Hepatitis E Virus (HEV) in the Swine Production Chain: From Farm to Fork Control Strategies

A special issue of Animals (ISSN 2076-2615). This special issue belongs to the section "Pigs".

Deadline for manuscript submissions: closed (1 October 2021) | Viewed by 20183

Special Issue Editors


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Guest Editor
Department of Veterinary Medical Sciences, University of Bologna, Ozzano dell'Emilia, BO, Italy
Interests: swine; hepatitis E virus (HEV); epidemiology; veterinary public health; infectious diseases; diagnosis
Special Issues, Collections and Topics in MDPI journals

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Guest Editor
Department of Food Safety, Nutrition and Veterinary Public Health, Istituto Superiore di Sanità, Viale Regina Elena, 299, 00161 Rome, Italy
Interests: swine; hepatitis E virus; HEV; epidemiology; veterinary public health; infectious diseases; diagnosis

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Guest Editor
Department of Veterinary Medical Sciences, University of Bologna, Via Tolara di Sopra 50, 40064 Ozzano Emilia (BO), Italy
Interests: swine; antimicrobial resistance; AMR; epidemiology; veterinary public health; infectious diseases; diagnosis

Special Issue Information

Dear Colleagues,

Over the last 10 years, an increasing number of autochthonous human hepatitis E cases have been described in developed countries and linked to the zoonotic transmission of the genotypes HEV-3 and HEV-4. The presence of HEV-3 and HEV-4 has been extensively described in domestic and feral swine populations and the transmission to humans may be favored by the widespread and high prevalence of HEV infection in pig farms and wild boar population. Due to the important HEV implications for public health, much additional information is needed to bridge the knowledge gap about HEV and to establish control measures to reduce the risk of introducing contaminated products into the food chain.

This Special Issue aims to provide new insights for a wide range of stakeholders from different countries, outlining and covering all the main topics related to the definition, planning, and implementation of control measures to reduce the risk of zoonotic transmission of HEV. Original manuscripts should focus on harmonization of HEV laboratory testing, risk analysis and surveillance studies on farms, wild boar hunting and slaughterhouses, interactions between HEV and other phatogens, etc., with special emphasis on identification of risk factors. The issue aims to provide new insights for a wide range of stakeholders from different countries.

Dr. Ilaria Di Bartolo
Dr. Fabio Ostanello
Dr. Alessia De Lucia
Guest Editors

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Keywords

  • pig
  • wild board
  • Hepatitis E virus
  • HEV
  • zoonosis
  • diagnosis
  • public health
  • surveillance
  • foodborne
  • risk analysis

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Published Papers (6 papers)

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Research

17 pages, 1107 KiB  
Article
Study of Animal Mixing and the Dynamics of Hepatitis E Virus Infection on a Farrow-to-Finish Pig Farm
by Susan M. Withenshaw, Sylvia S. Grierson and Richard P. Smith
Animals 2022, 12(3), 272; https://doi.org/10.3390/ani12030272 - 22 Jan 2022
Cited by 7 | Viewed by 3227
Abstract
In Europe, swine are a livestock reservoir for Hepatitis E virus genotype 3 (HEV-3). Consumption of food containing HEV-3 can cause zoonotic human infection, though risk is reduced by heat treatment. Implementing controls that limit infection in slaughter pigs may further reduce foodborne [...] Read more.
In Europe, swine are a livestock reservoir for Hepatitis E virus genotype 3 (HEV-3). Consumption of food containing HEV-3 can cause zoonotic human infection, though risk is reduced by heat treatment. Implementing controls that limit infection in slaughter pigs may further reduce foodborne transmission risk but knowledge of infection dynamics on commercial farms is limited. This study addressed this knowledge gap and in particular investigated the influence of group mixing. Faeces were collected from grower (n = 212) and fattener (n = 262) pigs on a farrow-to-finish farm on four occasions. HEV RNA was detected on all occasions, and prevalence was higher in growers (85.8%) than fatteners (26.0%; p < 0.001). HEV-positive samples were also collected from the wider farm environment (n = 67; 64.7% prevalence), indicating potential sources for HEV re-circulation within the herd. Timing of infection in a cohort was also investigated. HEV was absent from all piglet faeces (n = 98) and first detected at weaner stage (25.7% prevalence), but only in groups weaned earlier or comprising pigs from many different litters. Farrowing sow faeces (n = 75) were HEV-negative but antibodies were detected in blood from two sows. Results suggest that multiple factors influence HEV infection dynamics on pig farms, and potential foci for further study into practical control solutions are highlighted. Full article
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18 pages, 1892 KiB  
Article
Genetic Diversity of Hepatitis E Virus Type 3 in Switzerland—From Stable to Table
by Isabelle Vonlanthen-Specker, Roger Stephan, Xaver Sidler, Dominik Moor, Cornel Fraefel and Claudia Bachofen
Animals 2021, 11(11), 3177; https://doi.org/10.3390/ani11113177 - 7 Nov 2021
Cited by 8 | Viewed by 2839
Abstract
Hepatitis E caused by hepatitis E viruses of the genotype 3 (HEV-3) is a major health concern in industrialized countries and due to its zoonotic character requires a “One Health” approach to unravel routes and sources of transmission. Knowing the viral diversity present [...] Read more.
Hepatitis E caused by hepatitis E viruses of the genotype 3 (HEV-3) is a major health concern in industrialized countries and due to its zoonotic character requires a “One Health” approach to unravel routes and sources of transmission. Knowing the viral diversity present in reservoir hosts, i.e., pigs but also wild boars, is an important prerequisite for molecular epidemiology. The aim of this study was to gain primary information on the diversity of HEV-3 subtypes present along the food chain in Switzerland, as well as the diversity within these subtypes. To this end, samples of domestic pigs from slaughterhouses and carcass collection points, as well as from hunted wild boars, were tested for HEV RNA and antibodies. HEV positive meat products were provided by food testing labs. The HEV subtypes were determined using Sanger and next generation sequencing. The genetic analyses confirmed the predominance of a Swiss-specific cluster within subtype HEV-3h in pigs, meat products, and wild boars. This cluster, which may result from local virus evolution due to the isolated Swiss pig industry, supports fast differentiation of domestic and imported infections with HEV. Full article
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17 pages, 1836 KiB  
Article
Screening of Swiss Pig Herds for Hepatitis E Virus: A Pilot Study
by Julia Lienhard, Isabelle Vonlanthen-Specker, Xaver Sidler and Claudia Bachofen
Animals 2021, 11(11), 3050; https://doi.org/10.3390/ani11113050 - 25 Oct 2021
Cited by 5 | Viewed by 2613
Abstract
Hepatitis E virus (HEV) is an important cause of acute hepatitis in humans worldwide. In industrialised countries, most infections are caused by the zoonotic genotype 3. The main reservoir was found in pigs, with fattening pigs as the main shedders. The aim of [...] Read more.
Hepatitis E virus (HEV) is an important cause of acute hepatitis in humans worldwide. In industrialised countries, most infections are caused by the zoonotic genotype 3. The main reservoir was found in pigs, with fattening pigs as the main shedders. The aim of this study was to establish a screening tool to detect HEV in pig farms. HEV-positive samples were sequenced using Sanger sequencing. First, different sample materials, including floor swabs, slurry, dust swabs and faeces were tested for HEV. Floor swabs turned out to give the best results and, in the form of sock swabs, were used for the screening of Swiss pig herds. A total of 138 pig farms were tested, with a focus on fattening pigs. Overall, 81 farms (58.8%) were HEV positive. Most sequences belonged to subtype 3h, in which they formed a specific cluster (Swiss cluster). In addition, subtype 3l and two unassigned sequences were detected. As a conclusion, sock swabs were found to be a helpful tool to screen pig herds for HEV and establish a sequence collection that may enable molecular epidemiology and support outbreak investigation and prevention. Full article
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8 pages, 712 KiB  
Article
Hepatitis E Virus RNA Presence in Wild Boar Carcasses at Slaughterhouses in Italy
by Mario Forzan, Maria Irene Pacini, Marcello Periccioli and Maurizio Mazzei
Animals 2021, 11(6), 1624; https://doi.org/10.3390/ani11061624 - 31 May 2021
Cited by 14 | Viewed by 4226
Abstract
Hepatitis E virus (HEV) is a waterborne and foodborne pathogen largely spread around the world. HEV is responsible for acute hepatitis in humans and it is also diffused in domestic and wild animals. In particular, domestic pigs represent the main reservoir of the [...] Read more.
Hepatitis E virus (HEV) is a waterborne and foodborne pathogen largely spread around the world. HEV is responsible for acute hepatitis in humans and it is also diffused in domestic and wild animals. In particular, domestic pigs represent the main reservoir of the infection and particular attention should be paid to the consumption of raw and undercooked meat as a possible zoonotic vehicle of the pathogen. Several studies have reported the presence of HEV in wild boar circulating in European countries with similar prevalence rates. In this study, we evaluated the occurrence of HEV in wild boar hunted in specific areas of Tuscany. Sampling was performed by collecting liver samples and also by swabbing the carcasses at the slaughterhouses following hunting activities. Our data indicated that 8/67 (12%) of liver samples and 4/67 (6%) of swabs were positive for HEV RNA. The presence of HEV genome on swabs indicates the possible cross-contamination of carcass surfaces during slaughtering procedures. Altogether, our data indicated that it is essential to promote health education programmes for hunters and consumers to limit the diffusion of the pathogen to humans. Full article
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14 pages, 586 KiB  
Article
Hepatitis E Virus Occurrence in Pigs Slaughtered in Italy
by Eleonora Chelli, Elisabetta Suffredini, Paola De Santis, Dario De Medici, Santina Di Bella, Stefania D’Amato, Francesca Gucciardi, Annalisa Guercio, Fabio Ostanello, Vitantonio Perrone, Giuseppa Purpari, Gaia Sofia Scavia, Pietro Schembri, Bianca Maria Varcasia and Ilaria Di Bartolo
Animals 2021, 11(2), 277; https://doi.org/10.3390/ani11020277 - 22 Jan 2021
Cited by 24 | Viewed by 2947
Abstract
In Europe, foodborne transmission has been clearly associated to sporadic cases and small clusters of hepatitis E in humans linked to the consumption of contaminated pig liver sausages, raw venison, or undercooked wild boar meat. In Europe, zoonotic HEV-genotype 3 strains are widespread [...] Read more.
In Europe, foodborne transmission has been clearly associated to sporadic cases and small clusters of hepatitis E in humans linked to the consumption of contaminated pig liver sausages, raw venison, or undercooked wild boar meat. In Europe, zoonotic HEV-genotype 3 strains are widespread in pig farms but little information is available on the prevalence of HEV positive pigs at slaughterhouse. In the present study, the prevalence of HEV-RNA positive pigs was assessed on 585 animals from 4 abattoirs located across Italy. Twenty-one pigs (3.6%) tested positive for HEV in either feces or liver by real-time RT-PCR. In these 21 pigs, eight diaphragm muscles resulted positive for HEV-RNA. Among animals collected in one abattoir, 4 out of 91 plasma tested positive for HEV-RNA. ELISA tests for the detection of total antibodies against HEV showed a high seroprevalence (76.8%), confirming the frequent exposure of pigs to the virus. The phylogenetic analyses conducted on sequences of both ORF1 and ORF2 fragments, shows the circulation of HEV-3c and of a novel unclassified subtype. This study provides information on HEV occurrence in pigs at the slaughterhouse, confirming that muscles are rarely contaminated by HEV-RNA compared to liver, which is the most frequently positive for HEV. Full article
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13 pages, 886 KiB  
Article
Pilot Investigation on the Presence of Anti-Hepatitis E Virus (HEV) Antibodies in Piglet Processing Fluids
by Ilaria Di Bartolo, Luca De Sabato, Eleonora Chelli, Giovanni Loris Alborali, Matteo Tonni, Marina Monini, Alessia De Lucia and Fabio Ostanello
Animals 2020, 10(7), 1168; https://doi.org/10.3390/ani10071168 - 9 Jul 2020
Cited by 1 | Viewed by 2296
Abstract
Identifying Hepatitis E virus (HEV)-positive pig farms is important to implement surveillance programs for this emerging zoonotic agent. The aim of this study was to evaluate the use of serosanguineous fluids obtained as part of castration practice (processing fluids (PFs)) to detect anti-HEV [...] Read more.
Identifying Hepatitis E virus (HEV)-positive pig farms is important to implement surveillance programs for this emerging zoonotic agent. The aim of this study was to evaluate the use of serosanguineous fluids obtained as part of castration practice (processing fluids (PFs)) to detect anti-HEV antibodies in newborn piglets. Ninety-five paired serum and PF samples were collected from piglets of 29 different litters and tested with a commercial ELISA kit. A significant positive correlation (Spearman’s rho: 0.600; p < 0.01) was found between anti-HEV antibodies in serum and PF samples. In 26 out of 29 litters (89.7%), there was at least one positive piglet in the serum. Sixteen litters out of 29 (55.2%) were also positive in PFs. To simulate the use of PF as pooled samples, the limit of detection of the ELISA was assessed mixing the PF sample with strong, medium, medium-weak and weak ELISA titres with 3, 4, 5 and 6 negative PF samples. Our results suggest that it is still possible to identify a positive PF pool when at least one individual PF sample with medium or strong antibody levels is mixed with 5 or 6 individual negative PF samples. The detection of anti-HEV maternal-derived antibodies in PF confirms a past exposure of sows to the virus. PF may represent a rapid, noninvasive and economical tool to identify HEV-positive farms. Full article
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