[en] Hepatitis E virus (HEV) is the causative agent of hepatitis E disease in humans. While sporadic HEV infections, which occur in industrialised countries and are typically due to HEV genotypes 3 or 4, are asymptomatic and self-limiting, a chronic form of the disease can lead to liver cirrhosis in immunocompromised individuals. Pigs share HEV 3 and 4 genotypes and are thus considered a major animal reservoir for human infection. A subset of animals has been shown to carry HEV particles at the age of slaughter, rendering raw or undercooked pig products potential vectors for human infection. To provide an overview of the current dissemination of HEV in Belgian pig herds, this study was designed as a randomized, robust, large-scale, cross-sectional, serological survey. HEV genotypes and subtypes recently circulating in Belgium (2020-2021) were investigated. Sample stratification as well as epidemiological investigation through the available demographic data of the sampled herds showed that HEV widely circulated in the Belgian pig population during this time and that a change in the circulating HEV strains may have occurred in the last decade. Herd size and type were identified as risk factors for HEV herd-seropositivity. Identifying farms at risk of being HEV-positive is an important step in controlling HEV spread and human infection.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Wielick, Constance ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Santé publique vétérinaire
Ludwig-Begall, Louisa ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Santé publique vétérinaire
Faes, Christel ; Center for Statistics, Data Science Institute, Hasselt University, 3500 Hasselt, Belgium
Ribbens, Stefaan ; Animal Health Service Flanders (DGZ Vlaanderen), 8820 Torhout, Belgium
Saegerman, Claude ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Epidémiologie et analyse des risques appliqués aux sciences vétérinaires
Thiry, Etienne ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI)
Language :
English
Title :
A Randomized Large-Scale Cross-Sectional Serological Survey of Hepatitis E Virus Infection in Belgian Pig Farms.
Smith D.B. Simmonds P. Jameel S. Emerson S.U. Harrison T.J. Meng X.J. Okamoto H. van der Poel W.H.M. Purdy M.A. Consensus Proposals for Classification of the Family Hepeviridae J. Gen. Virol. 2014 95 Pt 10 2223 2232 10.1099/vir.0.068429-0
World Health Organization Hepatitis E Available online: https://www.who.int/news-room/fact-sheets/detail/hepatitis-e (accessed on 14 September 2022)
Lee G.H. Tan B.H. Chi-Yuan Teo E. Lim S.G. Dan Y.Y. Wee A. Kim Aw P.P. Zhu Y. Hibberd M.L. Tan C.K. et al. Chronic Infection with Camelid Hepatitis E Virus in a Liver Transplant Recipient Who Regularly Consumes Camel Meat and Milk Gastroenterology 2016 150 355 357 10.1053/j.gastro.2015.10.048
Thiry D. Mauroy A. Pavio N. Purdy M.A. Rose N. Thiry E. de Oliveira-Filho E.F. Hepatitis E Virus and Related Viruses in Animals Transbound. Emerg. Dis. 2017 64 37 52 10.1111/tbed.12351
Khuroo M.S. Khuroo M.S. Khuroo N.S. Transmission of Hepatitis E Virus in Developing Countries Viruses 2016 8 253 10.3390/v8090253
Singh M.P. Majumdar M. Goyal K. Lakshmi P.V.M. Bhatia D. Ratho R.K. Investigation of Suspected Viral Hepatitis Outbreaks in North West India Diagn. Microbiol. Infect. Dis. 2016 84 309 314 10.1016/j.diagmicrobio.2015.12.002
Belei O. Ancusa O. Mara A. Olariu L. Amaricai E. Folescu R. Zamfir C.L. Gurgus D. Motoc A.G. Stânga L.C. et al. Current Paradigm of Hepatitis E Virus among Pediatric and Adult Patients Front. Pediatr. 2021 9 721918 10.3389/fped.2021.721918
Kamar N. Legrand-Abravanel F. Izopet J. Rostaing L. Hepatitis E Virus: What Transplant Physicians Should Know Am. J. Transplant. 2012 12 2281 2287 10.1111/j.1600-6143.2012.04078.x
Sue P.K. Pisanic N. Heaney C.D. Forman M. Valsamakis A. Jackson A.M. Ticehurst J.R. Montgomery R.A. Schwarz K.B. Nelson K.E. et al. Hepatitis E Virus Infection Among Solid Organ Transplant Recipients at a North American Transplant Center Open Forum Infect. Dis. 2016 3 ofw006 10.1093/ofid/ofw006
Kamar N. Dalton H.R. Abravanel F. Izopet J. Hepatitis E Virus Infection Clin. Microbiol. Rev. 2014 27 116 138 10.1128/CMR.00057-13
Ho E. Schenk J. Hutse V. Suin V. Litzroth A. Blaizot S. Herzog S.A. Verburgh V. Jacques M. Rahman A. et al. Stable HEV IgG Seroprevalence in Belgium between 2006 and 2014 J. Viral Hepat. 2020 27 1253 1260 10.1111/jvh.13347
Meng X.-J. Halbur P.G. Shapiro M.S. Govindarajan S. Bruna J.D. Mushahwar I.K. Purcell R.H. Emerson S.U. Genetic and Experimental Evidence for Cross-Species Infection by Swine Hepatitis E Virus J. Virol. 1998 72 9714 9721 10.1128/JVI.72.12.9714-9721.1998
Halbur P.G. Kasorndorkbua C. Gilbert C. Guenette D. Potters M.B. Purcell R.H. Emerson S.U. Toth T.E. Meng X.J. Comparative Pathogenesis of Infection of Pigs with Hepatitis E Viruses Recovered from a Pig and a Human J. Clin. Microbiol. 2001 39 918 923 10.1128/JCM.39.3.918-923.2001
Li P. Liu J. Li Y. Su J. Ma Z. Bramer W.M. Cao W. de Man R.A. Peppelenbosch M.P. Pan Q. The Global Epidemiology of Hepatitis E Virus Infection: A Systematic Review and Meta-Analysis Liver Int. 2020 40 1516 1528 10.1111/liv.14468
Leblanc D. Ward P. Gagné M.J. Poitras E. Müller P. Trottier Y.L. Simard C. Houde A. Presence of Hepatitis E Virus in a Naturally Infected Swine Herd from Nursery to Slaughter Int. J. Food Microbiol. 2007 117 160 166 10.1016/j.ijfoodmicro.2007.03.008
Casas M. Pujols J. Rosell R. de Deus N. Peralta B. Pina S. Casal J. Martín M. Retrospective Serological Study on Hepatitis E Infection in Pigs from 1985 to 1997 in Spain Vet. Microbiol. 2009 135 248 252 10.1016/j.vetmic.2008.09.075
Rose N. Lunazzi A. Dorenlor V. Merbah T. Eono F. Eloit M. Madec F. Pavio N. High Prevalence of Hepatitis E Virus in French Domestic Pigs Comp. Immunol. Microbiol. Infect. Dis. 2011 34 419 427 10.1016/j.cimid.2011.07.003
Martinelli N. Luppi A. Cordioli P. Lombardi G. Lavazza A. Prevalence of Hepatitis E Virus Antibodies in Pigs in Northern Italy Infect. Ecol. Epidemiol. 2011 1 7331 10.3402/iee.v1i0.7331
Lange H. Overbo J. Borgen K. Dudman S. Hoddevik G. Urdahl A.M. Vold L. Sjurseth S.K. Hepatitis E in Norway: Seroprevalence in Humans and Swine Epidemiol. Infect. 2017 145 181 186 10.1017/S0950268816002144
Pavio N. Merbah T. Thébault A. Frequent Hepatitis E Virus Contamination in Food Containing Raw Pork Liver, France Emerg. Infect. Dis. 2014 20 1925 1927 10.3201/eid2011.140891
Salaün Y. Hémonic A. Marcon M. Courboulay V. Quiniou N. Bidanel J. Duflot B. Mémento de l’Éleveur de Porc 7th ed. Institut Technique du Porc Paris, France 2013
Collège des Producteurs Filagri—Le Secteur Porcs Available online: https://filagri.be/porcs/le-secteur-porcs/ (accessed on 16 September 2022)
Wavreille J. Rondia P. Decruyenaere V. Jamar D. Stilmant D. Gengler N. Mayeres P. Beckers Y. Sindic M. Bartiaux-Thill N. La Diversification En Productions Animales 10ème Carrefour des Productions Animales: L’élevage: Hier, Aujourd’hui, Demain Quelles Attentes Pour Quels Enjeux? CRA-W et FUSAGx Gembloux, Belgique 2005 53 57
Thiry D. Mauroy A. Saegerman C. Licoppe A. Fett T. Thomas I. Brochier B. Thiry E. Linden A. Belgian Wildlife as Potential Zoonotic Reservoir of Hepatitis E Virus Transbound. Emerg. Dis. 2017 64 764 773 10.1111/tbed.12435
von Elm E. Altman D.G. Egger M. Pocock S.J. Gøtzsche P.C. Vandenbroucke J.P. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) Statement: Guidelines for Reporting Observational Studies Int. J. Surg. 2014 12 1495 1499 10.1016/j.ijsu.2014.07.013 25046131
Thiry D. Mauroy A. Saegerman C. Thomas I. Wautier M. Miry C. Czaplicki G. Berkvens D. Praet N. van der Poel W. et al. Estimation of Hepatitis E Virus (HEV) Pig Seroprevalence Using ELISA and Western Blot and Comparison between Human and Pig HEV Sequences in Belgium Vet. Microbiol. 2014 172 407 414 10.1016/j.vetmic.2014.06.004 24975642
Angus C. Survey Toolbox for Livestock Diseases: A Practical Manual and Software Package for Active Surveillance of Livestock Diseases in Developing Countries Australian Centre for International Agricultural Research Australian Government Publishing Service Canberra, Australia 1999
Arrêté Ministériel Portant Exécution de l’Arrêté Royal du 12 Octobre 2010 Relatif à la Lutte Contre la Maladie d’Aujeszky. Moniteur Belge. 23 July 2013 Available online: http://www.ejustice.just.fgov.be/mopdf/2013/07/30_1.pdf#Page19 (accessed on 22 November 2022)
Cannon R.M. Roe R.T. Livestock Disease Surveys. A Field Manual for Veterinarians Australian Government Publishing Service Canberra, Australia 1982
De Deus N. Casas M. Peralta B. Nofrarías M. Pina S. Martín M. Segalés J. Hepatitis E Virus Infection Dynamics and Organic Distribution in Naturally Infected Pigs in a Farrow-to-Finish Farm Vet. Microbiol. 2008 132 19 28 10.1016/j.vetmic.2008.04.036 18562132
Huang F.F. Haqshenas G. Guenette D.K. Halbur P.G. Schommer S.K. Pierson F.W. Toth T.E. 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 10.1128/JCM.40.4.1326-1332.2002
Cooper K. Huang F.F. Batista L. Rayo C.D. Bezanilla J.C. Toth T.E. Meng X.J. 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 J. Clin. Microbiol. 2005 43 1684 1688 10.1128/JCM.43.4.1684-1688.2005
Baylis S.A. Hanschmann K.M. Blümel J. Nübling C.M. Standardization of Hepatitis E Virus (HEV) Nucleic Acid Amplification Technique-Based Assays: An Initial Study to Evaluate a Panel of HEV Strains and Investigate Laboratory Performance J. Clin. Microbiol. 2011 49 1234 1239 10.1128/JCM.02578-10
Shukla P. Nguyen H.T. Torian U. Engle R.E. Faulk K. Dalton H.R. Bendall R.P. Keane F.E. Purcell R.H. Emerson S.U. Cross-Species Infections of Cultured Cells by Hepatitis E Virus and Discovery of an Infectious Virus-Host Recombinant Proc. Natl. Acad. Sci. USA 2011 108 2438 2443 10.1073/pnas.1018878108
Graff J. Torian U. Nguyen H. Emerson S.U. A Bicistronic Subgenomic mRNA Encodes Both the ORF2 and ORF3 Proteins of Hepatitis E Virus J. Virol. 2006 80 5919 5926 10.1128/JVI.00046-06
Smith D.B. Simmonds P. Izopet J. Oliveira-Filho E.F. Ulrich R.G. Johne R. Koenig M. Jameel S. Harrison T.J. Meng X.J. et al. Proposed Reference Sequences for Hepatitis E Virus Subtypes J. Gen. Virol. 2016 97 Pt 3 537 542 10.1099/jgv.0.000393
Kumar S. Stecher G. Li M. Knyaz C. Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms Mol. Biol. Evol. 2018 35 1547 1549 10.1093/molbev/msy096 29722887
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 10.1002/rmv.482 16175650
Tamura K. Nei M. Estimation of the Number of Nucleotide Substitutions in the Control Region of Mitochondrial DNA in Humans and Chimpanzees Mol. Biol. Evol. 1993 10 512 526 10.1093/OXFORDJOURNALS.MOLBEV.A040023 8336541
Faes C. Aerts M. Litière S. Méroc E. van der Stede Y. Mintiens K. Estimating Herd Prevalence on the Basis of Aggregate Testing of Animals J. R. Stat. Soc. Ser. A Stat. Soc. 2011 174 155 174 10.1111/j.1467-985X.2010.00652.x
Li H. Wu J. Sheng Y. Lu Q. Liu B. Chen Y. Sun Y. Zhou E.M. Zhao Q. Prevalence of Hepatitis E Virus (HEV) Infection in Various Pig Farms from Shaanxi Province, China: First Detection of HEV RNA in Pig Semen Transbound. Emerg. Dis. 2019 66 72 82 10.1111/tbed.12966 30043495
Risalde M.A. Frias M. Caballero-Gómez J. Lopez-Lopez P. Fast C. Jiménez-Ruiz S. Agulló-Ros I. Eiden M. Jiménez-Martín D. García-Bocanegra I. et al. Presence of Hepatitis E Virus in Testis of Naturally Infected Wild Boars Transbound. Emerg. Dis. 2022 in press 10.1111/tbed.14682
Zhang W. Shen Q. Mou J. Gong G. Yang Z. Cui L. Zhu J. Ju G. Hua X. Hepatitis E Virus Infection among Domestic Animals in Eastern China Zoonoses Public Health 2008 55 291 298 10.1111/j.1863-2378.2008.01136.x
Seminati C. Mateu E. Peralta B. de Deus N. Martin M. Distribution of Hepatitis E Virus Infection and Its Prevalence in Pigs on Commercial Farms in Spain Vet. J. 2008 175 130 132 10.1016/j.tvjl.2006.11.018
Vitral C.L. Pinto M.A. Lewis-Ximenez L.L. Khudyakov Y.E. dos Santos D.R. Gaspar A.M.C. Serological Evidence of Hepatitis E Virus Infection in Different Animal Species from the Southeast of Brazil Mem. Inst. Oswaldo Cruz 2005 100 117 122 10.1590/S0074-02762005000200003
Kasorndorkbua C. Thacker B.J. Halbur P.G. Guenette D.K. Buitenwerf R.M. Royer R.L. Meng X.J. Experimental Infection of Pregnant Gilts with Swine Hepatitis E Virus Can. J. Vet. Res. 2003 67 303 306
Andraud M. Casas M. Pavio N. Rose N. Early-Life Hepatitis E Infection in Pigs: The Importance of Maternally-Derived Antibodies PLoS ONE 2014 9 e105527 10.1371/journal.pone.0105527
Andraud M. Dumarest M. Cariolet R. Aylaj B. Barnaud E. Eono F. Pavio N. Rose N. Direct Contact and Environmental Contaminations Are Responsible for HEV Transmission in Pigs Vet. Res. 2013 44 102 10.1186/1297-9716-44-102 24165278
Walachowski S. Dorenlor V. Lefevre J. Lunazzi A. Eono F. Merbah T. Eveno E. Pavio N. Rose N. Risk Factors Associated with the Presence of Hepatitis E Virus in Livers and Seroprevalence in Slaughter-Age Pigs: A Retrospective Study of 90 Swine Farms in France Epidemiol. Infect. 2014 142 1934 1944 10.1017/S0950268813003063 24284046
Hinjoy S. Nelson K.E. Gibbons R.V. Jarman R.G. Chinnawirotpisan P. Fernandez S. Tablerk P. Labrique A.B. Patchanee P. A Cross-Sectional Study of Hepatitis E Virus Infection in Pigs in Different-Sized Farms in Northern Thailand Foodborne Pathog. Dis. 2013 10 698 704 10.1089/fpd.2012.1369 23789726
Jinshan Jirintai Manglai D. Takahashi M. Nagashima S. Okamoto H. Molecular and Serological Survey of Hepatitis E Virus Infection among Domestic Pigs in Inner Mongolia, China Arch. Virol. 2010 155 1217 1226 10.1007/s00705-010-0706-0
Li W. She R. Wei H. Zhao J. Wang Y. Sun Q. Zhang Y. Wang D. Li R. Prevalence of Hepatitis E Virus in Swine under Different Breeding Environment and Abattoir in Beijing, China Vet. Microbiol. 2009 133 75 83 10.1016/j.vetmic.2008.06.026
di Bartolo I. Martelli F. Inglese N. Pourshaban M. Caprioli A. Ostanello F. Ruggeri F.M. Widespread Diffusion of Genotype 3 Hepatitis E Virus among Farming Swine in Northern Italy Vet. Microbiol. 2008 132 47 55 10.1016/j.vetmic.2008.04.028
Meester M. Bouwknegt M. der Honing R.H. Vernooij H. Houben M. van Oort S. van der Poel W.H.M. Stegeman A. Tobias T. Repeated Cross-Sectional Sampling of Pigs at Slaughter Indicates Varying Age of Hepatitis E Virus Infection within and between Pig Farms Vet. Res. 2022 53 50 10.1186/s13567-022-01068-3
Rutjes S.A. Bouwknegt M. van der Giessen J.W. de Roda Husman A.M. Reusken C.B.E.M. Seroprevalence of Hepatitis e Virus in Pigs from Different Farming Systems in the Netherlands J. Food Prot. 2014 77 640 642 10.4315/0362-028X.JFP-13-302
Bouwknegt M. Rutjes S.A. Reusken C.B.E.M. Stockhofe-Zurwieden N. Frankena K. de Jong M.C.M. de Roda Husman A.M. van der Poel W.H.M. The Course of Hepatitis E Virus Infection in Pigs after Contact-Infection and Intravenous Inoculation BMC Vet. Res. 2009 5 7 10.1186/1746-6148-5-7
Bouwknegt M. Teunis P.F.M. Frankena K. de Jong M.C.M. de Roda Husman A.M. Estimation of the Likelihood of Fecal-Oral HEV Transmission Among Pigs Risk Anal. 2011 31 940 950 10.1111/j.1539-6924.2010.01546.x
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 10.2807/1560-7917.ES.2019.24.10.1800141 30862337
Subissi L. Peeters M. Lamoral S. Klamer S. Suin V. van Gucht S. Subtype-Specific Differences in the Risk of Hospitalisation among Patients Infected with Hepatitis E Virus Genotype 3 in Belgium, 2010–2018 Epidemiol. Infect. 2019 147 E224 10.1017/S0950268819001122 31364564
Thiry D. Rose N. Mauroy A. Paboeuf F. Dams L. Roels S. Pavio N. Thiry E. Susceptibility of Pigs to Zoonotic Hepatitis E Virus Genotype 3 Isolated from a Wild Boar Transbound. Emerg. Dis. 2017 64 1589 1597 10.1111/tbed.12550 27477944
Ricci A. Allende A. Bolton D. Chemaly M. Davies R. Fernandez Escamez P.S. Herman L. Koutsoumanis K. Lindqvist R. Nørrung B. et al. Public Health Risks Associated with Hepatitis E Virus (HEV) as a Food-borne Pathogen EFSA J. 2017 15 4886 10.2903/J.EFSA.2017.4886