Prevalence of Hepatitis E Virus Infection in Pigs at the Time of Slaughter, United Kingdom, 2013 - Volume 21, Number 8—August 2015 - Emerging Infectious Disease journal - CDC
Volume 21, Number 8—August 2015
Prevalence of Hepatitis E Virus Infection in Pigs at the Time of Slaughter, United Kingdom, 2013
Hepatitis E virus (HEV) that infects humans is composed of 4 genotypes (G1–4), each with a different geographic distribution and host range (1). Although G1 and G2 infect humans only, G3 and G4 infect humans and animals. HEV G3 and G4 are distributed worldwide, with G3 most commonly infecting both humans and pigs in Europe (2).From the observed incidence of acute HEV infection in blood donors (3), it is clear that HEV G3 infection in humans in England is far more common than previously thought. Realistic estimates are >100,000 infections annually.
Public Health England instituted enhanced surveillance of HEV infections in England and Wales in 2003 (4) and identified a recent and marked increase in the number of patients seeking treatment for HEV infections. In 2013, a total of 691 cases were identified, of which 477 (69%) were considered indigenous (occurring in persons who had not traveled outside England and Wales). Sequencing of strains from these acutely infected persons has identified an emergent phylogenetic cluster of HEV G3 infection in humans, which is likely to represent a zoonosis acquired through the consumption of undercooked meat (B. Said, pers. comm.).
In an early study in the United Kingdom of porcine samples archived during 1991–2001, antibodies to HEV were detected in 85.5% of 256 samples tested (5). More recent studies across Europe indicate that many pig herds show evidence of HEV G3 infection (6–10). A transient viremia in pigs is associated with dissemination of HEV into muscle and other tissues (11). A recent UK study found HEV RNA in 6 of 63 pork sausages tested, of which 5 were in a single batch of 11 (12), and a case−control study in England and Wales showed that human consumption of processed pork products is associated with an increased risk of acquiring HEV (13). It has long been considered plausible that the persistence of viremia in infected pigs up to the time of slaughter could provide a potential vehicle for zoonotic transmission to humans (14). We conducted surveillance of pigs at slaughter to investigate the epizoology of HEV in the United Kingdom and the extent of infection at the time pigs enter the food chain.
Dr. Grierson is a research scientist in the Department of Virology at the Animal and Plant Health Agency, Weybridge, UK. Her research interests focus on the molecular characterization and epidemiology of veterinary viruses, primarily relating to pig diseases.
We thank colleagues at the Public Health England Blood Borne Virus Unit and the Animal and Plant Health Agency for their support and assistance.
The data collection described here was undertaken as part of a national “2013 Zoonoses in UK Pigs Abattoir Study” jointly funded by the Department for Environment, Food, and Rural Affairs; the Food Standards Agency; Veterinary Medicines Directorate; Public Health England (PHE); and UK pig industry levy boards including the British Pig Executive (a division of the Agriculture and Horticulture Development Board), Ulster Pork and Bacon Forum, and Quality Meat Scotland. Representatives from the Animal and Plant Health Agency (formerly known as the Animal Health and Veterinary Laboratories Agency); Department for Environment, Food, and Rural Affairs; and PHE designed the study. The laboratory testing, data collection, analysis, and interpretation of the information presented here were undertaken by staff from PHE and the Animal and Plant Health Agency.
- Aggarwal R, Naik S. Epidemiology of hepatitis E: current status. J Gastroenterol Hepatol. 2009;24:1484–93.
- Goens SD, Perdue ML. Hepatitis E viruses in humans and animals. Anim Health Res Rev. 2004;5:145–56.
- Hewitt PE, Ijaz S, Brailsford SR, Brett R, Dicks S, Haywood B, Hepatitis E virus in blood components: a prevalence and transmission study in southeast England. Lancet. 2014;384:1766-73.
- Ijaz S, Said B, Boxall E, Smit E, Morgan D, Tedder RS. Indigenous hepatitis E in England and Wales from 2003 to 2012: evidence of an emerging novel phylotype of viruses. J Infect Dis. 2014;209:1212-8.
- Banks M, Heath GS, Grierson SS, King DP, Gresham A, Girones R, Evidence for the presence of hepatitis E virus in pigs in the United Kingdom. Vet Rec. 2004;154:223–7.
- Berto A, Backer JA, Mesquita JR, Nascimento MS, Banks M, Martelli F, Prevalence and transmission of hepatitis E virus in domestic swine populations in different European countries. BMC Res Notes. 2012;5:190.
- Breum SØ, Hjulsager CK, de Deus N, Segalés J, Larsen LE. Hepatitis E virus is highly prevalent in the Danish pig population. Vet Microbiol.2010;146:144–9.
- Jiménez de Oya N, de Blas I, Blázquez AB, Martín-Acebes MA, Halaihel N, Gironés O, Widespread distribution of hepatitis E virus in Spanish pig herds. BMC Res Notes. 2011;4:412.
- Rose N, Lunazzi A, Dorenlor V, Merbah T, Eono F, Eloit M, High prevalence of hepatitis E virus in French domestic pigs. Comp Immunol Microbiol Infect Dis. 2011;34:419–27.
- Rutjes SA, Bouwknegt M, van der Giessen JW, de Roda Husman AM, Reusken CB. Seroprevalence of hepatitis E virus in pigs from different farming systems in The Netherlands. J Food Prot. 2014;77:640–2.
- Bouwknegt M, Rutjes SA, Reusken CB, Stockhofe-Zurwieden N, Frankena K, de Jong MC, The course of hepatitis E virus infection in pigs after contact-infection and intravenous inoculation. BMC Vet Res. 2009;5:7.
- Berto A, Martelli F, Grierson S, Banks M. Hepatitis E virus in pork food chain, United Kingdom, 2009–2010. Emerg Infect Dis. 2012;18:1358–60.
- Said B, Ijaz S, Chand MA, Kafatos G, Tedder R, Morgan D. Hepatitis E virus in England and Wales: indigenous infection is associated with the consumption of processed pork products. Epidemiol Infect. 2014;142:1467–75.
- Smith JL. A review of hepatitis E virus. J Food Prot. 2001;64:572–86.
- BPEX Agriculture and Horticulture Development Board. Pig pocketbook 2014 [cited 2014 Dec 16].http://www.bpex.org.uk/media/2426/pig_pocketbook_2014.pdf
- Department for Environment, Food, and Rural Affairs, Public Health England. Zoonoses report, UK, 2012 [cited 2014 Dec 16]. https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/236983/pb13987-zoonoses-report-2012.pdf
- Garson JA, Ferns RB, Grant PR, Ijaz S, Nastouli E, Szypulska R, Minor groove binder modification of widely used TaqMan probe for hepatitis E virus reduces risk of false negative real-time PCR results. J Virol Methods. 2012;186:157–60.
- Jothikumar N, Cromeans TL, Robertson BH, Meng XJ, Hill VR. 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.
- Meng XJ, Purcell RH, Halbur PG, Lehman JR, Webb DM, Tsareva TS, A novel virus in swine is closely related to the human hepatitis E virus. Proc Natl Acad Sci U S A. 1997;94:9860–5.
- Ijaz S, Arnold E, Banks M, Bendall RP, Cramp ME, Cunningham R, Non-travel-associated hepatitis E in England and Wales: demographic, clinical, and molecular epidemiological characteristics. J Infect Dis. 2005;192:1166–72.
- Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol.2013;30:2725–9.
- Walachowski S, Dorenlor V, Lefevre J, Lunazzi A, Eono F, Merbah T, 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;142:1934–44.
- Leblanc D, Poitras E, Gagné MJ, Ward P, Houde A. Hepatitis E virus load in swine organs and tissues at slaughterhouse determined by real-time RT-PCR. Int J Food Microbiol. 2010;139:206–9.
- Di Bartolo I, Ponterio E, Castellini L, Ostanello F, Ruggeri FM. Viral and antibody HEV prevalence in swine at slaughterhouse in Italy. Vet Microbiol.2011;149:330–8.
- Casas M, Cortés R, Pina S, Peralta B, Allepuz A, Cortey M, Longitudinal study of hepatitis E virus infection in Spanish farrow-to-finish swine herds.Vet Microbiol. 2011;148:27–34.
- Andraud M, Dumarest M, Cariolet R, Aylaj B, Barnaud E, Eono F, Direct contact and environmental contaminations are responsible for HEV transmission in pigs. Vet Res. 2013;44:102.
- Colson P, Borentain P, Queyriaux B, Kaba M, Moal V, Gallian P, Pig liver sausage as a source of hepatitis E virus transmission to humans. J Infect Dis.2010;202:825–34.
- Wacheck S, Werres C, Mohn U, Dorn S, Soutschek E, Fredriksson-Ahomaa M, Detection of IgM and IgG against hepatitis E virus in serum and meat juice samples from pigs at slaughter in Bavaria, Germany. Foodborne Pathog Dis. 2012;9:655–60.
- Satou K, Nishiura H. Transmission dynamics of hepatitis E among swine: potential impact upon human infection. BMC Vet Res. 2007;3:9.
- Backer JA, Berto A, McCreary C, Martelli F, van der Poel WH. Transmission dynamics of hepatitis E virus in pigs: estimation from field data and effect of vaccination. Epidemics. 2012;4:86–92.
Suggested citation for this article: Grierson S, Heaney J, Cheney T, Morgan D, Wyllie S, Powell L, et al. Prevalence of hepatitis E virus infection in pigs at the time of slaughter, United Kingdom, 2013. Emerg Infect Dis. 2015 Aug [date cited]. http://dx.doi.org/10.3201/eid2108.141995