitis–splenomegaly syndrome in different geographical regions of the United States
J. Gen. Virol. 85, 693 (2004); https://doi.org/10.1099/vir.0.19582-0
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