Abstract
Although rare in developed countries, most acquired human cases of hepatitis E virus (HEV) infection are associated with travel to developing countries where HEV is endemic. Increasingly, however, sporadic, non-travel-related HEV cases have been reported in developed countries. In Italy, only two studies to date have investigated the presence of HEV in wild boars. Here, we report a serological and virological survey of HEV in wild boar populations in northwestern Italy. During the hunting season, 594 serum and 320 liver samples were collected and screened for antibodies to HEV and HEV RNA. Overall, the seroprevalence was 4.9 %, and HEV RNA was detected in 12 liver samples (p = 3.7 %). No serum samples tested positive for HEV RNA. Phylogenetic analysis of the ORF2 region revealed that the isolates clustered within genotype 3, subtypes 3e and 3f, and were closely related to HEV strains previously detected in domestic pigs farmed in the same geographic area. Although the routes of viral transmission are still poorly understood, our data show that HEV genotypes 3e and 3f circulate in wild boars in northwestern Italy. Also, they provide evidence that autochthonous HEV infections in Italy could also be linked to wild boar populations, suggesting an increased risk for domestically acquired HEV infection in humans through wild animals. The HEV sequences determined in this study may be useful for comparing present and future human isolates to identify transmission events between wild boar, humans, and farmed pigs. Similarly to other more commonly known zoonotic agents, HEV should be included in national or regional disease surveillance programs for wild animals.
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Bouamra Y, Gérolami R, Arzouni J-P, Grimaud J-C, Lafforgue P, Nelli M, Tivoli N, Ferretti A, Motte A, Colson P (2014) Emergence of autochthonous infections with hepatitis E virus of genotype 4 in Europe. Intervirology 57:43–48
Cameron A, Garden I, Doherr MG, Wagner B (2003) Animal disease Surveillance and survey systems. Edited by Salman, 4:62
de Deus N, Peralta B, Pina S, Allepuz A, Mateu E, Vidal D, Ruiz-Fons F, Martın M, Gortazar C, Segales J (2007) Prevalence of Hepatitis E virus in European Wild boars. In: Proceedings of Second European Wildlife Disease Association Student Workshop April 26–29, pp 24–25
de Deus N, Seminati C, Mateu E, Martin M, Segales J (2007) Detection of hepatitis E virus in liver, mesenteric lymph node, serum, bile and faeces of naturally infected pigs affected by different pathological conditions. Vet Microbiol 119:105–114
de Deus N, Peralta B, Pina S, Allepuz A, Mateu E, Vidal D, Ruiz-Fons F, Martı´ M, Gortazar C, Segale´s J (2008) Epidemiological study of hepatitis E virus infection in European wild boars (Sus scrofa) in Spain. Vet Microbiol 129:163–170
Giordani MT, Fabris P, Brunetti E, Goblirsch S, Romanò L (2013) Hepatitis E and lymphocytic leukemia in man. Italy. Emerg Infect Dis 19:12
Halbur PG, Kasorndorkbua C, Gilbert C, Guenette D, Potters MB, Purcell RH, Emerson SU, Toth TE, Meng XJ (2001) Comparative pathogenesis of infection of pigs with hepatitis E viruses recovered from a pig and a human. J Clin Microbiol 39(3):918–923
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(4):1326–1332
Jothikumar N, Cromeans TL, Robertson BH, Meng XJ, Hill VR (2006) A broadly reactive one-step real-time RT-PCR assay for rapid and sensitive detection of hepatitis E virus. J Virol Methods 131:65–71
Kaba M, Davoust B, Marié J-L, Colson P (2010) Detection of hepatitis E virus in wild boar (Sus scrofa) livers. Vet J 186:259–261
Khudyakov Y, Kamili S (2011) Serological diagnostics of hepatitis E virus infection. Virus Res 161(1):84–92
Li T-C, Chijiwa K, Sera N, Ishibashi T, Etoh Y, Shinohara Y, Kurata Y, Ishida M, Sakamoto S, Takeda N, Miyamura T (2005) Hepatitis E virus transmission from wild boar meat. Emerg Infect Dis 11(12):1958–1960
Lu L, Li C, Hagedorn CH (2006) Phylogenetic analysis of global hepatitis E virus sequences: genetic diversity, subtypes and zoonosis. Rev Med Virol 16(1):5–36
Martelli F, Caprioli A, Zengarini M, Marata A, Fiegna C, Di Bartolo I, Ruggeri FM, Delogu M, Ostanello F (2008) Detection of hepatitis E virus (HEV) in a demographic managed wild boar (Sus scrofa) population in Italy. Vet Microbiol 126(1–3):74–81
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 Emerg Dis. doi:10.1111/tbed.12118
McCreary C, Martelli F, Grierson S, Otanello F, Nevel A, Banks M (2008) Excretion of hepatitis E virus by pigs of different ages and its presence in slurry stores in the United States. Vet Rec 163(9):261–265
Meng XJ, Lindsay DS, Sriranganathan N (2009) Wild boars as sources for infectious diseases in livestock and humans. Phil Trans R Soc B 364:2697. doi:10.1098/rstb.2009.0086
Michitaka K, Takahshi K, Furukawa S, Inoue G, Hiasa Y, Horiike N, Onji M, Abe N, Mishiro S (2007) Prevalence of hepatitis E virus among wild boar in the Ehime area of western Japan. Hepatology Research 37:214–220
Monne I, Ceglie L, DIMartino G, Natale A, Zamprogna S, Morreale A, Rampazzo E, Cattoli G, Bonfanti L (2013) Hepatitis E virus genotype 4 in a pig farm, Italy. Epidemiol Infect 15:1–5
Peletto S, Rosamilia A, Caruso C, Vitale N, Chiavacci L, Modesto P, Boin C, Acutis PL, Messana E, Gobbi E, Origlia S, Sona B, Masoero L (2013) Hepatitis E virus in pig farms from North Western Italy. WAVLD, Berlin, 5–8 June
Rutjes SA, Lodder-Verschoor F, Lodder WJ, VanVanGiessen J, Reesink H, Bouwknegt M, de Roda Husman AM (2010) Seroprevalence and molecular detection of hepatitis E virus in wild boar and red deer in The Netherlands. J Virol Methods 168:197–206
Saenz de Buruaga M, Lucio AJ, Purroy J (1991) Reconocimiento de sexo y edad en especies cinege´ticas. Vitoria, Diputacion Foral de Alava
Schlauder GG, Mushahwar IK (2001) Genetic heterogeneity of hepatitis E. J Med Virol 65(2):282–292
Seminati C, Mateu E, Peralta B, de Deus N, Martin M (2008) Distribution of hepatitis E virus infection and its prevalence in pigs on commercial farms in Spain. Vet J 175(1):130–132
Takahashi M, Nishizawa T, Sato H, Sato Y, Jirintai D, Nagashima S, Okamoto H (2011) Analysis of the full-length genome of a hepatitis E virus isolate obtained from a wild boar in Japan that is classifiable into a novel genotype. J Gen Virol 92:902–918
Tam AW, Smith MM, Guerra ME et al (1991) Hepatitis E virus (HEV): molecular cloning and sequencing of the full-length viral genome. Virology 185:120–131
Tamada Y, Yano K, Yatsuhashi H, Inoue O, Mawatari F, Ishibashi H (2003) Consumption of wild boar linked to cases of hepatitis E. J Hepatol 38:827–832
Van der Honing R, Van Coillie E, Antonis FGA, Van der Poel WHM (2011) First isolation of hepatitis E virus genotype 4 in Europe through swine surveillance in the Netherlands and Belgium. PLoS One 6(8):e22673. doi:10.1371/journal.pone.0022673
Acknowledgments
The authors are grateful to De Marco L., Gobbi E., and Messana E. for their technical assistance. We also would like to thank Boin C. for help with the phylogenetic analysis.
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None of the authors of this paper has a financial or personal relationship with other people or organisations that could inappropriately influence or bias the content of the paper.
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Caruso, C., Modesto, P., Bertolini, S. et al. Serological and virological survey of hepatitis E virus in wild boar populations in northwestern Italy: detection of HEV subtypes 3e and 3f. Arch Virol 160, 153–160 (2015). https://doi.org/10.1007/s00705-014-2246-5
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DOI: https://doi.org/10.1007/s00705-014-2246-5