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Molecular Investigation on the Presence of Hepatitis E Virus (HEV) in Wild Game in North-Western Italy

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Abstract

Meat products from HEV-infected reservoir animal species are capable of transmitting HEV to humans and represent a public health concern. Human HEV cases have been linked to the consumption of raw or undercooked pig liver sausages, pork, and game meats, such as wild boars and deer worldwide. Direct exposure to swine or wild game species might also represent a source of HEV transmission especially for veterinarians, hunters, or butchers. A limited amount of data is available on HEV prevalence in wild boars in Italy and no data are available for other wild game species intended for human consumption. In this study, the circulation of HEV in four different animal species hunted in north-western Italy was evaluated to gain insight into the infection levels and the genetic diversity of the virus in such animal populations. Liver samples of 372 wild boars, 30 roe deer, 47 European hares and 38 coypus were analyzed for HEV RNA by real-time RT-PCR; positive samples were then sequenced and submitted to phylogenetic analysis. HEV RNA was detected in the livers of 7/372 (1.9 %) wild boars tested, while no sample was positive for roe deer, European hare, and coypu. Phylogenetic analysis showed that wild boar HEV sequences belonged to HEV subtypes 3e, 3c, and 3f. Our results indicate that HEV is circulating only in wild boar among the considered game species in north-western Italy and suggest a potential zoonotic risk related to handling and/or consumption of raw or undercooked meat and products made of the liver from this species.

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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), 270–278.

    Article  PubMed  Google Scholar 

  • Andraud, H., & Guérin, J. L. (2013). Détection et estimation de la prevalence du virus de l’hépatite E chez le sanglier, le cerf élaphe et le rangondin dans la Région Midi-Pyrénées. PhD thesis, University, Toulose

  • Batts, W., Yun, S., Hedrick, R., & Winton, J. (2011). A novel member of the family Hepeviridae from cutthroat trout (Oncorhynchus clarkii). Virus Research, 158(1–2), 116–123.

    Article  CAS  PubMed  Google Scholar 

  • Berto, A., Grierson, S., Hakze-van der Honing, R., Martelli, F., Johne, R., Reetz, J., et al. (2013). Hepatitis E virus in pork liver sausage, France. Emerging Infectious Diseases, 19(2), 264–266.

    Article  PubMed Central  PubMed  Google Scholar 

  • Bollo, E., Pregel, P., Gennero, S., Pizzoni, E., Rosati, S., Nebbia, P., & Biolatti, B. (2003). Health status of a population of nutria (Myocastor coypus) living in a protected area in Italy. Research in Veterinary Science, 75(1), 21–25.

    Article  CAS  PubMed  Google Scholar 

  • Bouquet, J., Tessé, S., Lunazzi, A., Eloit, M., Rose, N., Nicand, E., & Pavio, N. (2011). Close similarity between sequences of hepatitis E virus recovered from humans and swine, France, 2008-2009. Emerging Infectious Diseases, 17, 2018–2025.

    Article  PubMed Central  PubMed  Google Scholar 

  • Carpentier, A., Chaussade, H., Rigaud, E., Rodriguez, J., Berthault, C., Boué, 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.

    Article  PubMed Central  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 in Virology, 160(1), 153–160.

    Article  CAS  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. The Journal of Infectious Diseases, 202(6), 825–834.

    Article  PubMed  Google Scholar 

  • Cossaboom, C. M., Cordoba, L., Dryman, B. A., & Meng, X. J. (2011). Hepatitis E virus in rabbits, Virginia, USA. Emerging Infectious Diseases, 17(11), 2047–2049.

    Article  PubMed Central  PubMed  Google Scholar 

  • de Deus, N., Casas, M., Peralta, B., Nofrarías, M., Pina, S., Martín, M., & Segalés, J. (2008a). Hepatitis E virus infection dynamics and organic distribution in naturally infected pigs in a farrow-to-finish farm. Veterinary Microbiology, 132(1–2), 19–28.

    Article  PubMed  Google Scholar 

  • de Deus, N., Peralta, B., Pina, S., Allepuz, A., Mateu, E., Vidal, D., et al. (2008b). Epidemiological study of hepatitis E virus infection in European wild boars (Sus scrofa) in Spain. Veterinary Microbiology, 129(1–2), 163–170.

    Article  PubMed  Google Scholar 

  • Di Bartolo, I., Angeloni, G., Ponterio, E., Ostanello, F., & Ruggeri, F. M. (2015). Detection of hepatitis E virus in pork liver sausages. International Journal of Food Microbiology, 193, 29–33.

    Article  PubMed  Google Scholar 

  • Di Bartolo, I., Ponterio, E., Castellini, L., Ostanello, F., & Ruggeri, F. M. (2011). Viral and antibody HEV prevalence in swine at slaughterhouse in Italy. Veterinary Microbiology, 149(3), 330–338.

    Article  PubMed  Google Scholar 

  • Drexler, J. F., Seelen, A., Corman, V. M., Fumie Tateno, A., Cottontail, V., Melim Zerbinati, R., et al. (2012). Bats worldwide carry hepatitis E virus related viruses that form a putative novel genus within the family Hepeviridae. Journal of Virology, 86(17), 9134–9147.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Forgách, P., Nowotny, N., Erdélyi, K., Boncz, A., Zentai, J., Szucs, G., et al. (2010). Detection of hepatitis E virus in samples of animal origin collected in Hungary. Veterinary Microbiology, 143(2), 106–116.

    Article  PubMed  Google Scholar 

  • Głogowski, R., Czauderna, M., Rozbicka, A., Krajewska, K. A., & Clauss, M. (2010). Fatty acid profile of hind leg muscle in female and male nutria (Myocastor coypus Mol.), fed green forage diet. Meat Science, 85(3), 577–579.

    Article  PubMed  Google Scholar 

  • He, J., Innis, B. L., Shrestha, M. P., Clayson, E. T., Scott, R. M., Linthicum, K. J., et al. (2012). Evidence that rodents are a reservoir of hepatitis E virus for humans in Nepal. Journal of Clinical Microbiology, 40(12), 4493–4498.

    Article  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 Central  PubMed  Google Scholar 

  • Izopet, J., Dubois, M., Bertagnoli, S., Lhomme, S., Marchandeau, S., Boucher, S., et al. (2012). Hepatitis E virus strains in rabbits and evidence of a closely related strain in humans, France. Emerging Infectious Diseases, 18(8), 1274–1281.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jirintai, S., Jinshan, Tanggis, Manglai, D., Mulyanto, Takahashi, M., et al. (2012). Molecular analysis of hepatitis E virus from farm rabbits in Inner Mongolia, China and its successful propagation in A549 and PLC/PRF/5 cells. Virus Research, 170(1-2), 126–137.

    Article  CAS  PubMed  Google Scholar 

  • Johne, R., Plenge-Bönig, A., Hess, M., Ulrich, R. G., Reetz, J., & Schielke, A. (2010). Detection of a novel hepatitis E-like virus in faeces of wild rats using a nested broad-spectrum RT-PCR. Journal of General Virology, 91(3), 750–758.

    Article  CAS  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.

    Article  CAS  PubMed  Google Scholar 

  • Kaba, M., Davoust, B., Marié, J. L., & Colson, P. (2010). Detection of hepatitis E virus in wild boar (Sus scrofa) livers. Veterinary Journal, 186(2), 259–261.

    Article  Google Scholar 

  • Kukielka, D., Rodriguez-Prieto, V., Vicente, J., & Sánchez-Vizcaíno, J. M. (2015). Constant hepatitis E virus (HEV) circulation in wild boar and red deer in Spain: An increasing concern source of HEV zoonotic transmission. Transboundary and Emerging Diseases. doi:10.1111/tbed.12311.

    Google Scholar 

  • Lack, J. B., Volk, K., & Van Den Bussche, R. A. (2012). Hepatitis E virus genotype 3 in wild rats, United States. Emerging Infectious Diseases, 18(8), 1268–1273.

    Article  PubMed Central  PubMed  Google Scholar 

  • Larska, M., Krzysiak, M. K., Jabłoński, A., Kęsik, J., Bednarski, M., & Rola, J. (2014). Hepatitis E virus antibody prevalence in wildlife in Poland. Zoonoses and Public Health, 62(2), 105–110.

    Article  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. Emerging Infectious Diseases, 11(12), 1958–1960.

    Article  PubMed Central  PubMed  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.

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • Martelli, F., Caprioli, A., Zengarini, M., Marata, A., Fiegna, C., Di Bartolo, I., et al. (2008). Detection of hepatitis E virus (HEV) in a demographic managed wild boar (Sus scrofa scrofa) population in Italy. Veterinary Microbiology, 126(1–3), 74–81.

    Article  CAS  PubMed  Google Scholar 

  • Martinelli, N., Pavoni, E., Filogari, D., Ferrari, N., Chiari, M., Canelli, E., & Lombardi, G. (2013). Hepatitis E virus in wild boar in the central northern part of Italy. Transboundary and Emerging Diseases. doi:10.1111/tbed.12118.

    PubMed  Google Scholar 

  • Matsuda, H., Okada, K., Takahashi, K., & Mishiro, S. (2003). Severe hepatitis E virus infection after ingestion of uncooked liver from a wild boar. Journal of Infectious Diseases, 188(6), 944.

    Article  PubMed  Google Scholar 

  • Meng, X. J. (2010). Hepatitis E virus: Animal reservoirs and zoonotic risk. Veterinary Microbiology, 140(3–4), 256–265.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Meng, X. J., Lindsay, D. S., & Sriranganathan, N. (2009). Wild boars as sources for infectious diseases in livestock and humans. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 364(1530), 2697–2707.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mesquita, J. R., Oliveira, R. M., Coelho, C., Vieira-Pinto, M., & Nascimento, M. S. (2014). Hepatitis E virus in sylvatic and captive wild boar from Portugal. Transboundary and Emerging Diseases. doi:10.1111/tbed.12297.

    PubMed  Google Scholar 

  • Michel, V., Ruvoen-Clouet, N., Menard, A., Sonrier, C., Fillonneau, C., Rakotovao, F., et al. (2001). Role of the coypu (Myocastor coypus) in the epidemiology of leptospirosis in domestic animals and humans in France. European Journal of Epidemiology, 17(2), 111–121.

    Article  CAS  PubMed  Google Scholar 

  • Nardoni, S., Angelici, C. M., Mugnaini, L., & Mancianti, F. (2011). Prevalence of Toxoplasma gondii infection in Myocastor coypus in a protected Italian wetland. Parasites & Vectors, 4, 240.

    Article  Google Scholar 

  • Nidaira, M., Takahashi, K., Ogura, G., Taira, K., Okano, S., Kudaka, J., et al. (2012). Detection and phylogenetic analysis of hepatitis E viruses from mongooses in Okinawa, Japan. Journal of Veterinary Medical Science, 74(12), 1665–1668.

    Article  PubMed  Google Scholar 

  • Paulsen, P., Smulders, F., & Hilbert, F. (2012). Salmonella in meat from hunted game: A Central European perspective. Food Research International, 45(2), 609–616.

    Article  Google Scholar 

  • Prigioni, C., Balestrieri, A., & Remonti, L. (2005). Food habits of the coypu, Myocastor coypus, and its impact on aquatic vegetation in a freshwater habitat of NW Italy. Folia Zoologica, 54(3), 269–277.

    Google Scholar 

  • Purcell, R. H., & Emerson, S. U. (2010). Hidden danger: The raw facts about hepatitis E virus. Journal of Infectious Diseases, 202(6), 819–821.

    Article  PubMed Central  PubMed  Google Scholar 

  • Raj, V. S., Smits, S. L., Pas, S. D., Provacia, L. B., Moorman-Roest, H., Osterhaus, A. D., & Haagmans, B. L. (2012). Novel hepatitis E virus in ferrets, the Netherlands. Emerging Infectious Diseases, 18(8), 1369–1370.

    Article  PubMed Central  PubMed  Google Scholar 

  • Renou, C., Afonso, A. M., & Pavio, N. (2014). Foodborne transmission of hepatitis E virus from raw pork liver sausage, France. Emerging Infectious Diseases, 20(11), 1945–1947.

    Article  PubMed Central  PubMed  Google Scholar 

  • Reuter, G., Fodor, D., Forgách, P., Kátai, 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., & de Roda Husman, A. M. (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.

    Article  CAS  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.

    Article  PubMed Central  PubMed  Google Scholar 

  • Schlosser, J., Eiden, M., Vina-Rodriguez, A., Fast, C., Dremsek, P., Lange, E., et al. (2014). Natural and experimental hepatitis E virus genotype 3-infection in European wild boar is transmissible to domestic pigs. Veterinary Research, 45, 121.

    Article  PubMed Central  PubMed  Google Scholar 

  • Schulp, C. J. E., Thuiller, W., & Verburg, P. H. (2014). Wild food in Europe: A synthesis of knowledge and data of terrestrial wild food as an ecosystem service. Ecological Economics, 105, 292–305.

    Article  Google Scholar 

  • Takahashi, K., Kitajima, N., Abe, N., & Mishiro, S. (2004). Complete or near-complete nucleotide sequences of hepatitis E virus genome recovered from a wild boar, a deer, and four patients who ate the deer. Virology, 330(2), 501–505.

    Article  CAS  PubMed  Google Scholar 

  • Tei, S., Kitajima, N., Takahashi, K., & Mishiro, S. (2003). Zoonotic transmission of hepatitis E from deer to human beings. Lancet, 362(9381), 371–373.

    Article  PubMed  Google Scholar 

  • Van der Poel, W. H. (2014). Food and environmental routes of Hepatitis E virus transmission. Current Opinion in Virology, 4, 91–96.

    Article  PubMed  Google Scholar 

  • Withers, M. R., Correa, M. T., Morrow, M., Stebbins, M. E., Seriwatana, J., Webster, W. D., et al. (2002). Antibody levels to hepatitis E virus in North Carolina swine workers, nonswine workers, swine, and murids. The American Journal of Tropical Medicine and Hygiene, 66(4), 384–388.

    PubMed  Google Scholar 

  • Zhao, C., Ma, Z., Harrison, T. J., Feng, R., Zhang, C., Qiao, Z., et al. (2009). A novel genotype of hepatitis E virus prevalent among farmed rabbits in China. Journal of Medical Virology, 81(8), 1371–1379.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgment

This work has been supported by a Grant of the Italian Ministry of Health (IZS PLV 20/11 RC).

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The authors declare that they have no conflict of interest.

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Correspondence to Laura Serracca.

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Serracca, L., Battistini, R., Rossini, I. et al. Molecular Investigation on the Presence of Hepatitis E Virus (HEV) in Wild Game in North-Western Italy. Food Environ Virol 7, 206–212 (2015). https://doi.org/10.1007/s12560-015-9201-9

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