Skip to main content

Advertisement

SpringerLink
Log in

Detection and Phylogenetic Analysis of the Hepatitis E Virus in a Canadian Swine Production Network

  • Original Paper
  • Published:
Food and Environmental Virology Aims and scope Submit manuscript

Abstract

Viral contamination along the production chain is a significant concern in both food safety and livestock health. Pigs have been reported to act as a reservoir for zoonotic viruses, sometimes emerging ones, and epidemiological studies have shown direct links between the consumption of uncooked pork offal and cases of hepatitis caused by the hepatitis E virus (HEV) genotype 3 in humans. The presence of HEV in swine herds has been reported, but its dissemination in pork production environments is still unknown. To investigate viral contamination sources in the swine industry, 452 environment and fecal samples, including samples from livestock transportation vehicles, were collected over a period of 11 months from ten farms and one slaughterhouse that together represent a single production network. Hepatitis E virus RNA was detected by nested RT-PCR in 32 samples from both inside and outside farm buildings, on trucks, and, mostly, from fomites collected in the slaughterhouse yard, such as on a utility vehicle. Phylogenetic analysis showed a wide diversity of HEV genotype 3 strains, similar to human and swine strains previously found. According to the results of this study, the movements of trucks and utility vehicles might play an important role in HEV dissemination on a slaughterhouse site and throughout an entire network.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Banks, M., Heath, G. S., Grierson, S. S., King, D. P., Gresham, A., Girones, R., et al. (2004). Evidence for the presence of hepatitis E virus in pigs in the United Kingdom. Veterinary Record, 154(8), 223–227.

    Article  CAS  PubMed  Google Scholar 

  • Brassard, J., Gagne, M. J., Genereux, M., & Cote, C. (2012). Detection of human food-borne and zoonotic viruses on irrigated, field-grown strawberries. [Research Support, Non-US Govt]. Applied and Environment Microbiology, 78(10), 3763–3766. doi:10.1128/AEM.00251-12.

    Article  CAS  Google Scholar 

  • Cook, N., & van der Poel, W. H. (2015). Survival and elimination of hepatitis E virus: A review. Food Environ Virol,. doi:10.1007/s12560-015-9196-2.

    Google Scholar 

  • Cooper, K., Huang, F. F., Batista, L., Rayo, C. D., Bezanilla, J. C., Toth, T. E., et al. (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. Journal of Clinical Microbiology, 43(4), 1684–1688.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Di Bartolo, I., Diez-Valcarce, M., Vasickova, P., Kralik, P., Hernandez, M., Angeloni, G., et al. (2012). Hepatitis E virus in pork production chain in Czech Republic, Italy, and Spain, 2010. Emerging Infectious Diseases, 18(8), 1282–1289. doi:10.3201/eid1808.111783.

    Article  PubMed  PubMed Central  Google Scholar 

  • Di Bartolo, I., Martelli, F., Inglese, N., Pourshaban, M., Caprioli, A., Ostanello, F., et al. (2008). Widespread diffusion of genotype 3 hepatitis E virus among farming swine in Northern Italy. Veterinary Microbiology, 132(1–2), 47–55. doi:10.1016/j.vetmic.2008.04.028.

    Article  PubMed  Google Scholar 

  • dos Santos, D. R., de Paula, V. S., de Oliveira, J. M., Marchevsky, R. S., & Pinto, M. A. (2011). Hepatitis E virus in swine and effluent samples from slaughterhouses in Brazil. Veterinary Microbiology, 149(1–2), 236–241. doi:10.1016/j.vetmic.2010.10.024.

    Article  PubMed  Google Scholar 

  • Garkavenko, O., Obriadina, A., Meng, J., Anderson, D. A., Benard, H. J., Schroeder, B. A., et al. (2001). Detection and characterisation of swine hepatitis E virus in New Zealand. Journal of Medical Virology, 65(3), 525–529.

    Article  CAS  PubMed  Google Scholar 

  • Goens, S. D., & Perdue, M. L. (2004). Hepatitis E viruses in humans and animals. Animal Health Research Reviews, 5(2), 145–156.

    Article  PubMed  Google Scholar 

  • Halac, U., Beland, K., Lapierre, P., Patey, N., Ward, P., Brassard, J., et al. (2012a). Chronic hepatitis E infection in children with liver transplantation. Gut, 61(4), 597–603. doi:10.1136/gutjnl-2011-300708.

    Article  CAS  PubMed  Google Scholar 

  • Halac, U., Beland, K., Lapierre, P., Patey, N., Ward, P., Brassard, J., et al. (2012b). Cirrhosis due to chronic hepatitis E infection in a child post-bone marrow transplant. The Journal of Pediatrics, 160(5), 871–874. doi:10.1016/j.jpeds.2012.01.028.

    Article  PubMed  Google Scholar 

  • Huang, F. F., Haqshenas, G., Guenette, D. K., Halbur, P. G., Schommer, S. K., Pierson, F. W., et al. (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. Journal of Clinical Microbiology, 40(4), 1326–1332.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. Journal of Viral Hepatitis, 4(1), 51–54.

    Article  CAS  PubMed  Google Scholar 

  • Koot, H., Hogema, B. M., Koot, M., Molier, M., & Zaaijer, H. L. (2015). Frequent hepatitis E in the Netherlands without traveling or immunosuppression. [Research Support, Non-US Govt]. Journal of Clinical Virology, 62, 38–40. doi:10.1016/j.jcv.2014.11.020.

    Article  CAS  PubMed  Google Scholar 

  • Kumar, A., Beniwal, M., Kar, P., Sharma, J. B., & Murthy, N. S. (2004). Hepatitis E in pregnancy. International Journal of Gynaecology and Obstetrics, 85(3), 240–244. doi:10.1016/j.ijgo.2003.11.018.

    Article  CAS  PubMed  Google Scholar 

  • Leblanc, D., Poitras, E., Gagne, M. J., Ward, P., & Houde, A. (2010). Hepatitis E virus load in swine organs and tissues at slaughterhouse determined by real-time RT-PCR. International Journal of Food Microbiology, 139(3), 206–209. doi:10.1016/j.ijfoodmicro.2010.02.016.

    Article  CAS  PubMed  Google Scholar 

  • Leblanc, D., Ward, P., Gagne, M. J., Poitras, E., Muller, P., Trottier, Y. L., et al. (2007). Presence of hepatitis E virus in a naturally infected swine herd from nursery to slaughter. International Journal of Food Microbiology, 117(2), 160–166. doi:10.1016/j.ijfoodmicro.2007.03.008.

    Article  CAS  PubMed  Google Scholar 

  • Li, T. C., Chijiwa, K., Sera, N., Ishibashi, T., Etoh, Y., Shinohara, Y., et al. (2005). Hepatitis E virus transmission from wild boar meat. [Case Reports Research Support, Non-US Govt]. Emerging Infectious Diseases, 11(12), 1958–1960. doi:10.3201/eid1112.051041.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lu, L., Li, C., & Hagedorn, C. H. (2006). Phylogenetic analysis of global hepatitis E virus sequences: genetic diversity, subtypes and zoonosis. Reviews in Medical Virology, 16(1), 5–36. doi:10.1002/rmv.482.

    Article  CAS  PubMed  Google Scholar 

  • Meng, X. J. (2010). Recent advances in Hepatitis E virus. Journal of Viral Hepatitis, 17(3), 153–161. doi:10.1111/j.1365-2893.2009.01257.x.

    Article  CAS  PubMed  Google Scholar 

  • Meng, X. J. (2011). From barnyard to food table: the omnipresence of hepatitis E virus and risk for zoonotic infection and food safety. Virus Research, 161(1), 23–30. doi:10.1016/j.virusres.2011.01.016.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meng, X. J., Purcell, R. H., Halbur, P. G., Lehman, J. R., Webb, D. M., Tsareva, T. S., et al. (1997). A novel virus in swine is closely related to the human hepatitis E virus. Proceedings of the National Academy of Sciences USA, 94(18), 9860–9865.

    Article  CAS  Google Scholar 

  • Meng, X. J., Wiseman, B., Elvinger, F., Guenette, D. K., Toth, T. E., Engle, R. E., et al. (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. Journal of Clinical Microbiology, 40(1), 117–122.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyashita, K., Kang, J. H., Saga, A., Takahashi, K., Shimamura, T., Yasumoto, A., et al. (2012). Three cases of acute or fulminant hepatitis E caused by ingestion of pork meat and entrails in Hokkaido, Japan: Zoonotic food-borne transmission of hepatitis E virus and public health concerns. Hepatology Research, 42(9), 870–878. doi:10.1111/j.1872-034X.2012.01006.x.

    Article  CAS  PubMed  Google Scholar 

  • Panda, S. K., Thakral, D., & Rehman, S. (2007). Hepatitis E virus. Reviews in Medical Virology, 17(3), 151–180. doi:10.1002/rmv.522.

    Article  CAS  PubMed  Google Scholar 

  • Perez-Gracia, M. T., Suay, B., & Mateos-Lindemann, M. L. (2014). Hepatitis E: An emerging disease. Infection, Genetics and Evolution, 22, 40–59. doi:10.1016/j.meegid.2014.01.002.

    Article  PubMed  Google Scholar 

  • Perez-Gracia, M. T., Suay-Garcia, B., Garcia, M., & Mateos-Lindemann, M. L. (2016). Hepatitis E: Latest developments in knowledge. Future Microbiology, 11, 789–808. doi:10.2217/fmb-2016-0012.

    Article  CAS  PubMed  Google Scholar 

  • Rutjes, S. A., Lodder, W. J., Bouwknegt, M., & de Roda Husman, A. M. (2007). Increased hepatitis E virus prevalence on Dutch pig farms from 33 to 55% by using appropriate internal quality controls for RT-PCR. Journal of Virological Methods, 143(1), 112–116. doi:10.1016/j.jviromet.2007.01.030.

    Article  CAS  PubMed  Google Scholar 

  • Saint-Jacques, P., Tissot-Dupont, H., Colson, P., & Colson, P. (2016). Autochthonous infection with hepatitis E virus related to subtype 3a, France: A case report. Annals of Hepatology, 15(3), 438–441. doi:10.5604/16652681.1198823.

    Article  PubMed  Google Scholar 

  • Slot, E., Hogema, B. M., Riezebos-Brilman, A., Kok, T. M., Molier, M., & Zaaijer, H. L. (2013). Silent hepatitis E virus infection in Dutch blood donors, 2011–2012. Euro Surveillance, 18(31). http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20550.

  • Smith, D. B., Simmonds, P., International Committee on Taxonomy of Viruses Hepeviridae Study Group, Jameel, S., Emerson, S. U., & Harrison, T. J. (2014). Consensus proposals for classification of the family Hepeviridae. Journal of General Virology, 95(Pt 10), 2223–2232. doi:10.1099/vir.0.068429-0.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sonoda, H., Abe, M., Sugimoto, T., Sato, Y., Bando, M., Fukui, E., et al. (2004). Prevalence of hepatitis E virus (HEV) infection in wild boars and deer and genetic identification of a genotype 3 HEV from a boar in Japan. Journal of Clinical Microbiology, 42(11), 5371–5374. doi:10.1128/JCM.42.11.5371-5374.2004.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular evolutionary genetics analysis version 6.0. [Research Support, N.I.H., Extramural Research Support, Non-US Govt]. Molecular Biology and Evolution, 30(12), 2725–2729. doi:10.1093/molbev/mst197.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tei, S., Kitajima, N., Takahashi, K., & Mishiro, S. (2003). Zoonotic transmission of hepatitis E virus from deer to human beings. Lancet, 362(9381), 371–373. doi:10.1016/S0140-6736(03)14025-1.

    Article  PubMed  Google Scholar 

  • Ward, P., Muller, P., Letellier, A., Quessy, S., Simard, C., Trottier, Y. L., et al. (2008). Molecular characterization of hepatitis E virus detected in swine farms in the province of Quebec. Canadian Journal of Veterinary Research, 72(1), 27–31.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wilhelm, B., Leblanc, D., Houde, A., Brassard, J., Gagne, M. J., Plante, D., et al. (2014). Survey of Canadian retail pork chops and pork livers for detection of hepatitis E virus, norovirus, and rotavirus using real time RT-PCR. International Journal of Food Microbiology, 185, 33–40. doi:10.1016/j.ijfoodmicro.2014.05.006.

    Article  CAS  PubMed  Google Scholar 

  • Williams, T. P., Kasorndorkbua, C., Halbur, P. G., Haqshenas, G., Guenette, D. K., Toth, T. E., et al. (2001). Evidence of extrahepatic sites of replication of the hepatitis E virus in a swine model. Journal of Clinical Microbiology, 39(9), 3040–3046.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan, Y., Zhang, W., Shen, Q., Cui, L., & Hua, X. (2008). Prevalence of four different subgenotypes of genotype 4 hepatitis E virus among swine in the Shanghai area of China. Acta Veterinaria Scandinavica, 50, 12. doi:10.1186/1751-0147-50-12.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yazaki, Y., Mizuo, H., Takahashi, M., Nishizawa, T., Sasaki, N., Gotanda, Y., et al. (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. Journal of General Virology, 84(Pt 9), 2351–2357.

    Article  CAS  PubMed  Google Scholar 

  • Yoo, D., Willson, P., Pei, Y., Hayes, M. A., Deckert, A., Dewey, C. E., et al. (2001). Prevalence of hepatitis E virus antibodies in Canadian swine herds and identification of a novel variant of swine hepatitis E virus. Clinical and Diagnostic Laboratory Immunology, 8(6), 1213–1219. doi:10.1128/CDLI.8.6.1213-1219.2001.

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors would like to thank the Canadian Swine Research and Development Cluster for its financial support (Project 1002) as well as the producers who participated in this project. This work was also financially supported by the Research Branch of Agriculture and Agri-Food Canada (RBPI 1485).

Author information

Authors and Affiliations

  1. NSERC Industrial Research Chair in Meat Safety, Faculty of Veterinary Medicine, University of Montréal, 3200 Rue Sicotte, Saint-Hyacinthe, QC, J2S 2M2, Canada

    Nicolas Nantel-Fortier, Ann Letellier, Virginie Lachapelle, Philippe Fravalo & Yvan L’Homme

  2. Saint-Hyacinthe Research and Development Center, Agriculture and Agri-Food Canada, 3600 Casavant Boulevard West, Saint-Hyacinthe, QC, J2S 8E3, Canada

    Julie Brassard

Authors
  1. Nicolas Nantel-Fortier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ann Letellier
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Virginie Lachapelle
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Philippe Fravalo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yvan L’Homme
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Julie Brassard
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Julie Brassard.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nantel-Fortier, N., Letellier, A., Lachapelle, V. et al. Detection and Phylogenetic Analysis of the Hepatitis E Virus in a Canadian Swine Production Network. Food Environ Virol 8, 296–304 (2016). https://doi.org/10.1007/s12560-016-9252-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12560-016-9252-6

Keywords

Search

Navigation