Hepatitis E Virus (HEV): Identification of Subtypes 3b and 3m in Wild Boar Population in Liguria Region, Italy
Abstract
:1. Introduction
2. Results
3. Discussion
4. Materials and Methods
4.1. Sampling
4.2. Viral Recovery and RNA Extraction
4.3. TaqMan Real-Time RT-PCR
4.4. Sequencing and Phylogenetic Analysis
4.5. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Kamar, N.; Izopet, J.; Pavio, N.; Aggarwal, R.; Labrique, A.; Wedemeyer, H.; Dalton, H.R. Hepatitis E virus infection. Nat. Rev. Dis. Prim. 2017, 16, 17086. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Purdy, M.A.; Drexler, J.F.; Meng, X.-J.; Norder, H.; Okamoto, H.; Van der Poel, W.H.M.; Reuter, G.; de Souza, W.M.; Ulrich, R.G.; Smith, D.B. ICTV Virus Taxonomy Profile: Hepeviridae 2022. J. Gen. Virol. 2022, 103, 001778. [Google Scholar] [CrossRef] [PubMed]
- LeDesma, R.; Nimgaonkar, I.; Ploss, A. Hepatitis E Virus Replication. Viruses 2019, 11, 719. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Denner, J. Hepatitis E virus (HEV)—The Future. Viruses 2019, 11, 251. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Di Cola, G.; Fantilli, A.C.; Pisano, M.B.; Ré, V.E. Foodborne transmission of hepatitis A and hepatitis E viruses: A literature review. Int. J. Food Microbiol. 2021, 338, 108986. [Google Scholar] [CrossRef] [PubMed]
- Treagus, S.; Wright, C.; Baker-Austin, C.; Longdon, B.; Lowther, J. The Foodborne Transmission of Hepatitis E Virus to Humans. Food Environ. Virol. 2021, 13, 127–145. [Google Scholar] [CrossRef] [PubMed]
- Aspinall, E.J.; Couturier, E.; Faber, M.; Said, B.; Ijaz, S.; Tavoschi, L.; Takkinen, J.; Adlhoch, C.; On Behalf of The Country Experts. Hepatitis E virus infection in Europe: Surveillance and descriptive epidemiology of confirmed cases, 2005 to 2015. Eurosurveillance 2017, 22, 30561. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Harrison, L.; DiCaprio, E. Hepatitis E Virus: An Emerging Foodborne Pathogen. Front. Sustain. Food Syst. 2018, 2, 14. [Google Scholar] [CrossRef]
- EFSA Panel on Biological Hazards (BIOHAZ); Ricci, A.; Allende, A.; Bolton, D.; Chemaly, M.; Davies, R.; Fernandez Escamez, P.S.; Herman, L.; Koutsoumanis, K.; Lindqvist, R.; et al. Public health risks associated with hepatitis E virus (HEV) as a food-borne pathogen. EFSA J. 2017, 15, e04886. [Google Scholar] [CrossRef]
- Bollettino SEIEVA. Epidemiologia Delle Epatiti Virali Acute in Italia. 2021, Number 10. Available online: https://www.epicentro.iss.it/epatite/bollettino/Bollettino-n-10-marzo-2022.pdf (accessed on 15 September 2022).
- Tosti, M.E.; Ferrigno, L.; Mele, A.; Romanò, L.; Fiacchini, D.; Bagnarelli, P.; Zotti, C.; Chironna, M.; Prato, R.; Giordani, M.T.; et al. Epidemiologia e sorveglianza dell’epatite E in Italia: Dati dalla sorveglianza SEIEVA 2007-2019. Epidemiol. Prev. 2021, 45, 46–53. [Google Scholar] [CrossRef] [PubMed]
- Garbuglia, A.; Bruni, R.; Villano, U.; Vairo, F.; Lapa, D.; Madonna, E.; Picchi, G.; Binda, B.; Mariani, R.; De Paulis, F.; et al. Hepatitis E Outbreak in the Central Part of Italy Sustained by Multiple HEV Genotype 3 Strains, June–December 2019. Viruses 2021, 13, 1159. [Google Scholar] [CrossRef]
- Izopet, J.; Tremeaux, P.; Marion, O.; Migueres, M.; Capelli, N.; Chapuy-Regaud, S.; Mansuy, J.-M.; Abravanel, F.; Kamar, N.; Lhomme, S. Hepatitis E virus infections in Europe. J. Clin. Virol. 2019, 120, 20–26. [Google Scholar] [CrossRef]
- Pierini, I.; Di Bartolo, I.; Manuali, E.; Pirani, S.; Bazzucchi, M.; Moscati, L.; De Mia, G.M.; Giammarioli, M. Hepatitis E virus (HEV) genotype 3 diversity: Identification of a novel HEV subtype in wild boar in Central Italy. Transbound. Emerg. Dis. 2021, 68, 2121–2129. [Google Scholar] [CrossRef] [PubMed]
- Ferri, G.; Piccinini, A.; Olivastri, A.; Vergara, A. Hepatitis E virus detection in hunted wild boar (Sus scrofa) livers in Central Italy. Ital. J. Food Saf. 2022, 21, 9979. [Google Scholar] [CrossRef] [PubMed]
- Forzan, M.; Pacini, M.; Periccioli, M.; Mazzei, M. Hepatitis E Virus RNA Presence in Wild Boar Carcasses at Slaughterhouses in Italy. Animals 2021, 11, 1624. [Google Scholar] [CrossRef]
- Aprea, G.; Amoroso, M.G.; Di Bartolo, I.; D’Alessio, N.; Di Sabatino, D.; Boni, A.; Cioffi, B.; D’Angelantonio, D.; Scattolini, S.; De Sabato, L.; et al. Molecular detection and phylogenetic analysis of hepatitis E virus strains circulating in wild boars in south-Central Italy. Transbound. Emerg. Dis. 2018, 65, e25–e31. [Google Scholar] [CrossRef] [PubMed]
- Di Pasquale, S.; De Santis, P.; La Rosa, G.; Di Domenico, K.; Iaconelli, M.; Micarelli, G.; Martini, E.; Bilei, S.; De Medici, D.; Suffredini, E. Quantification and genetic diversity of Hepatitis E virus in wild boar (Sus scrofa) hunted for domestic consumption in Central Italy. Food Microbiol. 2019, 82, 194–201. [Google Scholar] [CrossRef] [PubMed]
- Bonardi, S.; Filipello, V.; Pavoni, E.; Carta, V.; Bolzoni, L.; Corradi, M.; Gilioli, S.; Losio, M.N. Geographical restriction of Hepatitis E virus circulation in wild boars (Sus scrofa) in Emilia-Romagna region, Northern Italy. Ital. J. Food Saf. 2020, 9, 8463. [Google Scholar] [CrossRef] [Green Version]
- De Sabato, L.; Ostanello, F.; De Grossi, L.; Marcario, A.; Franzetti, B.; Monini, M.; Di Bartolo, I. Molecular survey of HEV infection in wild boar population in Italy. Transbound. Emerg. Dis. 2018, 65, 1749–1756. [Google Scholar] [CrossRef]
- Lorusso, P.; Bonerba, E.; Pandiscia, A.; Mottola, A.; Di Pinto, A.; Piredda, R.; Terio, V. Occurrence of hepatitis E virus (HEV) in Calabrian wild boars. Int. J. Food Microbiol. 2022, 371, 109671. [Google Scholar] [CrossRef] [PubMed]
- Schlosser, J.; Eiden, M.; Vina-Rodriguez, A.; Fast, C.; Dremsek, P.; Lange, E.; Ulrich, R.G.; Groschup, M.H. Natural and experimental hepatitis E virus genotype 3—Infection in European wild boar is transmissible to domestic pigs. Vet. Res. 2014, 45, 121. [Google Scholar] [CrossRef] [PubMed]
- Schlosser, J.; Vina-Rodriguez, A.; Fast, C.; Groschup, M.H.; Eiden, M. Chronically infected wild boar can transmit genotype 3 hepatitis E virus to domestic pigs. Vet. Microbiol. 2015, 180, 15–21. [Google Scholar] [CrossRef]
- Capai, L.; Maestrini, O.; Casabianca, F.; Villechenaud, N.; Masse, S.; Bosseur, F.; De Lamballerie, X.; Charrel, R.N.; Falchi, A. Drastic decline of hepatitis E virus detection in domestic pigs after the age of 6 months, Corsica, France. Transbound. Emerg. Dis. 2019, 66, 2462–2473. [Google Scholar] [CrossRef] [PubMed]
- Jori, F.; Laval, M.; Maestrini, O.; Casabianca, F.; Charrier, F.; Pavio, N. Assessment of Domestic Pigs, Wild Boars and Feral Hybrid Pigs as Reservoirs of Hepatitis E Virus in Corsica, France. Viruses 2016, 8, 236. [Google Scholar] [CrossRef] [Green Version]
- Lopez-Lopez, P.; Risalde, M.D.L.A.; Frias, M.; García-Bocanegra, I.; Brieva, T.; Caballero-Gomez, J.; Camacho, A.; Fernández-Molera, V.; Machuca, I.; Gomez-Villamandos, J.C.; et al. Risk factors associated with hepatitis E virus in pigs from different production systems. Vet. Microbiol. 2018, 224, 88–92. [Google Scholar] [CrossRef] [PubMed]
- Fredriksson-Ahomaa, M.; London, L.; Skrzypczak, T.; Kantala, T.; Laamanen, I.; Biström, M.; Maunula, L.; Gadd, T. Foodborne Zoonoses Common in Hunted Wild Boars. EcoHealth 2020, 17, 512–522. [Google Scholar] [CrossRef] [PubMed]
- Montagnaro, S.; De Martinis, C.; Sasso, S.; Ciarcia, R.; Damiano, S.; Auletta, L.; Iovane, V.; Zottola, T.; Pagnini, U. Viral and Antibody Prevalence of Hepatitis E in European Wild Boars (Sus scrofa) and Hunters at Zoonotic Risk in the Latium Region. J. Comp. Pathol. 2015, 153, 1–8. [Google Scholar] [CrossRef]
- Capai, L.; Masse, S.; Gallian, P.; Souty, C.; Isnard, C.; Blanchon, T.; Peres, B.; de Lamballerie, X.; Charrel, R.; Falchi, A. Seroprevalence Study of Anti-HEV IgG among Different Adult Populations in Corsica, France, 2019. Microorganisms 2019, 7, 460. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Teixeira, J.; Mesquita, J.R.; Pereira, S.S.; Oliveira, R.M.S.; Abreu-Silva, J.; Rodrigues, A.; Myrmel, M.; Stene-Johansen, K.; Øverbø, J.; Gonçalves, G.; et al. Prevalence of hepatitis E virus antibodies in workers occupationally exposed to swine in Portugal. Med. Microbiol. Immunol. 2017, 206, 77–81. [Google Scholar] [CrossRef] [PubMed]
- Schielke, A.; Ibrahim, V.; Czogiel, I.; Faber, M.; Schrader, C.; Dremsek, P.; Ulrich, R.G.; Johne, R. Hepatitis E virus antibody prevalence in hunters from a district in Central Germany, 2013: A cross-sectional study providing evidence for the benefit of protective gloves during disembowelling of wild boars. BMC Infect. Dis. 2015, 15, 440. [Google Scholar] [CrossRef] [PubMed]
- Massei, G.; Kindberg, J.; Licoppe, A.; Gačić, D.; Šprem, N.; Kamler, J.; Baubet, E.; Hohmann, U.; Monaco, A.; Ozoliņš, J.; et al. Wild boar populations up, numbers of hunters down? A review of trends and implications for Europe. Pest Manag. Sci. 2015, 71, 492–500. [Google Scholar] [CrossRef] [PubMed]
- Trogu, T.; Ferrari, N.; Formenti, N.; Filipello, V.; Pedrotti, L.; Viganò, R.; Lanfranchi, P.; Luzzago, C. Low Serologic Prevalences Suggest Sporadic Infections of Hepatitis E Virus in Chamois (Rupicapra rupicapra) and Red Deer (Cervus elaphus) in the Italian Alps. J. Wildl. Dis. 2020, 56, 443. [Google Scholar] [CrossRef]
- Mazzei, M.F.M.; Forzan, M.; Pizzurro, F.; Picciolli, F.; Bandecchi, P.; Poli, A. Detection of Hepatitis E Virus Antibodies in Domestic and Wild Animal Species in Central Italy. Clin. Microbiol. Open Access 2015, 4, 227. [Google Scholar] [CrossRef] [Green Version]
- Sarchese, V.; Fruci, P.; Palombieri, A.; Di Profio, F.; Robetto, S.; Ercolini, C.; Orusa, R.; Marsilio, F.; Martella, V.; Di Martino, B. Molecular Identification and Characterization of a Genotype 3 Hepatitis E Virus (HEV) Strain Detected in a Wolf Faecal Sample, Italy. Animals 2021, 11, 3465. [Google Scholar] [CrossRef] [PubMed]
- De Sabato, L.; Ianiro, G.; Monini, M.; De Lucia, A.; Ostanello, F.; Di Bartolo, I. Detection of hepatitis E virus RNA in rats caught in pig farms from Northern Italy. Zoonoses Public Health 2020, 67, 62–69. [Google Scholar] [CrossRef] [PubMed]
- Palombieri, A.; Robetto, S.; Di Profio, F.; Sarchese, V.; Fruci, P.; Bona, M.C.; Ru, G.; Orusa, R.; Marsilio, F.; Martella, V.; et al. Surveillance Study of Hepatitis E Virus (HEV) in Domestic and Wild Ruminants in Northwestern Italy. Animals 2020, 10, 2351. [Google Scholar] [CrossRef] [PubMed]
- Nicot, F.; Dimeglio, C.; Migueres, M.; Jeanne, N.; Latour, J.; Abravanel, F.; Ranger, N.; Harter, A.; Dubois, M.; Lameiras, S.; et al. Classification of the Zoonotic Hepatitis E Virus Genotype 3 Into Distinct Subgenotypes. Front. Microbiol. 2021, 11, 634430. [Google Scholar] [CrossRef]
- Smith, D.B.; Izopet, J.; Nicot, F.; Simmonds, P.; Jameel, S.; Meng, X.-J.; Norder, H.; Okamoto, H.; Van Der Poel, W.H.; Reuter, G.; et al. Update: Proposed reference sequences for subtypes of hepatitis E virus (species Orthohepevirus A). J. Gen. Virol. 2020, 101, 692–698. [Google Scholar] [CrossRef] [PubMed]
- Masotti, C.; Battistini, R.; Mignone, W.; Berio, E.; Dellepiane, M.; Andreoli, T.; Razzuoli, E.; Peletto, S.; Beltramo, C.; Acutis, P.; et al. Hepatitis E virus research in wild boars during 2017/2018 and 2018/2019 hunting season. Large Anim. Rev. 2020, 26, 149–151. [Google Scholar]
- Fanelli, A.; Tizzani, P.; Buonavoglia, D. A systematic review and meta-analysis of hepatitis E virus (HEV) in wild boars. Res. Vet. Sci. 2021, 142, 54–69. [Google Scholar] [CrossRef] [PubMed]
- Fredriksson-Ahomaa, M. Wild Boar: A Reservoir of Foodborne Zoonoses. Foodborne Pathog. Dis. 2019, 16, 153–165. [Google Scholar] [CrossRef]
- Serracca, L.; Battistini, R.; Rossini, I.; Mignone, W.; Peletto, S.; Boin, C.; Pistone, G.; Ercolini, R.; Ercolini, C. Molecular Investigation on the Presence of Hepatitis E Virus (HEV) in Wild Game in North-Western Italy. Food Environ. Virol. 2015, 7, 206–212. [Google Scholar] [CrossRef] [PubMed]
- Vina-Rodriguez, A.; Schlosser, J.; Becher, D.; Kaden, V.; Groschup, M.H.; Eiden, M. Hepatitis E Virus Genotype 3 Diversity: Phylogenetic Analysis and Presence of Subtype 3b in Wild Boar in Europe. Viruses 2015, 7, 2704–2726. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Milojević, L.; Velebit, B.; Teodorović, V.; Kirbiš, A.; Petrović, T.; Karabasil, N.; Dimitrijević, M. Screening and Molecular Characterization of Hepatitis E Virus in Slaughter Pigs in Serbia. Food Environ. Virol. 2019, 11, 410–419. [Google Scholar] [CrossRef] [PubMed]
- Lainšček, P.R.; Toplak, I.; Kirbiš, A. A comprehensive study of hepatitis E virus infection in pigs entering a slaughterhouse in Slovenia. Vet. Microbiol. 2017, 212, 52–58. [Google Scholar] [CrossRef]
- Muñoz-Chimeno, M.; Forero, J.; Echevarría, J.; Muñoz-Bellido, J.; Vázquez-López, L.; Morago, L.; García-Galera, M.; Avellón, A. Full coding hepatitis E virus genotype 3 genome amplification method. J. Virol. Methods 2016, 230, 18–23. [Google Scholar] [CrossRef]
- Caballero-Gómez, J.; Jiménez-Ruiz, S.; Lopez-Lopez, P.; Vicente, J.; Risalde, M.A.; Cano-Terriza, D.; Frias, M.; Barasona, J.A.; Rivero, A.; García-Bocanegra, I.; et al. Emergent subtype of hepatitis E virus genotype 3 in wild boar in Spain. Transbound. Emerg. Dis. 2019, 66, 1803–1808. [Google Scholar] [CrossRef]
- Wang, H.; Contreras, R.C.; Saguti, F.; López-Olvera, J.R.; Karlsson, M.; Mentaberre, G.; Lindh, M.; Serra-Cobo, J.; Norder, H. Genetically similar hepatitis E virus strains infect both humans and wild boars in the Barcelona area, Spain, and Sweden. Transbound. Emerg. Dis. 2019, 66, 978–985. [Google Scholar] [CrossRef]
- De Sabato, L.; Di Bartolo, I.; Lapa, D.; Capobianchi, M.R.; Garbuglia, A.R. Molecular Characterization of HEV Genotype 3 in Italy at Human/Animal Interface. Front. Microbiol. 2020, 11, 137. [Google Scholar] [CrossRef] [Green Version]
- Reuter, G.; Fodor, D.; Forgách, P.; Kátai, A.; Szűcs, G. Characterization and zoonotic potential of endemic hepatitis E virus (HEV) strains in humans and animals in Hungary. J. Clin. Virol. 2009, 44, 277–281. [Google Scholar] [CrossRef]
- Jemeršić, L.; Prpić, J.; Brnić, D.; Keros, T.; Pandak, N.; Rode, O. Genetic diversity of hepatitis E virus (HEV) strains derived from humans, swine and wild boars in Croatia from 2010 to 2017. BMC Infect. Dis. 2019, 19, 269. [Google Scholar] [CrossRef] [PubMed]
- Suin, V.; Klamer, S.E.; Hutse, V.; Wautier, M.; Jacques, M.; Abady, M.; Lamoral, S.; Verburgh, V.; Thomas, I.; Brochier, B.; et al. Epidemiology and genotype 3 subtype dynamics of hepatitis E virus in Belgium, 2010 to 2017. Eurosurveillance 2019, 24, 1800141. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kozyra, I.; Bigoraj, E.; Jabłoński, A.; Politi, K.; Rzeżutka, A. Genetic Diversity and Epidemiological Significance of Wild Boar HEV-3 Strains Circulating in Poland. Viruses 2021, 13, 1176. [Google Scholar] [CrossRef] [PubMed]
- De Sabato, L.; Suffredini, E.; Di Pasquale, S.; La Rosa, G.; De Santis, P.; Giammarioli, M.; Vaccari, G.; Di Bartolo, I. Novel subtypes and unexpected heterogeneity of hepatitis E viral strains in wild boar captured in a small area in Central Italy. Transbound. Emerg. Dis. 2022, 69, e2541–e2550. [Google Scholar] [CrossRef] [PubMed]
- Presti, A.L.; Bruni, R.; Villano, U.; Marcantonio, C.; Equestre, M.; Ciuffetelli, M.; Grimaldi, A.; Suffredini, E.; Di Pasquale, S.; De Medici, D.; et al. Phylogenetic analysis and epidemiological history of Hepatitis E virus 3f and 3c in swine and wild boar, Italy. Heliyon 2020, 6, e05110. [Google Scholar] [CrossRef]
- Schotte, U.; Martin, A.; Brogden, S.; Schilling-Loeffler, K.; Schemmerer, M.; Anheyer-Behmenburg, H.E.; Szabo, K.; Müller-Graf, C.; Wenzel, J.J.; Kehrenberg, C.; et al. Phylogeny and spatiotemporal dynamics of hepatitis E virus infections in wild boar and deer from six areas of Germany during 2013–2017. Transbound. Emerg. Dis. 2022, 69, e1992–e2005. [Google Scholar] [CrossRef]
- Arnaboldi, S.; Righi, F.; Carta, V.; Bonardi, S.; Pavoni, E.; Bianchi, A.; Losio, M.N.; Filipello, V. Hepatitis E Virus (HEV) Spread and Genetic Diversity in Game Animals in Northern Italy. Food Environ. Virol. 2021, 13, 146–153. [Google Scholar] [CrossRef]
- Lemel, J.; Truvé, J.; Söderberg, B. Variation in ranging and activity behaviour of European wild boar Sus scrofa in Sweden. Wildl. Biol. 2003, 9, 29–36. [Google Scholar] [CrossRef]
- Andrzejewski, R.; Jezierski, W. Management of a wild boar population and its effects on commercial land. Acta Thériol. 1978, 23, 309–339. [Google Scholar] [CrossRef] [Green Version]
- Jothikumar, N.; Cromeans, T.L.; Robertson, B.H.; Meng, X.J.; Hill, V.R. A broadly reactive one-step real-time RT-PCR assay for rapid and sensitive detection of hepatitis E virus. J. Virol. Methods 2006, 131, 65–71. [Google Scholar] [CrossRef]
- Valcarce, M.D.; Kovač, K.; Cook, N.; Rodriguez-Lazaro, D.; Hernández, M. Construction and Analytical Application of Internal Amplification Controls (IAC) for Detection of Food Supply Chain-Relevant Viruses by Real-Time PCR-Based Assays. Food Anal. Methods 2011, 4, 437–445. [Google Scholar] [CrossRef]
- Lu, L.; Li, C.; Hagedorn, C.H. Phylogenetic analysis of global hepatitis E virus sequences: Genetic diversity, subtypes and zoonosis. Rev. Med. Virol. 2006, 16, 5–36. [Google Scholar] [CrossRef] [PubMed]
- Huang, F.F.; Haqshenas, G.; Guenette, D.K.; Halbur, P.G.; Schommer, S.K.; Pierson, F.W.; Toth, T.; Meng, X.J. 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. 2002, 40, 1326–1332. [Google Scholar] [CrossRef] [Green Version]
- Darriba, D.; Taboada, G.L.; Doallo, R.; Posada, D. jModelTest 2: More models, new heuristics and parallel computing. Nat. Methods 2012, 9, 772. [Google Scholar] [CrossRef] [Green Version]
- Tamura, K.; Nei, M.; Kumar, S. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc. Natl. Acad. Sci. USA 2004, 101, 11030–11035. [Google Scholar] [CrossRef] [Green Version]
- Kumar, S.; Stecher, G.; Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 2016, 33, 1870–1874. [Google Scholar] [CrossRef] [PubMed]
Hunting Season Year | No. Positive/ No. Tested | Prevalence (%) [95% CI] | Sequenced/ Positive | HEV Subtype (No. Identified) |
---|---|---|---|---|
2019–2020 | 12/285 | 4.2 [2.4–7.2] | 7/12 | 3a(2), 3c(1), 3m(1), 3 UN 1 (3) |
2020–2021 | 23/280 | 8.2 [5.5–12.0] | 9/23 | 3a(3), 3m(1), 3 UN 1 (5) |
2021–2022 | 22/284 | 7.7 [2.2–11.4] | 11/22 | 3a(1), 3b(2), 3m(2),3 UN 1 (5), (1) 2 |
Total (2019–2022) | 57/849 | 6.7 [5.2–8.6] | 27/57 | 3a(6), 3b(2), 3c(1), 3m (4), 3 UN 1 (13), (1) 2 |
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Battistini, R.; Serracca, L.; Razzuoli, E.; Listorti, V.; Guardone, L.; Dellepiane, M.; Pussini, N.; Brunelli, F.; Peletto, S.; Beltramo, C.; et al. Hepatitis E Virus (HEV): Identification of Subtypes 3b and 3m in Wild Boar Population in Liguria Region, Italy. Pathogens 2022, 11, 1236. https://doi.org/10.3390/pathogens11111236
Battistini R, Serracca L, Razzuoli E, Listorti V, Guardone L, Dellepiane M, Pussini N, Brunelli F, Peletto S, Beltramo C, et al. Hepatitis E Virus (HEV): Identification of Subtypes 3b and 3m in Wild Boar Population in Liguria Region, Italy. Pathogens. 2022; 11(11):1236. https://doi.org/10.3390/pathogens11111236
Chicago/Turabian StyleBattistini, Roberta, Laura Serracca, Elisabetta Razzuoli, Valeria Listorti, Lisa Guardone, Monica Dellepiane, Nicola Pussini, Francesco Brunelli, Simone Peletto, Chiara Beltramo, and et al. 2022. "Hepatitis E Virus (HEV): Identification of Subtypes 3b and 3m in Wild Boar Population in Liguria Region, Italy" Pathogens 11, no. 11: 1236. https://doi.org/10.3390/pathogens11111236