Skip to main content

Hepatitis E Virus in Domestic Pigs, Wild Boars, Pig Farm Workers, and Hunters in Estonia

Abstract

While hepatitis E is a growing health concern in Europe, epidemiological data on hepatitis E virus (HEV) in Estonia are scarce. Along with imported HEV infections, autochthonous cases are reported from European countries. Both domestic and wild animals can be a source of human cases of this zoonosis. Here, we investigated the presence of anti-HEV antibodies and HEV RNA in domestic pigs and wild boars, as well as in pig farm workers and hunters in Estonia. Anti-HEV antibodies were detected in 234/380 (61.6 %) of sera from domestic pigs and in all investigated herds, and in 81/471 (17.2 %) of meat juice samples from wild boars. HEV RNA was detected by real-time PCR in 103/449 (22.9 %) of fecal samples from younger domestic pigs and 13/81 (16.0 %) of anti-HEV-positive wild boar samples. Analysis of sera from 67 pig farm workers and 144 hunters revealed the presence of HEV-specific IgG in 13.4 and 4.2 % of the samples, respectively. No HEV RNA was detected in the human serum samples. Phylogenetic analyses of HEV sequences from domestic pigs and wild boars, based on a 245 bp fragment from the open reading frame 2 showed that all of them belonged to genotype 3. The present study demonstrates the presence of HEV in Estonian domestic pig and wild boar populations, as well as in humans who have direct regular contact with these animals. Our results suggest that HEV infections are present in Estonia and require attention.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  • Adlhoch, C., Wolf, A., Meisel, H., Kaiser, M., Ellerbrok, H., & Pauli, G. (2009). High HEV presence in four different wild boar populations in East and West Germany. Veterinary Microbiology, 139(3–4), 270–278.

    Article  PubMed  Google Scholar 

  • Balayan, M. S. (1993). Hepatitis E virus infection in Europe: Regional situation regarding laboratory diagnosis and epidemiology. Clinical and Diagnostic Virology, 1(1), 1–9.

    CAS  Article  PubMed  Google Scholar 

  • Baylis, S. A., Blumel, J., Mizusawa, S., Matsubayashi, K., Sakata, H., Okada, Y., et al. (2013). World Health Organization International Standard to harmonize assays for detection of hepatitis E virus RNA. Emerging Infectious Diseases, 19(5), 729–735.

    PubMed Central  Article  PubMed  Google Scholar 

  • Carpentier, A., Chaussade, H., Rigaud, E., Rodriguez, J., Berthault, C., Boue, F., et al. (2012). High hepatitis E virus seroprevalence in forestry workers and in wild boars in France. Journal of Clinical Microbiology, 50(9), 2888–2893.

    PubMed Central  Article  PubMed  Google Scholar 

  • Caruso, C., Modesto, P., Bertolini, S., Peletto, S., Acutis, P. L., Dondo, A., et al. (2015). Serological and virological survey of hepatitis E virus in wild boar populations in northwestern Italy: Detection of HEV subtypes 3e and 3f. Archives of Virology, 160(1), 153–160.

    CAS  Article  PubMed  Google Scholar 

  • Casas, M., Pina, S., Peralta, B., Mateu, E., Casal, J., & Martin, M. (2010). Comparison of muscle fluid and serum for detection of antibodies against hepatitis E virus in slaughter pigs. The Veterinary Journal, 190(1), 179–180.

    Article  PubMed  Google Scholar 

  • Chaussade, H., Rigaud, E., Allix, A., Carpentier, A., Touze, A., Delzescaux, D., et al. (2013). Hepatitis E virus seroprevalence and risk factors for individuals in working contact with animals. Journal of Clinical Virology, 58(3), 504–508.

    Article  PubMed  Google Scholar 

  • Colson, P., Borentain, P., Queyriaux, B., Kaba, M., Moal, V., Gallian, P., et al. (2010). Pig liver sausage as a source of hepatitis E virus transmission to humans. Journal of Infectious Diseases, 202(6), 825–834.

    Article  PubMed  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.

    PubMed Central  Article  PubMed  Google Scholar 

  • Dremsek, P., Joel, S., Baechlein, C., Pavio, N., Schielke, A., Ziller, M., et al. (2013). Hepatitis E virus seroprevalence of domestic pigs in Germany determined by a novel in-house and two reference ELISAs. Journal of Virological Methods, 190(1–2), 11–16.

    CAS  Article  PubMed  Google Scholar 

  • Dremsek, P., Wenzel, J. J., Johne, R., Ziller, M., Hofmann, J., Groschup, M. H., et al. (2011). Seroprevalence study in forestry workers from eastern Germany using novel genotype 3- and rat hepatitis E virus-specific immunoglobulin G ELISAs. Medical Microbiology and Immunology, 201(2), 189–200.

    Article  PubMed  Google Scholar 

  • Drobeniuc, J., Favorov, M. O., Shapiro, C. N., Bell, B. P., Mast, E. E., Dadu, A., et al. (2001). Hepatitis E virus antibody prevalence among persons who work with swine. Journal of Infectious Diseases, 184(12), 1594–1597.

    CAS  Article  PubMed  Google Scholar 

  • Drobeniuc, J., Greene-Montfort, T., Le, N. T., Mixson-Hayden, T. R., Ganova-Raeva, L., Dong, C., et al. (2013). Laboratory-based surveillance for hepatitis E virus infection, United States, 2005-2012. Emerging Infectious Diseases, 19(2), 218–222.

    PubMed Central  Article  PubMed  Google Scholar 

  • Fernandez-Barredo, S., Galiana, C., Garcia, A., Vega, S., Gomez, M. T., & Perez-Gracia, M. T. (2006). Detection of hepatitis E virus shedding in feces of pigs at different stages of production using reverse transcription-polymerase chain reaction. Journal of Veterinary Diagnostic Investigation, 18(5), 462–465.

    Article  PubMed  Google Scholar 

  • Galiana, C., Fernandez-Barredo, S., Garcia, A., Gomez, M. T., & Perez-Gracia, M. T. (2008). Occupational exposure to hepatitis E virus (HEV) in swine workers. American Journal of Tropical Medicine and Hygeine, 78(6), 1012–1015.

    Google Scholar 

  • Gerolami, R., Moal, V., & Colson, P. (2008). Chronic hepatitis E with cirrhosis in a kidney-transplant recipient. New England Journal of Medicine, 358(8), 859–860.

    CAS  Article  PubMed  Google Scholar 

  • Jothikumar, N., Cromeans, T. L., Robertson, B. H., Meng, X. J., & Hill, V. R. (2006). A broadly reactive one-step real-time RT-PCR assay for rapid and sensitive detection of hepatitis E virus. Journal of Virological Methods, 131(1), 65–71.

    CAS  Article  PubMed  Google Scholar 

  • Kamar, N., Bendall, R., Legrand-Abravanel, F., Xia, N. S., Ijaz, S., Izopet, J., et al. (2012). Hepatitis E. Lancet, 379(9835), 2477–2488.

    Article  PubMed  Google Scholar 

  • Khuroo, M. S., Kamili, S., & Jameel, S. (1995). Vertical transmission of hepatitis E virus. Lancet, 345(8956), 1025–1026.

    CAS  Article  PubMed  Google Scholar 

  • Krumbholz, A., Mohn, U., Lange, J., Motz, M., Wenzel, J. J., Jilg, W., et al. (2011). Prevalence of hepatitis E virus-specific antibodies in humans with occupational exposure to pigs. Medical Microbiology and Immunology, 201(2), 239–244.

    Article  PubMed  Google Scholar 

  • Lara, J., Purdy, M. A., & Khudyakov, Y. E. (2014). Genetic host specificity of hepatitis E virus. Infection, Genetics and Evolution, 24, 127–139.

    CAS  Article  PubMed  Google Scholar 

  • Larska, M., Krzysiak, M. K., Jablonski, A., Kesik, J., Bednarski, M., & Rola, J. (2015). Hepatitis E virus antibody prevalence in wildlife in Poland. Zoonoses and Public Health, 62(2), 105–110.

    CAS  Article  PubMed  Google Scholar 

  • Mansuy, J. M., Bendall, R., Legrand-Abravanel, F., Saune, K., Miedouge, M., Ellis, V., et al. (2011). Hepatitis E virus antibodies in blood donors, France. Emerging Infectious Diseases, 17(12), 2309–2312.

    PubMed Central  Article  PubMed  Google Scholar 

  • Martinelli, N., Pavoni, E., Filogari, D., Ferrari, N., Chiari, M., Canelli, E., et al. (2015). Hepatitis E Virus in Wild Boar in the Central Northern Part of Italy. Transboundary and Emerging Diseases, 62(2), 217–222.

    CAS  Article  PubMed  Google Scholar 

  • Masuda, J., Yano, K., Tamada, Y., Takii, Y., Ito, M., Omagari, K., et al. (2005). Acute hepatitis E of a man who consumed wild boar meat prior to the onset of illness in Nagasaki, Japan. Hepatology Research, 31(3), 178–183.

    Article  PubMed  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 of the United States of America, 94(18), 9860–9865.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Nakano, T., Takahashi, K., Arai, M., Okano, H., Kato, H., Ayada, M., et al. (2013). Identification of European-type hepatitis E virus subtype 3e isolates in Japanese wild boars: Molecular tracing of HEV from swine to wild boars. Infection, Genetics and Evolution, 18, 287–298.

    Article  PubMed  Google Scholar 

  • Norder, H., Sundqvist, L., Magnusson, L., Ostergaard Breum, S., Lofdahl, M., Larsen, L. E., et al. (2009). Endemic hepatitis E in two Nordic countries. Eurosurveillance Weekly, 14(19), 20–28.

    Google Scholar 

  • Oliveira-Filho, E. F., Bank-Wolf, B. R., Thiel, H. J., & Konig, M. (2014). Phylogenetic analysis of hepatitis E virus in domestic swine and wild boar in Germany. Veterinary Microbiology, 174(1–2), 233–238.

    Article  PubMed  Google Scholar 

  • Olsen, B., Axelsson-Olsson, D., Thelin, A., & Weiland, O. (2006). Unexpected high prevalence of IgG-antibodies to hepatitis E virus in Swedish pig farmers and controls. Scandinavian Journal of Infectious Diseases, 38(1), 55–58.

    Article  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.

    Article  PubMed  Google Scholar 

  • Prükk, T., Proshkina, S., & Pihlak, R. (2013). Äge E-viirushepatiit. Haigusjuhu kirjeldus. Eesti Arstist, 92(10), 587–589.

    Google Scholar 

  • Reuter, G., Fodor, D., Forgach, P., Katai, A., & Szucs, G. (2009). Characterization and zoonotic potential of endemic hepatitis E virus (HEV) strains in humans and animals in Hungary. Journal of Clinical Virology, 44(4), 277–281.

    Article  PubMed  Google Scholar 

  • Rutjes, S. A., Lodder-Verschoor, F., Lodder, W. J., van der Giessen, J., Reesink, H., Bouwknegt, M., et al. (2010). Seroprevalence and molecular detection of hepatitis E virus in wild boar and red deer in The Netherlands. Journal of Virological Methods, 168(1–2), 197–206.

    CAS  Article  PubMed  Google Scholar 

  • Schielke, A., Sachs, K., Lierz, M., Appel, B., Jansen, A., & Johne, R. (2009). Detection of hepatitis E virus in wild boars of rural and urban regions in Germany and whole genome characterization of an endemic strain. Virology Journal, 6, 58.

    PubMed Central  Article  PubMed  Google Scholar 

  • Tam, A. W., Smith, M. M., Guerra, M. E., Huang, C. C., Bradley, D. W., Fry, K. E., et al. (1991). Hepatitis E virus (HEV): Molecular cloning and sequencing of the full-length viral genome. Virology, 185(1), 120–131.

    CAS  Article  PubMed  Google Scholar 

  • Tamura, K., & Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10(3), 512–526.

    CAS  PubMed  Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30(12), 2725–2729.

    PubMed Central  CAS  Article  PubMed  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.

    Article  PubMed  Google Scholar 

  • Thiry, D., Mauroy, A., Saegerman, C., Thomas, I., Wautier, M., Miry, C., et al. (2014). Estimation of hepatitis E virus (HEV) pig seroprevalence using ELISA and Western blot and comparison between human and pig HEV sequences in Belgium. Veterinary Microbiology, 172(3–4), 407–414.

    CAS  Article  PubMed  Google Scholar 

  • Vasickova, P., Psikal, I., Widen, F., Smitalova, R., Bendova, J., Pavlik, I., et al. (2009). Detection and genetic characterisation of Hepatitis E virus in Czech pig production herds. Research in Veterinary Science, 87(1), 143–148.

    CAS  Article  PubMed  Google Scholar 

  • Vasickova, P., Slany, M., Chalupa, P., Holub, M., Svoboda, R., & Pavlik, I. (2011). Detection and phylogenetic characterization of human hepatitis E virus strains, Czech Republic. Emerging Infectious Diseases, 17(5), 917–919.

    PubMed Central  Article  PubMed  Google Scholar 

  • Velström, K., Lassen, B., & Jokelainen, P. (2013). Toxoplasma gondii antibody prevalence in Estonian wild boars. In Tropical medicine and international health: 8th European Congress on tropical medicine and international health & 5th conference of the Scandinavian-Baltic Society for parasitology, Copenhagen, Denmark (pp. 226–226), 10–13 September 2013, Wiley-Blackwell.

  • Vulcano, A., Angelucci, M., Candelori, E., Martini, V., Patti, A. M., Mancini, C., et al. (2007). HEV prevalence in the general population and among workers at zoonotic risk in Latium Region. Annali di Igiene, Medicina preventiva e di comunità, 19(3), 181–186.

    CAS  PubMed  Google Scholar 

  • Wacheck, S., Werres, C., Mohn, U., Dorn, S., Soutschek, E., Fredriksson-Ahomaa, M., et al. (2012). Detection of IgM and IgG against hepatitis E virus in serum and meat juice samples from pigs at slaughter in Bavaria, Germany. Foodborne Pathogens and Disease, 9(7), 655–660.

    CAS  Article  PubMed  Google Scholar 

  • Wang, Y., Ling, R., Erker, J. C., Zhang, H., Li, H., Desai, S., et al. (1999). A divergent genotype of hepatitis E virus in Chinese patients with acute hepatitis. Journal of General Virology, 80(Pt 1), 169–177.

    CAS  Article  PubMed  Google Scholar 

  • Wichmann, O., Schimanski, S., Koch, J., Kohler, M., Rothe, C., Plentz, A., et al. (2008). Phylogenetic and case-control study on hepatitis E virus infection in Germany. Journal of Infectious Diseases, 198(12), 1732–1741.

    Article  PubMed  Google Scholar 

  • Widen, F., Sundqvist, L., Matyi-Toth, A., Metreveli, G., Belak, S., Hallgren, G., et al. (2010). Molecular epidemiology of hepatitis E virus in humans, pigs and wild boars in Sweden. Epidemiology and Infection, 139(3), 361–371.

    Article  PubMed  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.

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Sofia Sidorova, senior laboratory specialist, for technical assistance as well as Elina Shatova and Jana Muravjova for analyzing pig sera and wild boar meat juice as a part of their Bachelor theses, Nurses Anu Kuusmann, Marge Reiss for taking blood samples. The farm workers and hunters are warmly thanked for their contributions and interest in this study. The study was financially supported by the European Regional Development Fund (Estonian Research Council (http://www.etag.ee/), programme TerVe, Projects ZoonRisk 3.2.1002.11-0002, 3.2.1002.11-0002 EKZE_SS and by Ministry of Education and Research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anna Ivanova.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests.

Human rights and animals and informed consent

All procedures of this work were approved by Tallinn Medical Research Committee, No. 2921. The pig sera used in this study were collected for a regular survey on porcine pathogens performed at the Estonian University of Life Sciences. The fecal samples from pigs were collected from the pen floors with no physical contact with the animals. Serosanguineous meat juice samples were primarily collected for a study of Toxoplasma gondii in Estonian wild boars (Velström et al. 2013). Approval from the Research Ethics Committee of the University of Tartu (No. 216/T-15) as well as written informed consents was obtained from volunteer pig farm workers and hunters for the use of serum samples.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ivanova, A., Tefanova, V., Reshetnjak, I. et al. Hepatitis E Virus in Domestic Pigs, Wild Boars, Pig Farm Workers, and Hunters in Estonia. Food Environ Virol 7, 403–412 (2015). https://doi.org/10.1007/s12560-015-9210-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12560-015-9210-8

Keywords

  • Zoonosis
  • Hepatitis E virus
  • RNA
  • Seroprevalence