Zoonotic Hepatitis E Virus: A Focus on Animals, Food and Environment

A special issue of Pathogens (ISSN 2076-0817). This special issue belongs to the section "Viral Pathogens".

Deadline for manuscript submissions: closed (10 October 2024) | Viewed by 21443

Special Issue Editors


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Guest Editor
Faculty of Veterinary Medicine, Università degli Studi di Teramo, 64100 Teramo, Italy
Interests: feline; canine; infectious diseases; emerging viruses
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Guest Editor
Faculty of Veterinary Medicine, Università degli Studi di Teramo, 64100 Teramo, Italy
Interests: enteric and hepatotropic viruses of animals with potential zoonotic

E-Mail Website
Guest Editor
Faculty of Veterinary Medicine, Università degli Studi di Teramo, 64100 Teramo, Italy
Interests: enteric and hepatotropic viruses of animals with potential zoonotic

Special Issue Information

Dear Colleagues,

Hepatitis E virus (HEV) infection is a major health problem worldwide. HEV typically causes self-limiting acute viral hepatitis, although chronic infection with neurological and other extrahepatic manifestations has also been reported.

The literature indicates that domestic pigs and wild boars are the main reservoirs of genotype 3 and genotype 4 for human infections in industrialized countries. However, the recent identification of HEV from various animal species poses additional potential concerns for HEV zoonotic infection.

The consumption of poorly cooked or raw pork meat is considered the major source of human infection. However, other food types may represent additional sources of human infection, such as  bivalve molluscs when growing in coastal waters prone to sewage pollution and leafy vegetables following the use of contaminated organic fertilisers.

This Special Issue aims to provide new insights outlining and covering all the main topics on the pathways of HEV infection in the context of an integrated animal/food/environmental surveillance. We would like to invite colleagues investigating the epidemiology of HEV in animals, food, and environments to submit their manuscripts to this Special Issue in the form of original research or reviews.

Prof. Dr. Barbara Di Martino
Dr. Federica Di Profio
Dr. Andrea Palombieri
Guest Editors

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Keywords

  • HEV
  • animals
  • humans
  • food
  • environment

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Published Papers (9 papers)

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Research

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11 pages, 1743 KiB  
Article
Changes in Hepatitis E Virus Contamination during the Production of Liver Sausage from Naturally Contaminated Pig Liver and the Potential of Individual Production Parameters to Reduce Hepatitis E Virus Contamination in the Processing Chain
by Jan Bernd Hinrichs, Antonia Kreitlow, Lisa Siekmann, Madeleine Plötz, Nicole Kemper and Amir Abdulmawjood
Pathogens 2024, 13(4), 274; https://doi.org/10.3390/pathogens13040274 - 23 Mar 2024
Cited by 1 | Viewed by 1571
Abstract
In this study, changes in hepatitis E virus (HEV) contamination in the production of liver sausage from naturally contaminated pork liver were investigated. Furthermore, the potential effectiveness of individual production parameters in reducing viral loads was measured. When processing moderately contaminated liver (initial [...] Read more.
In this study, changes in hepatitis E virus (HEV) contamination in the production of liver sausage from naturally contaminated pork liver were investigated. Furthermore, the potential effectiveness of individual production parameters in reducing viral loads was measured. When processing moderately contaminated liver (initial Cq-value 29), HEV RNA persisted in the finished sausages, even after heating for 90 min at 75 °C. A matrix-specific standard curve was created using a spiking experiment to accurately quantify HEV RNA in a particularly challenging matrix like liver sausage. Variations in product-specific production parameters, including mincing and heating times, showed some reduction in contamination levels, but even prolonged heating did not render all finished products HEV negative. The persistence of HEV contamination underscores the importance of ongoing monitoring in the pig population and raw materials to enhance food safety measures and reduce the likelihood of transmission through pork consumption. The detection of HEV RNA within all processing stages of pork liver in the production of liver sausage suggests that further research into the risk of infection posed by this detection and vigilance in managing HEV risks in the food chain, particularly in pork products, are required to protect public health. Full article
(This article belongs to the Special Issue Zoonotic Hepatitis E Virus: A Focus on Animals, Food and Environment)
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12 pages, 2042 KiB  
Article
Hepatitis E Virus (HEV): Identification of Subtypes 3b and 3m in Wild Boar Population in Liguria Region, Italy
by Roberta Battistini, Laura Serracca, Elisabetta Razzuoli, Valeria Listorti, Lisa Guardone, Monica Dellepiane, Nicola Pussini, Francesco Brunelli, Simone Peletto, Chiara Beltramo, Carlo Ercolini and Chiara Masotti
Pathogens 2022, 11(11), 1236; https://doi.org/10.3390/pathogens11111236 - 26 Oct 2022
Cited by 3 | Viewed by 1960
Abstract
The wild boar is an important natural reservoir for the zoonotic transmission of the hepatitis E virus (HEV) around the world. In particular, HEV genotypes 3 and 4 are an emerging problem in industrialized countries, as the number of wild boars has increased, [...] Read more.
The wild boar is an important natural reservoir for the zoonotic transmission of the hepatitis E virus (HEV) around the world. In particular, HEV genotypes 3 and 4 are an emerging problem in industrialized countries, as the number of wild boars has increased, and their territory is ever closer to farms and populated areas. This study describes the HEV prevalence and geographic circulation among wild boar populations in the Ligurian region (Italy) during the period 2019–2022. Liver samples from 849 wild boars were analyzed for HEV RNA using real-time RT-PCR; positive samples were then subjected to sequencing and phylogenetic analysis. Overall, 6.7% of the wild boars were positive for HEV RNA; however, in the last two years, the percentage of positive animals almost doubled. Phylogenetic analysis showed that wild boar HEV sequences belonged to genotype 3 and clustered within subtypes 3a and 3c, and, for the first time in Italy, subtypes 3b and 3m were identified. Interestingly, 13 sequences could not be assigned to a recognized subtype. Furthermore, the results showed different circulations of identified subtypes across the territory. These findings increase the knowledge of HEV-3 heterogeneity in Italy and describe the role of wild boars in maintaining an active viral circulation in the environment. Full article
(This article belongs to the Special Issue Zoonotic Hepatitis E Virus: A Focus on Animals, Food and Environment)
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6 pages, 250 KiB  
Communication
Serological, Virological Investigation and Hepatic Injury Evaluation for Hepatitis E Virus in Hunting Dogs
by Angelica Bernardini, Maria Irene Pacini, Niccolò Fonti, Mario Forzan, Veronica Marchetti and Maurizio Mazzei
Pathogens 2022, 11(10), 1123; https://doi.org/10.3390/pathogens11101123 - 29 Sep 2022
Cited by 6 | Viewed by 1935
Abstract
Hepatitis E virus (HEV) is a quasi-enveloped single-stranded positive-sense RNA virus belonging to the Orthohepevirus A genus within the Hepeviridae family. The most common transmission route of this virus is fecal–oral, although zoonotic transmission by contact with infected animals has also been described. [...] Read more.
Hepatitis E virus (HEV) is a quasi-enveloped single-stranded positive-sense RNA virus belonging to the Orthohepevirus A genus within the Hepeviridae family. The most common transmission route of this virus is fecal–oral, although zoonotic transmission by contact with infected animals has also been described. In this study, 80 sera and rectal swabs were collected from dogs during the 2019/2020 and 2020/2021 wild boar hunting season in Tuscany. All dogs were submitted for serological screening to detect the presence of anti-HEV antibodies. To evaluate the circulation of HEV, rectal swabs from both seropositive dogs and dogs living in the same kennels were examined by One-Step RT-qPCR. In addition, the presence of markers of hepatic damage in dogs’ sera was investigated. Results indicated the presence of anti-HEV antibodies in 4/80 subjects (5%). However, neither HEV RNA nor signs of hepatic damage were found. In conclusion, although HEV can stimulate a specific immuno-response in dogs, this species does not seem to play an important role in HEV epidemiology. Full article
(This article belongs to the Special Issue Zoonotic Hepatitis E Virus: A Focus on Animals, Food and Environment)
11 pages, 1515 KiB  
Article
Co-Circulation of Different Hepatitis E Virus Genotype 3 Subtypes in Pigs and Wild Boar in North-East Germany, 2019
by Grit Priemer, Filip Cierniak, Carola Wolf, Rainer G. Ulrich, Martin H. Groschup and Martin Eiden
Pathogens 2022, 11(7), 773; https://doi.org/10.3390/pathogens11070773 - 6 Jul 2022
Cited by 12 | Viewed by 2467
Abstract
Hepatitis E is a major cause of acute liver disease in humans worldwide. The infection is caused by hepatitis E virus (HEV) which is transmitted in Europe to humans primarily through zoonotic foodborne transmission from domestic pigs, wild boar, rabbits, and deer. HEV [...] Read more.
Hepatitis E is a major cause of acute liver disease in humans worldwide. The infection is caused by hepatitis E virus (HEV) which is transmitted in Europe to humans primarily through zoonotic foodborne transmission from domestic pigs, wild boar, rabbits, and deer. HEV belongs to the family Hepeviridae, and possesses a positive-sense, single stranded RNA genome. This agent usually causes an acute self-limited infection in humans, but in people with low immunity, e.g., immunosuppressive therapy or underlying liver diseases, the infection can evolve to chronicity and is able to induce a variety of extrahepatic manifestations. Pig and wild boar have been identified as the primary animal reservoir in Europe, and consumption of raw and undercooked pork is known to pose a potential risk of foodborne HEV infection. In this study, we analysed pig and wild boar liver, faeces, and muscle samples collected in 2019 in Mecklenburg-Western Pomerania, north-east Germany. A total of 393 animals of both species were investigated using quantitative real-time reverse transcription polymerase chain reaction (RT-qPCR), conventional nested RT-PCR and sequence analysis of amplification products. In 33 animals, HEV RNA was detected in liver and/or faeces. In one individual, viral RNA was detected in muscle tissue. Sequence analysis of a partial open reading frame 1 region demonstrated a broad variety of genotype 3 (HEV-3) subtypes. In conclusion, the study demonstrates a high, but varying prevalence of HEV RNA in swine populations in Mecklenburg-Western Pomerania. The associated risk of foodborne HEV infection needs the establishment of sustainable surveillance and treatment strategies at the interface between humans, animals, and the environment within a One Health framework. Full article
(This article belongs to the Special Issue Zoonotic Hepatitis E Virus: A Focus on Animals, Food and Environment)
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Review

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21 pages, 397 KiB  
Review
Is Hepatitis E Virus a Neglected or Emerging Pathogen in Egypt?
by Ibrahim M. Sayed and Sayed F. Abdelwahab
Pathogens 2022, 11(11), 1337; https://doi.org/10.3390/pathogens11111337 - 12 Nov 2022
Cited by 7 | Viewed by 2359
Abstract
Though Egypt ranks among the top countries for viral hepatitis and death-related liver disease, Hepatitis E virus (HEV) is a neglected pathogen. Living in villages and rural communities with low sanitation, use of underground well water and contact with animals are the main [...] Read more.
Though Egypt ranks among the top countries for viral hepatitis and death-related liver disease, Hepatitis E virus (HEV) is a neglected pathogen. Living in villages and rural communities with low sanitation, use of underground well water and contact with animals are the main risk factors for HEV infection. Domestic animals, especially ruminants and their edible products, are one source of infection. Contamination of water by either human or animal stools is the main route of infection. In addition, HEV either alone or in coinfection with other hepatotropic viruses has been recorded in Egyptian blood donors. HEV seropositivity among Egyptian villagers was 60–80%, especially in the first decade of life. Though HEV seropositivity is the highest among Egyptians, HEV infection is not routinely diagnosed in Egyptian hospitals. The initial manifestations of HEV among Egyptians is a subclinical infection, although progression to fulminant hepatic failure has been recorded. With the improvement in serological and molecular approaches and increasing research on HEV, it is becoming clear that HEV represents a threat for Egyptians and preventive measures should be considered to reduce the infection rate and possible complications Full article
(This article belongs to the Special Issue Zoonotic Hepatitis E Virus: A Focus on Animals, Food and Environment)
20 pages, 1750 KiB  
Review
Current Knowledge of Hepatitis E Virus (HEV) Epidemiology in Ruminants
by Federica Di Profio, Vittorio Sarchese, Andrea Palombieri, Paola Fruci, Gianvito Lanave, Serena Robetto, Vito Martella and Barbara Di Martino
Pathogens 2022, 11(10), 1124; https://doi.org/10.3390/pathogens11101124 - 29 Sep 2022
Cited by 16 | Viewed by 3484
Abstract
Hepatitis E virus (HEV) infection represents an emerging public health concern worldwide. In industrialized countries, increasing numbers of autochthonous cases of human HEV infection are caused by zoonotic transmission of genotypes 3 and 4, mainly through the consumption of contaminated raw or undercooked [...] Read more.
Hepatitis E virus (HEV) infection represents an emerging public health concern worldwide. In industrialized countries, increasing numbers of autochthonous cases of human HEV infection are caused by zoonotic transmission of genotypes 3 and 4, mainly through the consumption of contaminated raw or undercooked meat of infected pigs and wild boars, which are considered the main reservoirs of HEV. However, in the last few years, accumulating evidence seems to indicate that several other animals, including different ruminant species, may harbor HEV. Understanding the impact of HEV infection in ruminants and identifying the risk factors affecting transmission among animals and to humans is critical in order to determine their role in the epidemiological cycle of HEV. In this review, we provide a summary of current knowledge on HEV ecology in ruminants. A growing body of evidence has revealed that these animal species may be potential important hosts of HEV, raising concerns about the possible implications for public health. Full article
(This article belongs to the Special Issue Zoonotic Hepatitis E Virus: A Focus on Animals, Food and Environment)
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Other

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14 pages, 1629 KiB  
Systematic Review
Higher Risk of HEV Transmission and Exposure among Blood Donors in Europe and Asia in Comparison to North America: A Meta-Analysis
by Annika Wolski, Sven Pischke, Ann-Kathrin Ozga, Marylyn M. Addo and Thomas Horvatits
Pathogens 2023, 12(3), 425; https://doi.org/10.3390/pathogens12030425 - 8 Mar 2023
Cited by 8 | Viewed by 2373
Abstract
Background and aims: The increasing number of diagnosed hepatitis E virus (HEV) infections in Europe has led to the implementation of the testing of blood products in various countries. Many nations have not yet implemented such screening. To assess the need for HEV [...] Read more.
Background and aims: The increasing number of diagnosed hepatitis E virus (HEV) infections in Europe has led to the implementation of the testing of blood products in various countries. Many nations have not yet implemented such screening. To assess the need for HEV screening in blood products worldwide, we conducted a systematic review and meta-analysis assessing HEV RNA positivity and anti-HEV seroprevalence in blood donors. Methods: Studies reporting anti-HEV IgG/IgM or HEV RNA positivity rates among blood donors worldwide were identified via predefined search terms in PubMed and Scopus. Estimates were calculated by pooling study data with multivariable linear mixed-effects metaregression analysis. Results: A total of 157 (14%) of 1144 studies were included in the final analysis. The estimated HEV PCR positivity rate ranged from 0.01 to 0.14% worldwide, with strikingly higher rates in Asia (0.14%) and Europe (0.10%) in comparison to North America (0.01%). In line with this, anti-HEV IgG seroprevalence in North America (13%) was lower than that in Europe (19%). Conclusions: Our data demonstrate large regional differences regarding the risk of HEV exposure and blood-borne HEV transmission. Considering the cost–benefit ratio, this supports blood product screening in high endemic areas, such as Europe and Asia, in contrast to low endemic regions, such as the U.S. Full article
(This article belongs to the Special Issue Zoonotic Hepatitis E Virus: A Focus on Animals, Food and Environment)
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7 pages, 259 KiB  
Brief Report
Hepatitis E Virus Infection in Patients with Chronic Inflammatory Bowel Disease Treated with Immunosuppressive Therapy
by Ilias Kounis, Christophe Renou, Stephane Nahon, Frederic Heluwaert, Gilles Macaigne, Morgane Amil, Stephane Talom, Benedicte Lambare, Claire Charpignon, Thierry Paupard, Monica Stetiu, Marie Pierre Ripault, Armand Yamaga, Florent Ehrhard, Franck Audemar, Maria Carmen Ortiz Correro, David Zanditenas, Florence Skinazi, Helene Agostini, Audrey Coilly and Anne Marie Roque-Afonsoadd Show full author list remove Hide full author list
Pathogens 2023, 12(2), 332; https://doi.org/10.3390/pathogens12020332 - 15 Feb 2023
Cited by 2 | Viewed by 1774
Abstract
Background: Medical treatment of inflammatory bowel disease (IBD) has evolved significantly, and treatment with immunomodulators is recommended. These medications may alter the patient’s immune response and increase the risk of opportunistic infections. Our aim was to evaluate the prevalence and the incidence of [...] Read more.
Background: Medical treatment of inflammatory bowel disease (IBD) has evolved significantly, and treatment with immunomodulators is recommended. These medications may alter the patient’s immune response and increase the risk of opportunistic infections. Our aim was to evaluate the prevalence and the incidence of acute or chronic HEV infection in IBD patients under immunomodulatory treatment. Patients and Methods: We conducted a retrospective, multicenter, observational study between 2017 and 2018. IBD outpatients hospitalized for the infusion of immunomodulators were included in 16 French centers. During their daily hospitalization, blood samples were drawn for HEV serology (IgM and IgG) and HEV RNA detection. Results: A total of 488 patients were included, of which 327 (67%) patients had Crohn’s disease and 161 (33%) ulcerative colitis. HEV IgM was detected in 3 patients, but HEV RNA was undetectable in all patients. The HEV IgG seroprevalence rate was 14.2%. IgG-positive patients were older at sampling (p = 0.01) and IBD diagnosis (p = 0.03), had higher seafood consumption (p = 0.01) and higher doses of azathioprine (p = 0.03). Ileal and upper digestive tract involvement was more frequent in IgG-positive patients (p = 0.009), and ileocolic involvement was more frequent in IgG-negative patients (p = 0.01). Under multivariate analysis, age > 50 years [OR: 2.21 (1.26, to 3.85), p = 0.004] was associated with previous HEV infection. Conclusion: Systematic screening for HEV infection is not needed among IBD patients on immunomodulatory medications. However, in the event of abnormal liver test findings, HEV should be part of the classic diagnostic assessment. Full article
(This article belongs to the Special Issue Zoonotic Hepatitis E Virus: A Focus on Animals, Food and Environment)
12 pages, 1668 KiB  
Brief Report
Characterization of a Near Full-Length Hepatitis E Virus Genome of Subtype 3c Generated from Naturally Infected South African Backyard Pigs
by Ravendra P. Chauhan and Michelle L. Gordon
Pathogens 2022, 11(9), 1030; https://doi.org/10.3390/pathogens11091030 - 11 Sep 2022
Cited by 4 | Viewed by 2256
Abstract
Eight genotypes of the hepatitis E virus (Orthohepevirus A; HEV) designated HEV-1 to HEV-8 have been reported from various mammalian hosts. Notably, domestic pigs and wild boars are the natural reservoirs of HEV-3 and HEV-4 genotypes with zoonotic propensity. Since [...] Read more.
Eight genotypes of the hepatitis E virus (Orthohepevirus A; HEV) designated HEV-1 to HEV-8 have been reported from various mammalian hosts. Notably, domestic pigs and wild boars are the natural reservoirs of HEV-3 and HEV-4 genotypes with zoonotic propensity. Since HEV infection in domestic pigs is usually subclinical, it may remain undetected, facilitating zoonotic spillover of HEV to the exposed human populations. A previous study from our group in 2021, using deep sequencing of a pooled saliva sample, generated various swine enteric virus genomes, including a near full-length swine HEV genome (7040 nt; 97.7% genome coverage) from five-month-old grower pigs at a backyard pig farm in the uMgungundlovu District, KwaZulu-Natal, South Africa. In the present study, we describe the further characterization, including genotyping and subtyping of the swine HEV isolate using phylogenetics and ‘HEVnet Typing Tool’. Our analyses confirmed that the South African swine HEV genome characterized in this study belonged to HEV genotype 3 subtype 3c (HEV-3c). While HEV-3c infections in domestic pigs have been previously reported from Brazil, Germany, Italy, and the Netherlands, they only generated partial genome sequences of open reading frame 1 (ORF1) and/or ORF2. To our knowledge, this is the first near full-length swine HEV-3c genome generated from naturally infected domestic pigs (Sus scrofa domesticus) in South Africa. However, due to the gap in the information on the HEV-3c genome sequences in various geographical locations worldwide, including South Africa, the epidemiology of the South African swine HEV genome characterized in this study remains inconclusive. Molecular and genomic surveillance of HEV in domestic pig populations in South Africa would be useful to determine their prevalence, circulating subtypes, and zoonosis risk. Full article
(This article belongs to the Special Issue Zoonotic Hepatitis E Virus: A Focus on Animals, Food and Environment)
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