Skip to main content

Advertisement

Log in

Molecular and serological survey of hepatitis E virus infection among domestic pigs in Inner Mongolia, China

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

To evaluate the prevalence and characteristics of swine hepatitis E virus (HEV) infection in Inner Mongolia, China, serum samples obtained from 356 2- to 4-month-old pigs on 14 farms in Inner Mongolia were tested for the presence of anti-HEV antibodies and HEV RNA. Overall, 186 pigs (52%) tested positive for anti-HEV antibodies, while 30 pigs (8%) had detectable HEV RNA levels. The 30 HEV isolates recovered from the viremic pigs were phylogenetically classified into genotype 4 and differed from each other by up to 15.3% in a 412 nt sequence within ORF2. The Inner Mongolian swine HEV strains were most similar to human or swine HEV strains isolated in the other provinces of China but differed by 15.9–18.9% from those in Mongolia (formerly known as Outer Mongolia). These results indicate that farm pigs in Inner Mongolia are frequently infected with markedly divergent genotype 4 HEV strains that may be indigenous to China.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Cooper K, Huang FF, Batista L, Rayo CD, Bezanilla JC, Toth TE, Meng XJ (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

    Article  CAS  PubMed  Google Scholar 

  2. Dalton HR, Bendall R, Ijaz S, Banks M (2008) Hepatitis E: an emerging infection in developed countries. Lancet Infect Dis 8:698–709

    Article  PubMed  Google Scholar 

  3. Emerson SU, Anderson D, Arankalle A, Meng XJ, Purdy M, Schlauder GG, Tsarev SA (2005) Hepevirus. In: Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (eds) Virus Taxonomy: the VIIIth report of the International Committee on Taxonomy of Viruses. Elsevier/Academic Press, London, pp 851–855

    Google Scholar 

  4. Emerson SU, Purcell RH (2003) Hepatitis E virus. Rev Med Virol 13:145–154

    Article  CAS  PubMed  Google Scholar 

  5. Geng Y, Wang C, Zhao C, Yu X, Harrison TJ, Tian K, Wang Y (2009) Serological prevalence of hepatitis E virus in domestic animals and diversity of genotype 4 hepatitis E virus in China. Vector Borne Zoonotic Dis (Epub ahead of print)

  6. Harrison TJ (1999) Hepatitis E virus—an update. Liver 19:171–176

    Article  CAS  PubMed  Google Scholar 

  7. Huang FF, Haqshenas G, Guenette DK, Halbur PG, Schommer SK, Pierson FW, Toth TE, Meng XJ (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

    Article  CAS  PubMed  Google Scholar 

  8. Ina Y (1994) ODEN: a program package for molecular evolutionary analysis and database of DNA and amino acid sequences. Comput Appl Biosci 10:11–12

    CAS  PubMed  Google Scholar 

  9. Inoue J, Takahashi M, Yazaki Y, Tsuda F, Okamoto H (2006) Development and validation of an improved RT-PCR assay with nested universal primers for detection of hepatitis E virus strains with significant sequence divergence. J Virol Methods 137:325–333

    Article  CAS  PubMed  Google Scholar 

  10. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  11. Kwok S, Higuchi R (1989) Avoiding false positives with PCR. Nature 339:237–238

    Article  CAS  PubMed  Google Scholar 

  12. Li K, Zhuang H, Zhu W (2002) Partial nucleotide sequencing of hepatitis E viruses detected in sera of patients with hepatitis E from 14 cities in China. Chin Med J (Engl) 115:1058–1063

    CAS  Google Scholar 

  13. Li RC, Ge SX, Li YP, Zheng YJ, Nong Y, Guo QS, Zhang J, Ng MH, Xia NS (2006) Seroprevalence of hepatitis E virus infection, rural southern People’s Republic of China. Emerg Infect Dis 12:1682–1688

    CAS  PubMed  Google Scholar 

  14. Li X, Zhao C, Harrison TJ, Song A, Fan J, Zhang J, Wang Y (2008) Investigation of hepatitis E virus infection in swine from Hunan province, China. J Med Virol 80:1391–1396

    Article  CAS  PubMed  Google Scholar 

  15. Li Z, Yu S, Dong S, Zhu Y, Si F, Shen S, Jiang Z, Yu R, Zou S (2009) Reduced prevalence of genotype 3 HEV in Shanghai pig farms and hypothetical homeostasis of porcine HEV reservoir. Vet Microbiol 137:184–189

    Article  PubMed  Google Scholar 

  16. Lorenzo FR, Tsatsralt-Od B, Ganbat S, Takahashi M, Okamoto H (2007) Analysis of the full-length genome of hepatitis E virus isolates obtained from farm pigs in Mongolia. J Med Virol 79:1128–1137

    Article  CAS  PubMed  Google Scholar 

  17. Lu J, Zhou Y, Lin X, Jiang Y, Tian R, Zhang Y, Wu J, Zhang F, Zhang Y, Wang Y, Bi S (2009) General epidemiological parameters of viral hepatitis A, B, C, E in six regions of China: a cross-sectional study in 2007. PLoS One 4:e8467

    Article  PubMed  Google Scholar 

  18. Lu L, Li C, Hagedorn CH (2006) Phylogenetic analysis of global hepatitis E virus sequences: genetic diversity, subtypes and zoonosis. Rev Med Virol 16:5–36

    Article  CAS  PubMed  Google Scholar 

  19. Meng XJ (2010) Hepatitis E virus: animal reservoirs and zoonotic risk. Vet Microbiol 140:256–265

    Article  CAS  PubMed  Google Scholar 

  20. Meng XJ, Purcell RH, Halbur PG, Lehman JR, Webb DM, Tsareva TS, Haynes JS, Thacker BJ, Emerson SU (1997) A novel virus in swine is closely related to the human hepatitis E virus. Proc Natl Acad Sci USA 94:9860–9865

    Article  CAS  PubMed  Google Scholar 

  21. Mizuo H, Suzuki K, Takikawa Y, Sugai Y, Tokita H, Akahane Y, Itoh K, Gotanda Y, Takahashi M, Nishizawa T, Okamoto H (2002) Polyphyletic strains of hepatitis E virus are responsible for sporadic cases of acute hepatitis in Japan. J Clin Microbiol 40:3209–3218

    Article  PubMed  Google Scholar 

  22. Ning H, Yu S, Zhu Y, Dong S, Yu R, Shen S, Niu Z, Li Z (2008) Genotype 3 hepatitis E has been widespread in pig farms of Shanghai suburbs. Vet Microbiol 126:257–263

    Article  PubMed  Google Scholar 

  23. Ning HQ, Niu ZX, Yu RS, Zhang PH, Dong SJ, Zh Li (2007) Identification of genotype 3 hepatitis E virus in fecal samples from a pig farm located in a Shanghai suburb. Vet Microbiol 121:125–130

    Article  CAS  PubMed  Google Scholar 

  24. 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

    Article  CAS  PubMed  Google Scholar 

  25. Okamoto H (2007) Genetic variability and evolution of hepatitis E virus. Virus Res 127:216–228

    Article  CAS  PubMed  Google Scholar 

  26. Okamoto H, Takahashi M, Nishizawa T (2003) Features of hepatitis E virus infection in Japan. Intern Med 42:1065–1071

    Article  CAS  PubMed  Google Scholar 

  27. Purcell RH, Emerson SU (2008) Hepatitis E: an emerging awareness of an old disease. J Hepatol 48:494–503

    Article  CAS  PubMed  Google Scholar 

  28. Reyes GR, Purdy MA, Kim JP, Luk K-C, Young LM, Fry KE, Bradley DW (1990) Isolation of a cDNA from the virus responsible for enterically transmitted non-A, non-B hepatitis. Science 247:1335–1339

    Article  CAS  PubMed  Google Scholar 

  29. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  30. Schlauder GG, Mushahwar IK (2001) Genetic heterogeneity of hepatitis E virus. J Med Virol 65:282–292

    Article  CAS  PubMed  Google Scholar 

  31. Shao ZJ, Li JH, Zheng YJ, Zhang JX, Ma YH, Ma WT, Jiang QW, Dang RL (2009) Epidemiological screening for hepatitis E virus in bile specimens from livestock in northwest China. J Clin Microbiol 47:814–816

    Article  PubMed  Google Scholar 

  32. Shrestha SM, Shrestha S, Tsuda F, Nishizawa T, Takahashi M, Gotanda Y, Okamoto H (2004) Genetic changes in hepatitis E virus of subtype 1a in patients with sporadic acute hepatitis E in Kathmandu, Nepal, from 1997 to 2002. J Gen Virol 85:97–104

    Article  CAS  PubMed  Google Scholar 

  33. Smith JL (2001) A review of hepatitis E virus. J Food Prot 64:572–586

    CAS  PubMed  Google Scholar 

  34. 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

    Article  CAS  PubMed  Google Scholar 

  35. Takahashi M, Nishizawa T, Tanaka T, Tsatsralt-Od B, Inoue J, Okamoto H (2005) Correlation between positivity for immunoglobulin A antibodies and viraemia of swine hepatitis E virus observed among farm pigs in Japan. J Gen Virol 86:1807–1813

    Article  CAS  PubMed  Google Scholar 

  36. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Bio Evol 24:1596–1599

    Article  CAS  Google Scholar 

  37. Tanaka H, Yoshino H, Kobayashi E, Takahashi M, Okamoto H (2004) Molecular investigation of hepatitis E virus infection in domestic and miniature pigs used for medical experiments. Xenotransplantation 11:503–510

    Article  PubMed  Google Scholar 

  38. Tei S, Kitajima N, Takahashi K, Mishiro S (2003) Zoonotic transmission of hepatitis E virus from deer to human beings. Lancet 362:371–373

    Article  PubMed  Google Scholar 

  39. Thompson JD, Higgins DG, Gibson TJ (1994) ClustalW. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  Google Scholar 

  40. Wang Y, Ling R, Erker JC, Zhang H, Li H, Desai S, Mushahwar IK, Harrison TJ (1999) A divergent genotype of hepatitis E virus in Chinese patients with acute hepatitis. J Gen Virol 80:169–177

    CAS  PubMed  Google Scholar 

  41. Wang Y, Zhang H, Ling R, Li H, Harrison TJ (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

    CAS  PubMed  Google Scholar 

  42. Wang YC, Zhang HY, Xia NS, Peng G, Lan HY, Zhuang H, Zhu YH, Li SW, Tian KG, Gu WJ, Lin JX, Wu X, Li HM, Harrison TJ (2002) Prevalence, isolation, and partial sequence analysis of hepatitis E virus from domestic animals in China. J Med Virol 67:516–521

    Article  CAS  PubMed  Google Scholar 

  43. Wibawa ID, Suryadarma IG, Mulyanto Tsuda F, Matsumoto Y, Ninomiya M, Takahashi M, Okamoto H (2007) Identification of genotype 4 hepatitis E virus strains from a patient with acute hepatitis E and farm pigs in Bali, Indonesia. J Med Virol 79:1138–1146

    Article  CAS  PubMed  Google Scholar 

  44. Worm HC, van der Poel WH, Brandstätter G (2002) Hepatitis E: an overview. Microbes Infect 4:657–666

    Article  CAS  PubMed  Google Scholar 

  45. Wu B, Nan L, Wang J, Guo S, Wang H, Jin G, Bai L, Ren L (1996) Seroprevalence of viral hepatitis in Inner Mongolia, China. Clin Diagn Virol 6:77–78

    Article  CAS  PubMed  Google Scholar 

  46. Wu JC, Chen CM, Chiang TY, Tsai WH, Jeng WJ, Sheen IJ, Lin CC, Meng XJ (2002) Spread of hepatitis E virus among different-aged pigs: two-year survey in Taiwan. J Med Virol 66:488–492

    Article  PubMed  Google Scholar 

  47. 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

    Article  CAS  PubMed  Google Scholar 

  48. Yu Y, Sun J, Liu M, Xia L, Zhao C, Harrison TJ, Wang Y (2009) Seroepidemiology and genetic characterization of hepatitis E virus in the northeast of China. Infect Genet Evol 9:554–561

    Article  CAS  PubMed  Google Scholar 

  49. Zhang W, Shen Q, Mou J, Gong G, Yang Z, Cui L, Zhu J, Ju G, Hua X (2008) Hepatitis E virus infection among domestic animals in eastern China. Zoonoses Public Health 55:291–298

    Article  CAS  PubMed  Google Scholar 

  50. Zhang W, Yang S, Ren L, Shen Q, Cui L, Fan K, Huang F, Kang Y, Shan T, Wei J, Xiu H, Lou Y, Liu J, Yang Z, Zhu J, Hua X (2009) Hepatitis E virus infection in central China reveals no evidence of cross-species transmission between human and swine in this area. PLoS One 4:e8156

    Article  PubMed  Google Scholar 

  51. Zhang W, Yang S, Shen Q, Huang F, Shan T, Yang Z, Cui L, Zhu J, Hua X (2010) Genotype 3 hepatitis E virus existed among swine groups in 4 geographically far regions in China. Vet Microbiol 140:193–195

    Article  CAS  PubMed  Google Scholar 

  52. Zheng Y, Ge S, Zhang J, Guo Q, Ng MH, Wang F, Xia N, Jiang Q (2006) Swine as a principal reservoir of hepatitis E virus that infects humans in eastern China. J Infect Dis 193:1643–1649

    Article  PubMed  Google Scholar 

  53. Zhu G, Qu Y, Jin N, Sun Z, Liu T, Lee H, Tian M, Wang T (2008) Seroepidemiology and molecular characterization of hepatitis E virus in Jilin, China. Infection 36:140–146

    Article  CAS  PubMed  Google Scholar 

  54. Zhuang H, Cao XY, Liu CB, Wang GM (1991) Enterically transamitted non-A, non-B, hepatitis in China. In: Shikata T, Purcell RH, Uchida T (eds) Viral Hepatitis C, D and E. Excerpta Medica, Amsterdam, pp 277–285

    Google Scholar 

Download references

Acknowledgments

This study was supported in part by a grant from the Ministry of Health, Labor and Welfare of Japan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hiroaki Okamoto.

Additional information

The nucleotide sequence data reported in this study have been assigned DDBJ/EMBL/GenBank accession numbers AB550613–AB550642 for 30 swine HEV sequences.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jinshan, Jirintai, Manglai, D. et al. Molecular and serological survey of hepatitis E virus infection among domestic pigs in Inner Mongolia, China. Arch Virol 155, 1217–1226 (2010). https://doi.org/10.1007/s00705-010-0706-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-010-0706-0

Keywords

Navigation