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Elois MA, Pavi CP, Jempierre YFSH, Pilati GVT, Zanchetta L, Grisard HBDS, García N, Rodríguez-Lázaro D, Fongaro G. Trends and Challenges in the Detection and Environmental Surveillance of the Hepatitis E Virus. Microorganisms 2025; 13:998. [PMID: 40431171 PMCID: PMC12114463 DOI: 10.3390/microorganisms13050998] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/07/2025] [Revised: 04/22/2025] [Accepted: 04/24/2025] [Indexed: 05/29/2025] Open
Abstract
The Hepatitis E virus (HEV) is responsible for causing Hepatitis E, a zoonotic disease that has emerged as a significant global health concern, accounting for about 20 million infections and 70,000 deaths annually. Although it is often recognized as a disease that is acute in low-income countries, HEV has also been recognized as a zoonotic disease in high-income countries. The zoonotic transmission requires flexible approaches to effectively monitor the virus, vectors, and reservoirs. However, the environmental monitoring of HEV presents additional challenges due to limitations in current detection methods, making it difficult to accurately assess the global prevalence of the virus. These challenges hinder efforts to fully understand the scope of the disease and to implement effective control measures. This review will explore these and other critical concerns, addressing gaps in HEV research and highlighting the need for improved strategies in the monitoring, prevention, and management of Hepatitis E using a One Health approach.
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Affiliation(s)
- Mariana Alves Elois
- Laboratory of Applied Virology, Department of Microbiology, Immunology and Parasitology, Federal University of Santa Catarina, Florianópolis 88040-900, Brazil; (M.A.E.); (C.P.P.); (Y.F.S.H.J.); (G.V.T.P.); (L.Z.); (H.B.d.S.G.); (G.F.)
- Microbiology Division, Faculty of Sciences, University of Burgos, 09001 Burgos, Spain
- Research Centre for Emerging Pathogens and Global Health, University of Burgos, 09001 Burgos, Spain
| | - Catielen Paula Pavi
- Laboratory of Applied Virology, Department of Microbiology, Immunology and Parasitology, Federal University of Santa Catarina, Florianópolis 88040-900, Brazil; (M.A.E.); (C.P.P.); (Y.F.S.H.J.); (G.V.T.P.); (L.Z.); (H.B.d.S.G.); (G.F.)
| | - Yasmin Ferreira Souza Hoffmann Jempierre
- Laboratory of Applied Virology, Department of Microbiology, Immunology and Parasitology, Federal University of Santa Catarina, Florianópolis 88040-900, Brazil; (M.A.E.); (C.P.P.); (Y.F.S.H.J.); (G.V.T.P.); (L.Z.); (H.B.d.S.G.); (G.F.)
| | - Giulia Von Tönnemann Pilati
- Laboratory of Applied Virology, Department of Microbiology, Immunology and Parasitology, Federal University of Santa Catarina, Florianópolis 88040-900, Brazil; (M.A.E.); (C.P.P.); (Y.F.S.H.J.); (G.V.T.P.); (L.Z.); (H.B.d.S.G.); (G.F.)
| | - Lucas Zanchetta
- Laboratory of Applied Virology, Department of Microbiology, Immunology and Parasitology, Federal University of Santa Catarina, Florianópolis 88040-900, Brazil; (M.A.E.); (C.P.P.); (Y.F.S.H.J.); (G.V.T.P.); (L.Z.); (H.B.d.S.G.); (G.F.)
| | - Henrique Borges da Silva Grisard
- Laboratory of Applied Virology, Department of Microbiology, Immunology and Parasitology, Federal University of Santa Catarina, Florianópolis 88040-900, Brazil; (M.A.E.); (C.P.P.); (Y.F.S.H.J.); (G.V.T.P.); (L.Z.); (H.B.d.S.G.); (G.F.)
| | - Nerea García
- Department of Animal Health, Complutense University of Madrid, 28040 Madrid, Spain;
- VISAVET Health Surveillance Centre, Complutense University of Madrid, 28040 Madrid, Spain
| | - David Rodríguez-Lázaro
- Microbiology Division, Faculty of Sciences, University of Burgos, 09001 Burgos, Spain
- Research Centre for Emerging Pathogens and Global Health, University of Burgos, 09001 Burgos, Spain
| | - Gislaine Fongaro
- Laboratory of Applied Virology, Department of Microbiology, Immunology and Parasitology, Federal University of Santa Catarina, Florianópolis 88040-900, Brazil; (M.A.E.); (C.P.P.); (Y.F.S.H.J.); (G.V.T.P.); (L.Z.); (H.B.d.S.G.); (G.F.)
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Pavlova A, Kocikova B, Dolinska MU, Jackova A. Hepatitis E Virus in the Role of an Emerging Food-Borne Pathogen. Microorganisms 2025; 13:885. [PMID: 40284721 PMCID: PMC12029509 DOI: 10.3390/microorganisms13040885] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/11/2025] [Revised: 04/04/2025] [Accepted: 04/07/2025] [Indexed: 04/29/2025] Open
Abstract
Viral hepatitis E represents an important global health problem caused by the hepatitis E virus (HEV). Cases of HEV infection are increasingly associated with food-borne transmissions after the consumption of raw or undercooked food products from infected animals in high-income regions. Although most cases of infection are asymptomatic, severe courses of infection have been reported in specific groups of people, predominantly among pregnant women and immunocompromised patients. The viral nucleic acid of HEV is increasingly being reported in food-producing animals and different products of an animal origin. Even though the incubation period for HEV infection is long, several direct epidemiological links between human cases and the consumption of HEV-contaminated meat and meat products have been described. In this article, we review the current knowledge on human HEV infections, HEV in different food-producing animals and products of an animal origin, as well as the accumulation and resistance to HEV in farm and slaughterhouse environments. We also provide preventive measures to help eliminate HEV from animals, the human population, and the environment.
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Affiliation(s)
| | | | | | - Anna Jackova
- Department of Epizootiology, Parasitology and Protection of One Health, University of Veterinary Medicine and Pharmacy in Kosice, Komenskeho 73, 041 81 Kosice, Slovakia; (A.P.); (B.K.); (M.U.D.)
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Baymakova MP, Konaktchieva M, Kunchev M, Popivanov G, Kundurzhiev T, Tsachev I, Mutafchiyski V. First Insight into the Seroprevalence of Hepatitis E Virus and Associated Risk Factors Among Liver Transplant Recipients from Bulgaria. Vector Borne Zoonotic Dis 2025; 25:303-313. [PMID: 39943906 DOI: 10.1089/vbz.2024.0101] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/19/2025] Open
Abstract
Introduction: Hepatitis E virus (HEV) infection is caused by viruses belonging to the Hepeviridae family. HEV infection can be self-limiting; however, extrahepatic manifestations may be present. The purpose of the current study was to establish the seroprevalence of HEV among Bulgarian liver transplant recipients (LTRs) and to identify associated risk factors. Materials & Methods: The present study was conducted between April 1, 2023, and October 30, 2023, at the Military Medical Academy, Sofia, Bulgaria. All serum samples were tested for anti-HEV IgG/IgM using HEV IgG/IgM enzyme-linked immunosorbent assay on Dia.Pro (Milan, Italy). Each participating LTR completed a detailed paper-based closed-ended questionnaire regarding the associated risk factors for HEV infection. Results: The study included 73 LTRs with a mean age of 47.0 ± 14.0 years. Anti-HEV IgG antibodies were detected in 25 LTRs (34.2%), including 20 males (37.7%) and 5 females (25%). All participants were HEV-IgM negative. HEV seropositivity rates were higher but not statistically significant in LTRs aged >60 years than in those aged <60 years (40% vs. 32.7%). A significant factor by logistic regression was "high level of education" (odds ratio [OR] = 2.917; p = 0.038). Conclusion: To the best of our knowledge, this is the first seroepidemiological HEV study among LTRs from Bulgaria that found a high seroprevalence (34.2%).
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Affiliation(s)
| | - Marina Konaktchieva
- Department of Gastroenterology and Hepatology, Military Medical Academy, Sofia, Bulgaria
| | - Metodi Kunchev
- Department of Virology, Military Medical Academy, Sofia, Bulgaria
| | - Georgi Popivanov
- Department of Surgery, Military Medical Academy, Sofia, Bulgaria
| | - Todor Kundurzhiev
- Department of Occupational Medicine, Faculty of Public Health, Medical University, Sofia, Bulgaria
| | - Ilia Tsachev
- Department of Microbiology, Infectious and Parasitic Diseases, Faculty of Veterinary Medicine, Trakia University, Stara Zagora, Bulgaria
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Santos-Silva S, Romalde JL, Bento JT, Cruz AVS, López-López P, Gonçalves HMR, Van der Poel WHM, Nascimento MSJ, Rivero-Juarez A, Mesquita JR. Serological and Molecular Survey of Hepatitis E Virus in Small Ruminants from Central Portugal. FOOD AND ENVIRONMENTAL VIROLOGY 2024; 16:516-524. [PMID: 39235492 PMCID: PMC11525313 DOI: 10.1007/s12560-024-09612-4] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Subscribe] [Scholar Register] [Received: 06/20/2024] [Accepted: 08/26/2024] [Indexed: 09/06/2024]
Abstract
Hepatitis E virus (HEV) is currently recognized as an emerging problem and a growing concern for public health in developed countries, with HEV infections mainly attributable to foodborne transmission of HEV-3. The zoonotic HEV genotype 3 infects a wide range of mammalian hosts, with swine considered as the primary host. This study investigates the occurrence of HEV among small ruminants in Portugal. The primary aim of the present research was to evaluate the circulation and the potential for HEV infection among sheep and goats. A total of 400 bile samples and 493 blood samples were collected from sheep and goats at a slaughterhouse in the center region of Portugal, between January 2022 and March 2023. The HEV RNA detection in bile samples was performed using a nested broad-spectrum RT-PCR targeting the ORF1 region. Serological analysis to detect anti-HEV antibodies was conducted using a commercial double-antigen sandwich multi-species ELISA. The HEV RNA was not detected in any bile samples using the nested broad-spectrum RT-PCR. Serological analysis revealed an overall HEV antibody seroprevalence of 2% (10/493, 95% CI: 0.98-3.70) among the small ruminants, namely 2.2% in goats and 2.0% in sheep. Curiously, no statistically significant association among the factors, age, sex and species and HEV seroprevalence was observed. Although HEV RNA was not detected in the bile of sheep and goats, this study the evidence of seroprevalence in these small ruminant species. Further research could provide additional insights into the factors influencing HEV transmission dynamics in small ruminants in Portugal and its potential implications for public health.
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Affiliation(s)
- Sérgio Santos-Silva
- School of Medicine and Biomedical Sciences (ICBAS), University of Porto, Porto, Portugal
| | - Jesús L Romalde
- Department of Microbiology and Parasitology, CIBUS-Faculty of Biology, Cross-Disciplinary Research Center in Environmental Technologies (CRETUS), Universidad de Santiago de Compostela, Santiago de Compostela, Spain
| | | | - Andreia V S Cruz
- School of Medicine and Biomedical Sciences (ICBAS), University of Porto, Porto, Portugal
| | - Pedro López-López
- Unit of Infectious Diseases, Clinical Virology and Zoonoses, Hospital Universitario Reina Sofia, Instituto Maimonides de Investigación Biomédica de Córdoba (IMIBIC), Universidad de Córdoba (UCO), Cordoba, Spain
- Center for Biomedical Research Network (CIBER) in Infectious Diseases, Health Institute Carlos III, Madrid, Spain
| | - Helena M R Gonçalves
- LAQV, REQUIMTE, Department of Chemistry and Biochemistry, Faculty of Sciences, University of Porto, Porto, Portugal
| | - Wim H M Van der Poel
- Quantitative Veterinary Epidemiology, Wageningen University, Wageningen, The Netherlands
- Department Virology & Molecular Biology, Wageningen Bioveterinary Research, Lelystad, The Netherlands
| | | | - António Rivero-Juarez
- Unit of Infectious Diseases, Clinical Virology and Zoonoses, Hospital Universitario Reina Sofia, Instituto Maimonides de Investigación Biomédica de Córdoba (IMIBIC), Universidad de Córdoba (UCO), Cordoba, Spain
- Center for Biomedical Research Network (CIBER) in Infectious Diseases, Health Institute Carlos III, Madrid, Spain
| | - João R Mesquita
- School of Medicine and Biomedical Sciences (ICBAS), University of Porto, Porto, Portugal.
- Epidemiology Research Unit (EPIUnit), Instituto de Saúde Pública da Universidade Do Porto, Porto, Portugal.
- Laboratory for Integrative and Translational Research in Population Health (ITR), Porto, Portugal.
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Blanda V, Giacchino I, Vaglica V, Milioto V, Migliore S, Di Bella S, Gucciardi F, Bongiorno C, Chiarenza G, Cardamone C, Mancuso I, Scatassa ML, Cannella V, Guercio A, Purpari G, Grippi F. Foodborne Pathogens Across Different Food Matrices in Sicily (Southern Italy). Pathogens 2024; 13:998. [PMID: 39599551 PMCID: PMC11597087 DOI: 10.3390/pathogens13110998] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/18/2024] [Revised: 11/12/2024] [Accepted: 11/12/2024] [Indexed: 11/29/2024] Open
Abstract
Foodborne diseases result from the consumption of foods contaminated with pathogens or their toxins and represent a serious public health problem worldwide. This study aimed to assess the presence of Rotavirus (RoV), Adenovirus (AdV), Norovirus (NoV), Hepatitis A and Hepatitis E viruses (HAV and HEV, respectively), Toxoplasma gondii, Coxiella burnetii and Leptospira spp. across various food matrices in Sicily. The analysis concerned 504 samples, including mussels, farmed meat, game meat, vegetables and bulk milk. Following appropriate pre-treatment, acid nucleic extraction was carried out and amplification of pathogen nucleic acids was carried out by molecular methods. The mussels tested positive for NoVs (3/51, 5.9%) and farm meat resulted positive for T. gondii (1/34, 2.9%). The game offal samples tested positive for HEV, which was detected in 17 out of 222 samples (7.7%), and T. gondii (18/318, 5.7%) and Leptospira spp. (2/318, 0.6%). The milk samples tested positive for C. burnetii (15/85, 17.6%), T. gondii (2/85, 2.4%) and Leptospira spp. (1/85, 1.2%). This study highlights the variability in the risk of contamination of different food matrices, confirming the importance of vigilance in the consumption of potentially contaminated food products.
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Affiliation(s)
| | | | | | | | | | - Santina Di Bella
- Istituto Zooprofilattico Sperimentale della Sicilia A. Mirri, Via G. Marinuzzi 3, 90129 Palermo, Italy; (V.B.); (I.G.); (V.V.); (V.M.); (S.M.); (C.B.); (G.C.); (C.C.); (I.M.); (M.L.S.); (V.C.); (A.G.); (G.P.); (F.G.)
| | - Francesca Gucciardi
- Istituto Zooprofilattico Sperimentale della Sicilia A. Mirri, Via G. Marinuzzi 3, 90129 Palermo, Italy; (V.B.); (I.G.); (V.V.); (V.M.); (S.M.); (C.B.); (G.C.); (C.C.); (I.M.); (M.L.S.); (V.C.); (A.G.); (G.P.); (F.G.)
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Gherlan GS. Rocahepevirus ratti: An underrecognised cause of acute hepatitis. World J Hepatol 2024; 16:1084-1090. [PMID: 39221102 PMCID: PMC11362906 DOI: 10.4254/wjh.v16.i8.1084] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/25/2024] [Revised: 07/25/2024] [Accepted: 07/30/2024] [Indexed: 08/21/2024] Open
Abstract
Zoonoses are responsible for many of all emerging infectious diseases as well as for those already established. Rocahepevirus ratti is a rat-originated virus related to the hepatitis E virus (Paslahepevirus balayani) but highly divergent genetically from this, with a high cross-species infection potential and zoonotic transmission. It can infect humans, leading to acute hepatitis, and is primarily transmitted through the consumption of contaminated water. Rocahepevirus ratti was first discovered in Germany in 2010. The first human case was described in 2017 in Hong Kong in an immune-compromised patient. The first case of chronic infection with Rocahepevirus ratti was described in 2023. A meta-analysis based on 38 studies published between 2000 and 2023 identified 21 cases in humans described up to this date and 489 infections in different animals. Raising awareness regarding this virus is essential, as there are probably many cases that remain undiagnosed, and the virus even has the ability to produce chronic infections in selected patients.
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Affiliation(s)
- George S Gherlan
- Department of Infectious Diseases, "Carol Davila" University of Medicine and Pharmacy, Bucharest 050474, Romania.
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Zahmanova G, Takova K, Lukov GL, Andonov A. Hepatitis E Virus in Domestic Ruminants and Virus Excretion in Milk-A Potential Source of Zoonotic HEV Infection. Viruses 2024; 16:684. [PMID: 38793568 PMCID: PMC11126035 DOI: 10.3390/v16050684] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/27/2024] [Revised: 04/21/2024] [Accepted: 04/23/2024] [Indexed: 05/26/2024] Open
Abstract
The hepatitis E virus is a serious health concern worldwide, with 20 million cases each year. Growing numbers of autochthonous HEV infections in industrialized nations are brought on via the zoonotic transmission of HEV genotypes 3 and 4. Pigs and wild boars are the main animal reservoirs of HEV and play the primary role in HEV transmission. Consumption of raw or undercooked pork meat and close contact with infected animals are the most common causes of hepatitis E infection in industrialized countries. However, during the past few years, mounting data describing HEV distribution has led experts to believe that additional animals, particularly domestic ruminant species (cow, goat, sheep, deer, buffalo, and yak), may also play a role in the spreading of HEV. Up to now, there have not been enough studies focused on HEV infections associated with animal milk and the impact that they could have on the epidemiology of HEV. This critical analysis discusses the role of domestic ruminants in zoonotic HEV transmissions. More specifically, we focus on concerns related to milk safety, the role of mixed farming in cross-species HEV infections, and what potential consequences these may have on public health.
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Affiliation(s)
- Gergana Zahmanova
- Department of Molecular Biology, University of Plovdiv, 4000 Plovdiv, Bulgaria
- Department of Technology Transfer and IP Management, Center of Plant Systems Biology and Biotechnology, 4000 Plovdiv, Bulgaria
| | - Katerina Takova
- Department of Molecular Biology, University of Plovdiv, 4000 Plovdiv, Bulgaria
| | - Georgi L. Lukov
- Faculty of Sciences, Brigham Young University–Hawaii, Laie, HI 96762, USA
| | - Anton Andonov
- Department of Medical Microbiology and Infectious Diseases, Max Rady College of Medicine, University of Manitoba, Winnipeg, MB R3T 2N2, Canada;
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Nombot-Yazenguet MPDM, Modiyinji AF, Tricou V, Manirakiza A, Njouom R, Komas NPJ. Investigating animal reservoirs for hepatitis E virus in Bangui, Central African Republic. PLoS One 2024; 19:e0300608. [PMID: 38489313 PMCID: PMC10942039 DOI: 10.1371/journal.pone.0300608] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/26/2023] [Accepted: 02/29/2024] [Indexed: 03/17/2024] Open
Abstract
BACKGROUND Hepatitis E virus (HEV) is a major cause of enterotropic viral hepatitis, a major public health problem in many developing countries. In Central African Republic (CAR), HEV genotypes 1, 2, and 3 have been found to have an impact on human health. However, data on HEV in animal reservoirs are still lacking for CAR. Here, we investigated the presence of HEV in farmed pigs and goats in Bangui, the capital city of CAR, using molecular methods. METHODOLOGY In a prospective study, fecal samples from 61 pigs and 39 goats from farms in five districts (2nd, 4th, 6th, 7th, 8th) of Bangui were collected and tested for HEV RNA by real-time RT-PCR. The samples were further analyzed by nested-PCR and sequenced to determine the genotype and subtype to which the virus belong. RESULTS In total, 22/100 (22.0%) feces samples were successfully amplified for HEV RNA by real time RT-PCR. All positive samples were from pigs (22/61; 36.1%), while all goat samples were negative (0/39). Twelve HEV RNA samples (12/22 or 54.5%) were successfully amplified by nested RT-PCR, and subsequently sequenced. Phylogenetic analysis revealed that the obtained sequences clustered with subtype 3h and were genetically related to the human HEV sequences from CAR. CONCLUSION This study confirms that pigs constitute an HEV reservoir, with genotype 3 being the major circulating strain. Further studies are needed to investigate other local reservoirs and to improve knowledge of the molecular epidemiology of HEV in CAR.
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Affiliation(s)
| | | | - Vianney Tricou
- Viral Hepatitis Laboratory, Institut Pasteur de Bangui, Bangui, Central African Republic
| | - Alexandre Manirakiza
- Epidemiological Service, Institut Pasteur de Bangui, Bangui, Central African Republic
| | - Richard Njouom
- Department of Virology, Centre Pasteur of Cameroon, Yaoundé, Cameroon
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Turlewicz-Podbielska H, Augustyniak A, Wojciechowski J, Pomorska-Mól M. Hepatitis E Virus in Livestock-Update on Its Epidemiology and Risk of Infection to Humans. Animals (Basel) 2023; 13:3239. [PMID: 37893962 PMCID: PMC10603682 DOI: 10.3390/ani13203239] [Citation(s) in RCA: 4] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/22/2023] [Revised: 10/09/2023] [Accepted: 10/16/2023] [Indexed: 10/29/2023] Open
Abstract
Hepatitis E virus (HEV) is a public health problem worldwide and an important food pathogen known for its zoonotic potential. Increasing numbers of infection cases with human HEV are caused by the zoonotic transmission of genotypes 3 and 4, mainly by consuming contaminated, undercooked or raw porcine meat. Pigs are the main reservoir of HEV. However, it should be noted that other animal species, such as cattle, sheep, goats, and rabbits, may also be a source of infection for humans. Due to the detection of HEV RNA in the milk and tissues of cattle, the consumption of infected uncooked milk and meat or offal from these species also poses a potential risk of zoonotic HEV infections. Poultry infected by avian HEV may also develop symptomatic disease, although avian HEV is not considered a zoonotic pathogen. HEV infection has a worldwide distribution with different prevalence rates depending on the affected animal species, sampling region, or breeding system.
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Affiliation(s)
- Hanna Turlewicz-Podbielska
- Department of Preclinical Sciences and Infectious Diseases, Poznan University of Life Sciences, Wolynska 35, 60-637 Poznan, Poland; (H.T.-P.); (A.A.)
| | - Agata Augustyniak
- Department of Preclinical Sciences and Infectious Diseases, Poznan University of Life Sciences, Wolynska 35, 60-637 Poznan, Poland; (H.T.-P.); (A.A.)
| | | | - Małgorzata Pomorska-Mól
- Department of Preclinical Sciences and Infectious Diseases, Poznan University of Life Sciences, Wolynska 35, 60-637 Poznan, Poland; (H.T.-P.); (A.A.)
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Monini M, Di Bartolo I, De Sabato L, Ianiro G, Agostinelli F, Ostanello F. Hepatitis E Virus (HEV) in Heavy Pigs in Slaughterhouses of Northern Italy: Investigation of Seroprevalence, Viraemia, and Faecal Shedding. Animals (Basel) 2023; 13:2942. [PMID: 37760342 PMCID: PMC10525452 DOI: 10.3390/ani13182942] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/08/2023] [Revised: 09/12/2023] [Accepted: 09/13/2023] [Indexed: 09/29/2023] Open
Abstract
Hepatitis E virus (HEV) is considered an emerging threat in Europe, owing to the increased number of human cases and the widespread presence of the virus in pigs at farms. Most cases in industrialized countries are caused by the zoonotic HEV-3 genotype. The main transmission route of HEV-3 in Europe is foodborne, through consumption of raw or undercooked liver pork and wild boar meat. Pigs become susceptible to HEV infection after the loss of maternal immunity, and the majority of adult pigs test positive for IgG anti-HEV antibodies. Nonetheless, HEV-infected pigs in terms of liver, faeces, and rarely blood are identified at slaughterhouses. The present study aimed to investigate the prevalence of HEV-positive batches of Italian heavy pigs at slaughterhouses, assessing the presence of animals still shedding HEV upon their arrival at the slaughterhouse by sampling faeces collected from the floor of the trucks used for their transport. The occurrence of viraemic animals and the seroprevalence of anti-HEV antibodies were also assessed. The results obtained indicated the presence of anti-HEV IgM (1.9%), and a high seroprevalence of anti-HEV total antibodies (IgG, IgM, IgA; 89.2%, n = 260). HEV RNA was not detected in either plasma or faecal samples. Nevertheless, seropositive animals were identified in all eight batches investigated, confirming the widespread exposure of pigs to HEV at both individual and farm levels. Future studies are needed to assess the factors associated with the risk of HEV presence on farms, with the aim to prevent virus introduction and spread within farms, thereby eliminating the risk at slaughterhouse.
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Affiliation(s)
- Marina Monini
- Department of Food Safety, Nutrition and Veterinary Public Health, Istituto Superiore di Sanità, Viale Regina Elena, 299, 00161 Rome, Italy; (M.M.); (L.D.S.); (G.I.); (F.A.)
| | - Ilaria Di Bartolo
- Department of Food Safety, Nutrition and Veterinary Public Health, Istituto Superiore di Sanità, Viale Regina Elena, 299, 00161 Rome, Italy; (M.M.); (L.D.S.); (G.I.); (F.A.)
| | - Luca De Sabato
- Department of Food Safety, Nutrition and Veterinary Public Health, Istituto Superiore di Sanità, Viale Regina Elena, 299, 00161 Rome, Italy; (M.M.); (L.D.S.); (G.I.); (F.A.)
| | - Giovanni Ianiro
- Department of Food Safety, Nutrition and Veterinary Public Health, Istituto Superiore di Sanità, Viale Regina Elena, 299, 00161 Rome, Italy; (M.M.); (L.D.S.); (G.I.); (F.A.)
| | - Francesca Agostinelli
- Department of Food Safety, Nutrition and Veterinary Public Health, Istituto Superiore di Sanità, Viale Regina Elena, 299, 00161 Rome, Italy; (M.M.); (L.D.S.); (G.I.); (F.A.)
| | - Fabio Ostanello
- Department of Veterinary Medical Sciences, University of Bologna, Via Tolara di Sopra, 50, Ozzano dell’Emilia, 40064 Bologna, Italy;
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Prpić J, Baymakova M. Hepatitis E Virus (HEV) Infection among Humans and Animals: Epidemiology, Clinical Characteristics, Treatment, and Prevention. Pathogens 2023; 12:931. [PMID: 37513778 PMCID: PMC10383665 DOI: 10.3390/pathogens12070931] [Citation(s) in RCA: 12] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/06/2023] [Accepted: 07/11/2023] [Indexed: 07/30/2023] Open
Abstract
The public health significance of hepatitis E is very important [...].
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Affiliation(s)
- Jelena Prpić
- Croatian Veterinary Institute, Savska Cesta 143, 10000 Zagreb, Croatia
| | - Magdalena Baymakova
- Department of Infectious Diseases, Military Medical Academy, 1606 Sofia, Bulgaria
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12
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Santos-Silva S, López-López P, Gonçalves HMR, Rivero-Juarez A, Van der Poel WHM, Nascimento MSJ, Mesquita JR. A Systematic Review and Meta-Analysis on Hepatitis E Virus Detection in Farmed Ruminants. Pathogens 2023; 12:550. [PMID: 37111437 PMCID: PMC10146180 DOI: 10.3390/pathogens12040550] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/16/2023] [Revised: 03/28/2023] [Accepted: 03/30/2023] [Indexed: 04/05/2023] Open
Abstract
Swine are widely recognized as the main reservoir of zoonotic HEV; however, a growing body of data on the HEV prevalence in farmed ruminants of different species also points to a potential route for HEV transmission through ruminants and ruminant products and by-products. Definite information on the zoonotic potential of ruminants is still absent or unclear, compelling the necessity for increasing knowledge on this. The aim of the current study was to analyze the state-of-the-art in this research topic and provide a summary of HEV detection and characterization in farmed ruminants. A total of 1567 papers were retrieved from four search databases that resulted in 35 eligible papers after application of exclusion/inclusion criteria. Studies on HEV in farmed ruminants were mainly based on the detection of HEV RNA and were reported in Africa (n = 1), America (n = 3), Asia (n = 18) and Europe (n = 13), and focused on a variety of ruminants species, namely cow, goat, sheep, deer, buffalo and yak. The overall pooled prevalence of HEV was 0.02% (0.01-0.03, 95% CI). The subgroup pooled prevalence of HEV RNA was 0.01% (0.00-0.02, 95% CI) in cow milk, stool, serum, liver, intestinal, bile, blood, spleen and rectal swab samples; 0.09% (0.02-0.18, 95% CI) in goat serum, bile, stool, milk, liver, rectal swab and blood samples; 0.01% (0.00-0.04, 95% CI) in sheep stool, serum, milk, blood and liver samples. Most of the HEV genotypes found in farmed ruminants belonged to the zoonotic HEV-3 (subtypes 3a, 3c) and HEV-4 (subtype 4d, 4h), with Rocahepevirus also found. The wide HEV circulation observed in different farmed ruminants raises concerns for the possibility of HEV transmission through products from infected ruminants and alerts for the potential zoonotic route for HEV in ruminant products, such as meat and dairy products. Also, contact exposure to infected farmed animals could be a risk factor. Further research should be conducted in order to understand the circulation of HEV in these animals and its zoonotic potential, as there is currently a lack of data on this topic.
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Affiliation(s)
- Sérgio Santos-Silva
- School of Medicine and Biomedical Sciences (ICBAS), University of Porto, 4050-313 Porto, Portugal;
| | - Pedro López-López
- Unit of Infectious Diseases, Hospital Universitario Reina Sofia, Clinical Virology and Zoonoses, Instituto Maimonides de Investigación Biomédica de Córdoba (IMIBIC), Universidad de Córdoba (UCO), 14004 Cordoba, Spain
- Center for Biomedical Research Network (CIBER) in Infectious Diseases, Health Institute Carlos III, 28220 Madrid, Spain
| | - Helena M. R. Gonçalves
- Biosensor NTech—Nanotechnology Services, Lda, Avenida da Liberdade, 249, 1º Andar, 1250-143 Lisboa, Portugal
- Porto School of Engineering, Rede de Química e Tecnologia—REQUIMTE, 4200-072 Porto, Portugal
| | - António Rivero-Juarez
- Unit of Infectious Diseases, Hospital Universitario Reina Sofia, Clinical Virology and Zoonoses, Instituto Maimonides de Investigación Biomédica de Córdoba (IMIBIC), Universidad de Córdoba (UCO), 14004 Cordoba, Spain
- Center for Biomedical Research Network (CIBER) in Infectious Diseases, Health Institute Carlos III, 28220 Madrid, Spain
| | - Wim H. M. Van der Poel
- Quantitative Veterinary Epidemiology, Wageningen University, 6708 PB Wageningen, The Netherlands
- Department Virology & Molecular Biology, Wageningen Bioveterinary Research, 8200 AB Lelystad, The Netherlands
| | | | - João R. Mesquita
- School of Medicine and Biomedical Sciences (ICBAS), University of Porto, 4050-313 Porto, Portugal;
- Epidemiology Research Unit (EPIUnit), Instituto de Saúde Pública da Universidade do Porto, 4050-600 Porto, Portugal
- Laboratory for Integrative and Translational Research in Population Health (ITR), 4050-600 Porto, Portugal
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13
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Al-Eitan L, Alnemri M, Alkhawaldeh M, Mihyar A. Rodent-borne viruses in the region of Middle East. Rev Med Virol 2023:e2440. [PMID: 36924105 DOI: 10.1002/rmv.2440] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/29/2022] [Revised: 02/22/2023] [Accepted: 03/02/2023] [Indexed: 03/18/2023]
Abstract
Rodents are one of the most abundant mammal species in the world. They form more than two-fifth of all mammal species and there are approximately 4600 existing rodent species. Rodents are capable of transmitting deadly diseases, especially those that are caused by viruses. Viruses and their consequences have plagued the world for the last two centuries, three pandemics occurred during the last century only. The Middle East is situated at the crossroads of Africa and Asia, along with the Mediterranean Sea and the Indian Ocean, its geographic importance is gained through the diversity of topographies, biosphere, as well as climate aspects that make the region vulnerable to host emerging diseases. Refugee crises also play a major role in expected epidemic outbreaks in the region. Public health has always been the most important priority, and our aim in this review is to raise awareness among public health organisations across the Middle East about the dangers of rodent borne diseases that have been reported or are suspected to be found in the region.
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Affiliation(s)
- Laith Al-Eitan
- Department of Biotechnology and Genetic Engineering, Jordan University of Science and Technology, Irbid, Jordan
| | - Malek Alnemri
- Department of Biotechnology and Genetic Engineering, Jordan University of Science and Technology, Irbid, Jordan
| | - Mishael Alkhawaldeh
- Department of Biotechnology and Genetic Engineering, Jordan University of Science and Technology, Irbid, Jordan
| | - Ahmad Mihyar
- Department of Biotechnology and Genetic Engineering, Jordan University of Science and Technology, Irbid, Jordan
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14
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Batmagnai E, Boldbaatar B, Sodbayasgalan A, Kato-Mori Y, Hagiwara K. Hepatitis E Virus (HEV) Spreads from Pigs and Sheep in Mongolia. Animals (Basel) 2023; 13:ani13050891. [PMID: 36899748 PMCID: PMC10000034 DOI: 10.3390/ani13050891] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/13/2023] [Revised: 02/26/2023] [Accepted: 02/27/2023] [Indexed: 03/05/2023] Open
Abstract
Hepatitis E is a viral infectious disease in pigs, wild boars, cows, deer, rabbits, camels, and humans as hosts caused by Paslahepevirus. Recently, it has been detected in a wide variety of animals including domestic small ruminants. Mongolia is a land of nomadic people living with livestock such as sheep, goats, and cattle. Due to how Mongolian lifestyles have changed, pork has become popular and swine diseases have emerged. Among them, Hepatitis E disease has become a zoonotic infectious disease that needs to be addressed. The HEV problem in pigs is that infected pigs excrete the virus without showing clinical symptoms and it spreads into the environment. We attempted to detect HEV RNA in sheep which had been raised in Mongolia for a long time, and those animals living together with pigs in the same region currently. We also conducted a longitudinal analysis of HEV infection in pigs in the same area and found that they were infected with HEV of the same genotype and cluster. In this study, we examined 400 feces and 120 livers (pigs and sheep) by RT-PCR in Töv Province, Mongolia. HEV detection in fecal samples was 2% (4/200) in sheep and 15% (30/200) in pigs. The results of ORF2 sequence analysis of the HEV RT-PCR-positive pigs and sheep confirmed genotype 4 in both animals. The results suggest that HEV infection is widespread in both pigs and sheep and that urgent measures to prevent infection are needed. This case study points to the changing nature of infectious diseases associated with livestock farming. It will be necessary to reconsider livestock husbandry and public health issues based on these cases.
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Affiliation(s)
- Enkhbaatar Batmagnai
- Laboratory of Virology, Institute of Veterinary Medicine, Mongolian University of Life Sciences, Ulaanbaatar 17024, Mongolia
| | - Bazartseren Boldbaatar
- Department of Infectious Diseases and Microbiology, School of Veterinary Medicine, Mongolian University of Life Sciences, Ulaanbaatar 17024, Mongolia
| | - Amarbayasgalan Sodbayasgalan
- Laboratory of Virology, Institute of Veterinary Medicine, Mongolian University of Life Sciences, Ulaanbaatar 17024, Mongolia
| | - Yuko Kato-Mori
- Graduate School of Science, Technology and Innovation, Kobe University, 7-1-49 Minatojima Minami-Machi, Chuo-ku, Kobe 650-0047, Japan
| | - Katsuro Hagiwara
- Department of Pathobiology, School of Veterinary Medicine, Rakuno Gakuen University, Hokkaido 069-8501, Japan
- Correspondence:
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15
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Animal reservoirs for hepatitis E virus within the Paslahepevirus genus. Vet Microbiol 2023; 278:109618. [PMID: 36640568 DOI: 10.1016/j.vetmic.2022.109618] [Citation(s) in RCA: 27] [Impact Index Per Article: 13.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/07/2022] [Revised: 11/23/2022] [Accepted: 12/03/2022] [Indexed: 12/14/2022]
Abstract
Hepatitis E virus (HEV) is responsible for acute hepatitis in humans. It is a single-stranded, positive-sense RNA virus that belongs to the Hepeviridae family. The majority of concerning HEV genotypes belong to the Paslahepevirus genus and are subsequently divided into eight genotypes. HEV genotypes 1 and 2 exclusively infect humans and primates while genotypes 3 and 4 infect both humans and other mammals. Whereas HEV genotypes 5 and 6 are isolated from wild boars and genotypes 7 and 8 were identified from camels in the United Arab Emirates and China, respectively. HEV mainly spreads from humans to humans via the fecal-oral route. However, some genotypes with the capability of zoonotic transmissions, such as 3 and 4 transmit from animals to humans through feces, direct contact, and ingestion of contaminated meat products. As we further continue to uncover novel HEV strains in various animal species, it is becoming clear that HEV has a broad host range. Therefore, understanding the potential animal reservoirs for this virus will allow for better risk management and risk mitigation of infection with HEV. In this review, we mainly focused on animal reservoirs for the members of the species Paslahepevirus balayani and provided a comprehensive list of the host animals identified to date.
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16
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Detection of Hepatitis E Virus Genotype 3 in Feces of Capybaras (Hydrochoeris hydrochaeris) in Brazil. Viruses 2023; 15:v15020335. [PMID: 36851548 PMCID: PMC9959927 DOI: 10.3390/v15020335] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/09/2023] [Revised: 01/18/2023] [Accepted: 01/19/2023] [Indexed: 01/26/2023] Open
Abstract
Hepatitis E virus (HEV) is an emerging zoonotic pathogen associated with relevant public health issues. The aim of this study was to investigate HEV presence in free-living capybaras inhabiting urban parks in São Paulo state, Brazil. Molecular characterization of HEV positive samples was undertaken to elucidate the genetic diversity of the virus in these animals. A total of 337 fecal samples were screened for HEV using RT-qPCR and further confirmed by conventional nested RT-PCR. HEV genotype and subtype were determined using Sanger and next-generation sequencing. HEV was detected in one specimen (0.3%) and assigned as HEV-3f. The IAL-HEV_921 HEV-3f strain showed a close relationship to European swine, wild boar and human strains (90.7-93.2% nt), suggesting an interspecies transmission. Molecular epidemiology of HEV is poorly investigated in Brazil; subtype 3f has been reported in swine. This is the first report of HEV detected in capybara stool samples worldwide.
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17
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Wang Y, Zhao C, Qi Y, Geng Y. Hepatitis E Virus. ADVANCES IN EXPERIMENTAL MEDICINE AND BIOLOGY 2023; 1417:1-13. [PMID: 37223855 DOI: 10.1007/978-981-99-1304-6_1] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 05/25/2023]
Abstract
Since the sequence of hepatitis E virus (HEV) was determined from a patient with enterically transmitted non-A, non-B hepatitis in 1989, similar sequences have been isolated from many different animals, including pigs, wild boars, deer, rabbits, bats, rats, chicken, and trout. All of these sequences have the same genomic organization, which contains open reading frames (ORFs) 1, 2, and 3, although their genomic sequences are variable. Some have proposed that they be classified as new family, Hepeviridae, which would be further divided into different genera and species according to their sequence variability. The size of these virus particles generally ranged from 27 to 34 nm. However, HEV virions produced in cell culture differ in structure from the viruses found in feces. Those from cell culture have a lipid envelope and either lack or have a little ORF3, whereas the viruses isolated from feces lack a lipid envelope but have ORF3 on their surfaces. Surprisingly, most of the secreted ORF2 proteins from both these sources are not associated with HEV RNA.
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Affiliation(s)
- Youchun Wang
- Institute of Medical Biology, Chinese Academy of Medical Science & Peking Union Medical College, Kunming, China.
| | - Chenyan Zhao
- Division of HIV/AIDS and Sex-Transmitted Virus Vaccines, National Institutes for Food and Drug Control, Beijing, China
| | - Ying Qi
- Division of HIV/AIDS and Sex-Transmitted Virus Vaccines, National Institutes for Food and Drug Control, Beijing, China
| | - Yansheng Geng
- Key Laboratory of Public Health Safety of Hebei Province, School of Public Health, Hebei University, Baoding, China
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18
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Sayed IM, Abdelwahab SF. Is Hepatitis E Virus a Neglected or Emerging Pathogen in Egypt? Pathogens 2022; 11:1337. [PMID: 36422589 PMCID: PMC9697431 DOI: 10.3390/pathogens11111337] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/11/2022] [Revised: 11/04/2022] [Accepted: 11/08/2022] [Indexed: 09/02/2023] Open
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 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.
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Affiliation(s)
- Ibrahim M. Sayed
- Department of Biomedical and Nutritional Sciences, University of Massachusetts Lowell, Lowell, MA 01854, USA
- Department of Medical Microbiology and Immunology, Faculty of Medicine, Assiut University, Assiut 71515, Egypt
| | - Sayed F. Abdelwahab
- Department of Pharmaceutics and Industrial Pharmacy, College of Pharmacy, Taif University, P.O. Box 11099, Taif 21944, Saudi Arabia
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19
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Sayed IM, Karam-Allah Ramadan H, Hafez MHR, Elkhawaga AA, El-Mokhtar MA. Hepatitis E virus (HEV) open reading frame 2: Role in pathogenesis and diagnosis in HEV infections. Rev Med Virol 2022; 32:e2401. [PMID: 36209386 DOI: 10.1002/rmv.2401] [Citation(s) in RCA: 7] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/27/2022] [Revised: 09/27/2022] [Accepted: 09/28/2022] [Indexed: 11/12/2022]
Abstract
Hepatitis E virus (HEV) infection occurs worldwide. The HEV genome includes three to four open reading frames (ORF1-4). ORF1 proteins are essential for viral replication, while the ORF3 protein is an ion channel involved in the exit of HEV from the infected cells. ORF2 proteins form the viral capsid required for HEV invasion and assembly. They also suppress interferon production and inhibit antibody-mediated neutralisation of HEV, allowing the virus to hijack the host immune response. ORF2 is the only detectable viral protein in the human liver during HEV infection and it is secreted in the plasma, stool, and urine of HEV-infected patients, making it a reliable diagnostic marker. The plasma HEV ORF2 antigen level can predict the outcome of HEV infections. Hence, monitoring HEV ORF2 antigen levels may be useful in assessing the efficacy of anti-HEV therapy. The ORF2 antigen is immunogenic and includes epitopes that can induce neutralising antibodies; therefore, it is a potential HEV vaccine candidate. In this review, we highlighted the different forms of HEV ORF2 protein and their roles in HEV pathogenesis, diagnosis, monitoring the therapeutic efficacy, and vaccine development.
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Affiliation(s)
- Ibrahim M Sayed
- Department of Medical Microbiology and Immunology, Faculty of Medicine, Assiut University, Assiut, Egypt
| | - Haidi Karam-Allah Ramadan
- Department of Tropical Medicine and Gastroenterology, Faculty of Medicine, Assiut University, Assiut, Egypt
| | - Mahmoud H R Hafez
- International Scholar, African Leadership Academy, Johannesburg, South Africa
| | - Amal A Elkhawaga
- Department of Medical Microbiology and Immunology, Faculty of Medicine, Assiut University, Assiut, Egypt
| | - Mohamed A El-Mokhtar
- Department of Medical Microbiology and Immunology, Faculty of Medicine, Assiut University, Assiut, Egypt.,Microbiology and Immunology Department, Faculty of Pharmacy, Sphinx University, Assiut, Egypt
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20
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Current Knowledge of Hepatitis E Virus (HEV) Epidemiology in Ruminants. Pathogens 2022; 11:pathogens11101124. [PMID: 36297181 PMCID: PMC9609093 DOI: 10.3390/pathogens11101124] [Citation(s) in RCA: 19] [Impact Index Per Article: 6.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/02/2022] [Revised: 09/26/2022] [Accepted: 09/27/2022] [Indexed: 12/20/2022] Open
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 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.
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21
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The first evidence of zoonotic hepatitis E virus (HEV) exposure in domestic cats in Türkiye. Comp Immunol Microbiol Infect Dis 2022; 86:101820. [DOI: 10.1016/j.cimid.2022.101820] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/19/2022] [Revised: 05/03/2022] [Accepted: 05/09/2022] [Indexed: 11/18/2022]
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22
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Caballero-Gómez J, García-Bocanegra I, Jiménez-Martín D, Cano-Terriza D, Risalde MA, López-López P, Jiménez-Ruiz S, Rivero A, Rivero-Juarez A. Epidemiological survey and risk factors associated with hepatitis E virus in small ruminants in southern Spain. Zoonoses Public Health 2022; 69:387-393. [PMID: 35244968 PMCID: PMC9311081 DOI: 10.1111/zph.12935] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/10/2022] [Revised: 02/21/2022] [Accepted: 02/23/2022] [Indexed: 12/21/2022]
Abstract
Autochthonous cases of hepatitis E (HE) associated with zoonotic genotypes HEV-3 and HEV-4 have significantly increased in industrialized countries over the last decade. Suidae are generally recognized as the main reservoirs of these genotypes. Susceptibility to HE virus (HEV) infection and zoonotic potential have also been confirmed in other species, including sheep and goat. However, the information about their role in the epidemiology of HEV remains very scarce. The objective of this study was to assess the prevalence, spatial distribution and risk factors associated with HEV exposure in sheep and goats in southern Spain, the country with the highest census of small domestic ruminants in the European Union. Blood samples from 240 sheep and 240 goats were collected between 2015 and 2017. Sera were analysed in parallel using a commercial double-antigen ELISA and real-time PCR. A total of 38 (7.9%; 95%CI: 5.5-10.3) out of 480 sampled animals showed anti-HEV antibodies. By species, the seroprevalences found in sheep and goats were 2.1% (5/240; 95%CI: 0.3-3.9) and 13.8% (33/240; 95%CI: 9.4-18.1) respectively. Anti-HEV antibodies were found on 19 (59.4%; 95%CI: 42.4-76.4) of the 32 sampled farms. The GEE model showed that species (goat) and number of small ruminants in the farm (≤348 animals and ≥538 animals) were risk factors potentially associated with HEV exposure in small ruminants in the study area. HEV RNA was not detected in any of the 480 (0.0%; 95%CI: 0.0-0.8) tested animals. Our results confirm that sheep and goats are naturally, but not equally exposed to HEV and indicate the widespread spatial distribution of HEV among small ruminant populations in southern Spain. Further studies are required to elucidate the role of sheep and goat in the epidemiology of HEV and their potential implications for public health.
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Affiliation(s)
- Javier Caballero-Gómez
- Grupo de Investigación en Sanidad Animal y Zoonosis (GISAZ), Departamento de Sanidad Animal, Facultad de Veterinaria, Universidad de Córdoba (UCO), Córdoba, Spain.,Grupo de Virología Clínica y Zoonosis, Unidad de Enfermedades Infecciosas, Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Hospital Universitario Reina Sofía, Universidad de Córdoba (UCO), Córdoba, Spain.,CIBERINFEC
| | - Ignacio García-Bocanegra
- Grupo de Investigación en Sanidad Animal y Zoonosis (GISAZ), Departamento de Sanidad Animal, Facultad de Veterinaria, Universidad de Córdoba (UCO), Córdoba, Spain.,CIBERINFEC
| | - Débora Jiménez-Martín
- Grupo de Investigación en Sanidad Animal y Zoonosis (GISAZ), Departamento de Sanidad Animal, Facultad de Veterinaria, Universidad de Córdoba (UCO), Córdoba, Spain
| | - David Cano-Terriza
- Grupo de Investigación en Sanidad Animal y Zoonosis (GISAZ), Departamento de Sanidad Animal, Facultad de Veterinaria, Universidad de Córdoba (UCO), Córdoba, Spain.,CIBERINFEC
| | - María A Risalde
- Grupo de Virología Clínica y Zoonosis, Unidad de Enfermedades Infecciosas, Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Hospital Universitario Reina Sofía, Universidad de Córdoba (UCO), Córdoba, Spain.,CIBERINFEC.,Grupo de Investigación en Sanidad Animal y Zoonosis (GISAZ), Departamento de Anatomía y Anatomía Patológica Comparadas y Toxicología, Facultad de Veterinaria, Universidad de Córdoba (UCO), Córdoba, Spain
| | - Pedro López-López
- Grupo de Virología Clínica y Zoonosis, Unidad de Enfermedades Infecciosas, Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Hospital Universitario Reina Sofía, Universidad de Córdoba (UCO), Córdoba, Spain.,CIBERINFEC
| | - Saúl Jiménez-Ruiz
- Grupo de Investigación en Sanidad Animal y Zoonosis (GISAZ), Departamento de Sanidad Animal, Facultad de Veterinaria, Universidad de Córdoba (UCO), Córdoba, Spain.,Health & Biotechnology (SaBio) Group, Instituto de Investigación en Recursos Cinegéticos (CSIC-UCLM-JCCM), Ciudad Real, Spain
| | - Antonio Rivero
- Grupo de Virología Clínica y Zoonosis, Unidad de Enfermedades Infecciosas, Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Hospital Universitario Reina Sofía, Universidad de Córdoba (UCO), Córdoba, Spain.,CIBERINFEC
| | - Antonio Rivero-Juarez
- Grupo de Virología Clínica y Zoonosis, Unidad de Enfermedades Infecciosas, Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Hospital Universitario Reina Sofía, Universidad de Córdoba (UCO), Córdoba, Spain.,CIBERINFEC
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23
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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 (Basel) 2021; 11:ani11123465. [PMID: 34944242 PMCID: PMC8698176 DOI: 10.3390/ani11123465] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/29/2021] [Revised: 11/26/2021] [Accepted: 12/03/2021] [Indexed: 12/27/2022] Open
Abstract
Hepatitis E virus (HEV) infection is a major health problem worldwide. In developed countries, zoonotic transmission of HEV genotypes (Gt) 3 and 4 is caused by the ingestion of raw or undercooked meat of infected pigs and wild boars, the main reservoirs of HEV. However, additional animals may harbour HEV or HEV-related strains, including carnivores. In this study, we investigated the molecular epidemiology of orthohepeviruses in wild canids by screening a total of 136 archival faecal samples, collected from wolves (42) and red foxes (94) in Northwestern Italy. Orthohepevirus RNA was identified in a faecal specimen, collected from a wolf carcass in the province of La Spezia (Liguria Region, Italy). The nearly full-length (7212 nucleotides) genome of the strain HEV/81236/Wolf/2019/ITA (GenBank accession no. MZ463196) was determined by combining a sequence-independent single-primer amplification (SISPA) approach with the Oxford Nanopore Technologies sequencing platform. Upon phylogenetic analysis, the HEV detected in wolf was segregated into clade HEV-3.1, displaying the highest nucleotide (nt) identity (89.0-93.3%) to Gt3 strains belonging to subtype c. Interestingly, the wolf faecal sample also contained porcine astrovirus sequences, endorsing the hypothesis of a dietary origin of the HEV strain due to preying habits.
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Affiliation(s)
- Vittorio Sarchese
- Faculty of Veterinary Medicine, Università degli Studi di Teramo, 64100 Teramo, Italy; (V.S.); (P.F.); (A.P.); (F.D.P.); (F.M.)
| | - Paola Fruci
- Faculty of Veterinary Medicine, Università degli Studi di Teramo, 64100 Teramo, Italy; (V.S.); (P.F.); (A.P.); (F.D.P.); (F.M.)
| | - Andrea Palombieri
- Faculty of Veterinary Medicine, Università degli Studi di Teramo, 64100 Teramo, Italy; (V.S.); (P.F.); (A.P.); (F.D.P.); (F.M.)
| | - Federica Di Profio
- Faculty of Veterinary Medicine, Università degli Studi di Teramo, 64100 Teramo, Italy; (V.S.); (P.F.); (A.P.); (F.D.P.); (F.M.)
| | - Serena Robetto
- Istituto Zooprofilattico Sperimentale del Piemonte, Liguria e Valle d’Aosta, Centro di Referenza Nazionale per le Malattie degli Animali Selvatici (CeRMAS), 11020 Aosta, Italy; (S.R.); (R.O.)
| | - Carlo Ercolini
- Istituto Zooprofilattico Sperimentale del Piemonte, Liguria e Valle d’Aosta, SC Liguria e Portualità Marittima, 19100 La Spezia, Italy;
| | - Riccardo Orusa
- Istituto Zooprofilattico Sperimentale del Piemonte, Liguria e Valle d’Aosta, Centro di Referenza Nazionale per le Malattie degli Animali Selvatici (CeRMAS), 11020 Aosta, Italy; (S.R.); (R.O.)
| | - Fulvio Marsilio
- Faculty of Veterinary Medicine, Università degli Studi di Teramo, 64100 Teramo, Italy; (V.S.); (P.F.); (A.P.); (F.D.P.); (F.M.)
| | - Vito Martella
- Department of Veterinary Medicine, Università Aldo Moro di Bari, 70121 Valenzano, Italy;
| | - Barbara Di Martino
- Faculty of Veterinary Medicine, Università degli Studi di Teramo, 64100 Teramo, Italy; (V.S.); (P.F.); (A.P.); (F.D.P.); (F.M.)
- Correspondence:
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Sayed IM, El-Mokhtar MA. Are ruminants and their products potential sources of human hepatitis E virus infection? Future Virol 2021. [DOI: 10.2217/fvl-2021-0188] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/19/2022]
Affiliation(s)
- Ibrahim M Sayed
- Department of Medical Microbiology & Immunology, Faculty of Medicine, Assiut University, Assiut, Egypt
- Department of Pathology, School of Medicine, University of California, San Diego, La Jolla, CA 92093, USA
| | - Mohamed A El-Mokhtar
- Department of Medical Microbiology & Immunology, Faculty of Medicine, Assiut University, Assiut, Egypt
- Microbiology and Immunology Department, Faculty of Pharmacy, Sphinx University, Assiut, Egypt
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Hepatitis E Outbreak in the Central Part of Italy Sustained by Multiple HEV Genotype 3 Strains, June-December 2019. Viruses 2021; 13:v13061159. [PMID: 34204376 PMCID: PMC8235070 DOI: 10.3390/v13061159] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/03/2021] [Revised: 06/11/2021] [Accepted: 06/14/2021] [Indexed: 12/20/2022] Open
Abstract
In European countries, autochthonous acute hepatitis E cases are caused by Hepatitis E Virus (HEV) genotype 3 and are usually observed as sporadic cases. In mid/late September 2019, a hepatitis E outbreak caused by HEV genotype 3 was recognized by detection of identical/highly similar HEV sequences in some hepatitis E cases from two Italian regions, Abruzzo and Lazio, with most cases from this latter region showing a link with Abruzzo. Overall, 47 cases of HEV infection were finally observed with onsets from 8 June 2019 to 6 December 2019; they represent a marked increase as compared with just a few cases in the same period of time in the past years and in the same areas. HEV sequencing was successful in 35 cases. The phylogenetic analysis of the viral sequences showed 30 of them grouped in three distinct molecular clusters, termed A, B, and C: strains in cluster A and B were of subtype 3e and strains in cluster C were of subtype 3f. No strains detected in Abruzzo in the past years clustered with the strains involved in the present outbreak. The outbreak curve showed partially overlapped temporal distribution of the three clusters. Analysis of collected epidemiological data identified pork products as the most likely source of the outbreak. Overall, the findings suggest that the outbreak might have been caused by newly and almost simultaneously introduced strains not previously circulating in this area, which are possibly harbored by pork products or live animals imported from outside Abruzzo. This possibility deserves further studies in this area in order to monitor the circulation of HEV in human cases as well as in pigs and wild boars.
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Capozza P, Decaro N, Beikpour F, Buonavoglia C, Martella V. Emerging Hepatotropic Viruses in Cats: A Brief Review. Viruses 2021; 13:v13061162. [PMID: 34204394 PMCID: PMC8233973 DOI: 10.3390/v13061162] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/27/2021] [Revised: 06/14/2021] [Accepted: 06/15/2021] [Indexed: 12/19/2022] Open
Abstract
The possible role of viruses in feline liver disease has long remained neglected. However, in 2018, an analogue of human hepatitis B virus was identified in cats. Moreover, antibodies for human hepatitis E have been detected consistently at various prevalence rates in cats. Although the correlation between these viruses and the liver injury in cats must be clarified, hepatotropic viruses might represent an increasing risk for feline and public health.
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Treagus S, Wright C, Baker-Austin C, Longdon B, Lowther J. The Foodborne Transmission of Hepatitis E Virus to Humans. FOOD AND ENVIRONMENTAL VIROLOGY 2021; 13:127-145. [PMID: 33738770 PMCID: PMC8116281 DOI: 10.1007/s12560-021-09461-5] [Citation(s) in RCA: 55] [Impact Index Per Article: 13.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 10/20/2020] [Accepted: 01/16/2021] [Indexed: 05/04/2023]
Abstract
Globally, Hepatitis E virus (HEV) causes over 20 million cases worldwide. HEV is an emerging and endemic pathogen within economically developed countries, chiefly resulting from infections with genotype 3 (G3) HEV. G3 HEV is known to be a zoonotic pathogen, with a broad host range. The primary source of HEV within more economically developed countries is considered to be pigs, and consumption of pork products is a significant risk factor and known transmission route for the virus to humans. However, other foods have also been implicated in the transmission of HEV to humans. This review consolidates the information available regarding transmission of HEV and looks to identify gaps where further research is required to better understand how HEV is transmitted to humans through food.
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Affiliation(s)
- Samantha Treagus
- Biosciences, College of Life and Environmental Sciences, University of Exeter, Penryn Campus, Penryn, Cornwall, UK.
- Centre for Environment Fisheries and Aquaculture Science, Barrack Road, Weymouth, Dorset, DT4 8UB, UK.
| | | | - Craig Baker-Austin
- Centre for Environment Fisheries and Aquaculture Science, Barrack Road, Weymouth, Dorset, DT4 8UB, UK
| | - Ben Longdon
- Biosciences, College of Life and Environmental Sciences, University of Exeter, Penryn Campus, Penryn, Cornwall, UK
| | - James Lowther
- Centre for Environment Fisheries and Aquaculture Science, Barrack Road, Weymouth, Dorset, DT4 8UB, UK
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Alvarado-Esquivel C, Gutierrez-Martinez VD, Ramirez-Valles EG, Sifuentes-Alvarez A. Hepatitis E Virus Infection and Butchers: A Case-Control Seroprevalence Study. Gastroenterology Res 2021; 14:96-103. [PMID: 34007351 PMCID: PMC8110237 DOI: 10.14740/gr1198] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/17/2019] [Accepted: 07/11/2019] [Indexed: 12/14/2022] Open
Abstract
Background Very few case-control studies to assess the risk of hepatitis E virus (HEV) infection in meat workers have been published. Therefore, we sought to determine: 1) the association of HEV IgG seropositivity and the occupation of butcher; and 2) the sociodemographic, work, clinical and behavioral characteristics of butchers associated with HEV exposure. Methods We performed a case-control seroprevalence study of 101 butchers (mean age: 38.50 ± 12.52 years) and 101 age-, gender- and residence-matched control subjects of the general population. Anti-HEV IgG antibodies were determined using a commercially available enzyme-linked immunoassay. Bivariate and regression analyses were used to assess the association between HEV seropositivity and characteristics of butchers. Results Anti-HEV IgG antibodies were found in 18 (17.8%) of the 101 butchers and in 14 (13.9%) of the 101 control subjects (odds ratio (OR): 1.34; 95% confidence interval (CI): 0.63 - 2.88; P = 0.44). Stratification by sex, age and area of residence (rural or urban) in cases and controls showed similar seroprevalences of HEV infection among groups. Bivariate analysis showed that HEV seroprevalence was associated with low education (up to 6 years), work place, seniority, eating while working, a history of raising farm animals and national trips. However, further analysis by logistic regression showed that only the variable of national trips was associated with HEV exposure (OR: 5.38; 95% CI: 1.02 - 28.16; P = 0.04). Concerning clinical characteristics of butchers, no association between HEV exposure and health status, history of surgery or blood transfusion was found. Conclusions Results from this first age-, gender- and residence-matched serosurvey of HEV infection in butchers in Mexico suggest that this population group does not have a higher risk for HEV infection than people from the general population. However, further studies to confirm the lack of association between HEV infection and the occupation of butcher are needed.
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Affiliation(s)
- Cosme Alvarado-Esquivel
- Biomedical Research Laboratory, Faculty of Medicine and Nutrition, Juarez University of Durango State, Avenida Universidad S/N, 34000 Durango, Dgo, Mexico
| | | | - Eda Guadalupe Ramirez-Valles
- Faculty of Chemical Sciences, Juarez University of Durango State, Avenida Veterinarias S/N, 34120 Durango, Dgo, Mexico
| | - Antonio Sifuentes-Alvarez
- Biomedical Research Laboratory, Faculty of Medicine and Nutrition, Juarez University of Durango State, Avenida Universidad S/N, 34000 Durango, Dgo, Mexico
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Seroprevalence of Hepatitis E Virus in Moose ( Alces alces), Reindeer ( Rangifer tarandus), Red Deer ( Cervus elaphus), Roe Deer ( Capreolus capreolus), and Muskoxen ( Ovibos moschatus) from Norway. Viruses 2021; 13:v13020224. [PMID: 33535675 PMCID: PMC7912786 DOI: 10.3390/v13020224] [Citation(s) in RCA: 13] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/21/2020] [Revised: 01/25/2021] [Accepted: 01/26/2021] [Indexed: 12/18/2022] Open
Abstract
Hepatitis E virus (HEV), a major cause of viral hepatitis worldwide, is considered an emerging foodborne zoonosis in Europe. Pigs (Sus scrofa domestica) and wild boars (S. scrofa) are recognized as important HEV reservoirs. Additionally, HEV infection and exposure have been described in cervids. In Norway, HEV has been identified in pigs and humans; however, little is known regarding its presence in wild ungulates in the country. We used a species-independent double-antigen sandwich ELISA to detect antibodies against HEV in the sera of 715 wild ungulates from Norway, including 164 moose (Alces alces), 186 wild Eurasian tundra reindeer (Rangifer tarandus tarandus), 177 red deer (Cervus elaphus), 86 European roe deer (Capreolus capreolus), and 102 muskoxen (Ovibos moschatus). The overall seroprevalence was 12.3% (88/715). Wild reindeer had the highest seropositivity (23.1%, 43/186), followed by moose (19.5%, 32/164), muskoxen (5.9%, 6/102), and red deer (4%, 7/177). All roe deer were negative. According to our results, HEV is circulating in wild ungulates in Norway. The high seroprevalence observed in wild reindeer and moose indicates that these species may be potential reservoirs of HEV. To the authors’ knowledge, this is the first report of HEV exposure in reindeer from Europe and in muskoxen worldwide.
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Modiyinji AF, Bigna JJ, Kenmoe S, Simo FBN, Amougou MA, Ndangang MS, Nola M, Njouom R. Epidemiology of hepatitis E virus infection in animals in Africa: a systematic review and meta-analysis. BMC Vet Res 2021; 17:50. [PMID: 33494758 PMCID: PMC7831161 DOI: 10.1186/s12917-021-02749-5] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/31/2019] [Accepted: 01/06/2021] [Indexed: 11/10/2022] Open
Abstract
BACKGROUND Hepatitis E virus (HEV) is a major cause of acute hepatitis in humans worldwide and have high burden in the resource-limited countries. Better knowledge of the epidemiology of hepatitis in animals in Africa can help to understand the epidemiology among humans. The objective of this study was to summarize the prevalence of HEV infection and distribution of HEV genotypes among animals in Africa. METHODS In this systematic review and meta-analysis, we comprehensively searched PubMed, EMBASE, African Journals Online, and Africa Index Medicus from January 1st, 2000 to March 22th, 2020 without any language restriction. We considered cross-sectional studies of HEV infection in animals in Africa. Study selection, data extraction, and methodological quality of included studies were done independently by two investigators. Prevalence data were pooled using the random-effects meta-analysis. This review was registered in PROSPERO, CRD42018087684. RESULTS Twenty-five studies (13 species and 6983 animals) were included. The prevalence (antibodies or ribonucleic acid [RNA]) of HEV infection in animals varied widely depending on biological markers of HEV infection measured: 23.4% (95% confidence interval; 12.0-37.2) for anti-HEV immunoglobulins G, 13.1% (3.1-28.3) for anti-HEV immunoglobulins M, and 1.8% (0.2-4.3) for RNA; with substantial heterogeneity. In subgroup analysis, the immunoglobulins G seroprevalence was higher among pigs 37.8% (13.9-65.4). The following HEV genotypes were reported in animals: Rat-HEV genotype 1 (rats and horses), HEV-3 (pigs), HEV-7 (dromedaries), and Bat hepeviruses (bats). CONCLUSIONS We found a high prevalence of HEV infection in animals in Africa and HEV genotypes close to that of humans. Some animals in Africa could be the reservoir of HEV, highlighting the need of molecular epidemiological studies for investigating zoonotic transmission.
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Affiliation(s)
- Abdou Fatawou Modiyinji
- Department of Virology, Centre Pasteur of Cameroon, Yaoundé, Cameroon
- Department of Biology and Animal Physiology, Faculty of Sciences, University of Yaoundé I, Yaoundé, Cameroon
| | - Jean Joel Bigna
- Department of Epidemiology and Public Health, Centre Pasteur of Cameroon, Yaoundé, Cameroon
- School of Public Health, Faculty of Medicine, University of Paris Sud, Le Kremlin-Bicêtre, France
| | - Sebastien Kenmoe
- Department of Virology, Centre Pasteur of Cameroon, Yaoundé, Cameroon
| | - Fredy Brice N. Simo
- Department of Virology, Centre Pasteur of Cameroon, Yaoundé, Cameroon
- Department of Epidemiology and Public Health, Centre Pasteur of Cameroon, Yaoundé, Cameroon
| | - Marie A. Amougou
- Department of Virology, Centre Pasteur of Cameroon, Yaoundé, Cameroon
- Department of Epidemiology and Public Health, Centre Pasteur of Cameroon, Yaoundé, Cameroon
| | - Marie S. Ndangang
- Department of Medical Information and Informatics, Rouen University Hospital, Rouen, France
| | - Moise Nola
- Department of Biology and Animal Physiology, Faculty of Sciences, University of Yaoundé I, Yaoundé, Cameroon
| | - Richard Njouom
- Department of Virology, Centre Pasteur of Cameroon, Yaoundé, Cameroon
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Dziedzinska R, Krzyzankova M, Bena M, Vasickova P. Evidence of Hepatitis E Virus in Goat and Sheep Milk. Viruses 2020; 12:v12121429. [PMID: 33322702 PMCID: PMC7763044 DOI: 10.3390/v12121429] [Citation(s) in RCA: 14] [Impact Index Per Article: 2.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/08/2020] [Revised: 12/08/2020] [Accepted: 12/10/2020] [Indexed: 12/25/2022] Open
Abstract
Hepatitis E virus (HEV) is the etiological agent behind hepatitis E infection. Domestic pigs and wild boars are the main animal reservoirs of HEV. Very few papers describe HEV infection in goats and sheep. As the data pertaining to the presence of HEV virus in the milk of small ruminants in Europe are lacking, the aim of this paper was to examine a representative number of milk samples from these animals. The detection of HEV genome (HEV RNA) was performed using reverse transcriptase real-time polymerase chain reaction (RT-qPCR). HEV RNA was found in 2.8% of the examined samples. Positivity ranged from 101 to 103 genome equivalents/mL (GE/mL) with a median of 9.99 × 102 GE/mL. On the basis of these results, the milk of small ruminants could represent a source of HEV infection to consumers.
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Surveillance Study of Hepatitis E Virus (HEV) in Domestic and Wild Ruminants in Northwestern Italy. Animals (Basel) 2020; 10:ani10122351. [PMID: 33317114 PMCID: PMC7764585 DOI: 10.3390/ani10122351] [Citation(s) in RCA: 20] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/18/2020] [Revised: 12/06/2020] [Accepted: 12/08/2020] [Indexed: 02/07/2023] Open
Abstract
Simple Summary Hepatitis E virus (HEV) infection can cause both acute and chronic hepatitis in humans and represents an emerging public health concern worldwide. In developed countries, zoonotic transmission of HEV genotypes 3 and 4 is caused by ingestion of raw or undercooked meat of infected swine or wild boars, the main reservoirs of HEV. However, in the last few years, molecular and serological evidence seem to indicate that several other animal species may act as HEV host, including domestic and wild ruminants. In this study, serum and fecal specimens from sheep, goats, red deer, roe deer, chamois, and Alpine ibex collected in two northwestern Italian regions (Piemonte and Valle d’Aosta) were screened molecularly and serologically. With the exception of chamois, HEV antibodies were found both in the domestic and wild ruminant species investigated with the highest rates in sheep and goats. These findings demonstrate that wild also domestic ruminants may be implicated in the viral cycle transmission. Abstract In industrialized countries, increasing autochthonous infections of hepatitis E virus (HEV) are caused by zoonotic transmission of genotypes (Gts) 3 and 4, mainly through consumption of contaminated raw or undercooked pork meat. Although swine and wild boar are recognized as the main reservoir for Gt3 and Gt4, accumulating evidence indicates that other animal species, including domestic and wild ruminants, may harbor HEV. Herein, we screened molecularly and serologically serum and fecal samples from two domestic and four wild ruminant species collected in Valle d’Aosta and Piemonte regions (northwestern Italy. HEV antibodies were found in sheep (21.6%), goats (11.4%), red deer (2.6%), roe deer (3.1%), and in Alpine ibex (6.3%). Molecular screening was performed using different primer sets targeting highly conserved regions of hepeviruses and HEV RNA, although at low viral loads, was detected in four fecal specimens (3.0%, 4/134) collected from two HEV seropositive sheep herds. Taken together, the data obtained document the circulation of HEV in the geographical area assessed both in wild and domestic ruminants, but with the highest seroprevalence in sheep and goats. Consistently with results from other studies conducted in southern Italy, circulation of HEV among small domestic ruminants seems to occur more frequently than expected.
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El-Mokhtar MA, Elkhawaga AA, Sayed IM. Assessment of hepatitis E virus (HEV) in the edible goat products pointed out a risk for human infection in Upper Egypt. Int J Food Microbiol 2020; 330:108784. [PMID: 32659521 DOI: 10.1016/j.ijfoodmicro.2020.108784] [Citation(s) in RCA: 29] [Impact Index Per Article: 5.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/08/2020] [Revised: 06/24/2020] [Accepted: 07/01/2020] [Indexed: 02/06/2023]
Abstract
Hepatitis E virus (HEV) infection is endemic in developed and developing countries. Although the seroprevalence of HEV among the Egyptians is high, the sources of HEV infection in Egypt are not completely identified. Zoonotic HEV transmission among Egyptians is underestimated. Recently, we detected HEV in the milk of cows, this suggests the possibility of HEV transmission through the ingestion of contaminated milk. However, the role of small ruminants especially the goats in HEV epidemiology in Egypt remains unclear. Herein, we screened HEV markers in the edible goat products, mainly the milk and liver and we assessed the risk factor for HEV infection to the goat owners. A total of 280 goat milk samples were collected from 15 villages in the Assiut governorate. Anti-HEV IgG and HEV Ag were detected in 7.14% and 1.8% of the samples, respectively. HEV RNA was detected in 2 milk samples, cladogram analysis revealed that the isolated viruses belonged to HEV-3 subtype 3a. One viral isolate showed high homology to HEV recently isolated from the cow milk in the same geographic area. The level of anti-HEV IgG and HEV Ag were comparable in the milk and matched blood samples. While the urine and stool of HEV seropositive goats tested negative for HEV markers. HEV RNA was also detectable in the fresh goat liver samples (n = 2) derived from HEV seropositive goats. Finally, we analyzed HEV seroprevalence in households (n = 5) that owned the seropositive goats and households (n = 5) that owned the seronegative goats. Interestingly, anti-HEV IgG was recorded in 80% of households owned and frequently consumed the products of HEV seropositive goats, while HEV markers were not detectable in the owners of the seronegative goats. In conclusion: Here, we report HEV in the milk and liver of goats distributed in the villages of Assiut governorate. Higher HEV seroprevalence was recorded in the households that owned the seropositive goats. Investigation of the goat products is pivotal to assess the risk factor of HEV transmission to villagers in the Assiut governorate.
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Affiliation(s)
- Mohamed A El-Mokhtar
- Department of Medical Microbiology and Immunology, Faculty of Medicine, Assiut University, Assiut, Egypt
| | - Amal A Elkhawaga
- Department of Medical Microbiology and Immunology, Faculty of Medicine, Assiut University, Assiut, Egypt
| | - Ibrahim M Sayed
- Department of Medical Microbiology and Immunology, Faculty of Medicine, Assiut University, Assiut, Egypt; Department of Pathology, School of Medicine, University of California, San Diego, La Jolla, CA, USA.
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Obaidat MM, Roess AA. Individual animal and herd level seroprevalence and risk factors of Hepatitis E in ruminants in Jordan. INFECTION GENETICS AND EVOLUTION 2020; 81:104276. [PMID: 32147473 DOI: 10.1016/j.meegid.2020.104276] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 12/25/2019] [Revised: 03/03/2020] [Accepted: 03/04/2020] [Indexed: 01/09/2023]
Abstract
OBJECTIVES Hepatitis E virus (HEV) is zoonotic and endemic in several countries. There are no data on the farm level-prevalence and risk factors of HEV in ruminant farms in Jordan or elsewhere. This study aimed to estimate the seroprevalence and risk factors of HEV in ruminant farms in all regions of Jordan. MATERIAL AND METHODS A total of 460 apparently healthy ruminants from 115 (31 cow, 51 sheep and 33 goat) farms were tested for HEV antibodies using a double antigen sandwich enzyme linked immunosorbent test. A validated questionnaire was used to collect data on animal health and husbandry practices. RESULTS The results showed that 37.4% of the dairy farms under study (51.6%, 37.2% and 24.2% of dairy cow, sheep and goat farms; respectively) had at least one HEV seropositive animal. At the individual animal level, 12.1% of the tested animals were HEV positive; 14.5% (n = 18), 12.7% (n = 26) and 8.3% (n = 11) of cows, sheep and goats; respectively. Infrequent cleaning of feeders was associated with a significantly greater odds of HEV seropositivity in both large and small dairy ruminant farms (AOR = 16.0, p-val = 0.03, AOR = 3.4, p-val = 0.02, respectively). Farms which reported that small ruminants (sheep and goats) were mixed together had a greater odds of farm-level HEV seroprevalence (AOR = 3.1, p-val = 0.04). CONCLUSIONS This study shows widespread and high farm-level HEV seroprevalence in dairy farms in Jordan. Husbandry practices and off-abattoir carcass processing in Jordan could amplify emergence and transmission of zoonotic HEV. Future studies should include HEV genotyping in ruminants, their products and humans to better understand HEV epidemiology in Jordan.
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Affiliation(s)
- Mohammad M Obaidat
- Department of Veterinary Pathology and Public Health, Faculty of Veterinary Medicine, Jordan University of Science and Technology, Irbid, Jordan.
| | - Amira A Roess
- Department of Global Health, Milken Institute School of Public Health, George Washington University, Washington, DC, USA; Department of Global and Community Health, College of Health and Human Services, George Mason University, Fairfax, VA, USA
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Di Profio F, Melegari I, Palombieri A, Sarchese V, Arbuatti A, Fruci P, Marsilio F, Martella V, Di Martino B. High prevalence of hepatitis E virus in raw sewage in Southern Italy. Virus Res 2019; 272:197710. [PMID: 31415790 DOI: 10.1016/j.virusres.2019.197710] [Citation(s) in RCA: 22] [Impact Index Per Article: 3.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/12/2019] [Revised: 08/09/2019] [Accepted: 08/09/2019] [Indexed: 12/27/2022]
Abstract
Hepatitis E virus (HEV) infections constitute a significant health problem worldwide. The burden of hepatitis E in Italy seems low when compared with other European countries. In recent years, improved surveillance activities in Italy have revealed marked geographical differences in HEV epidemiology, with some regions characterised by higher seroprevalence rates. Abruzzo Region (Southern Italy) is currently recognised as a high-risk area for HEV infection. In this study, we investigated the epidemiology of HEV in Teramo Province by monitoring four wastewater treatment plants (WWTPs). Out of 56 influent sewage specimens collected during 2016-2017, HEV RNA was detected in 13/56 (23.2%) sewage samples from all the four WWTPs. Upon sequence analysis of the partial ORF2 gene, four strains showed the highest nucleotide identity to Gt3 subtype c, being more closely related to other HEVs previously identified in human and animal hosts in Abruzzo. For one strain, sequence data were generated only for a short region of the ORF1 gene, revealing the highest identity to HEVs Gt3 of subtype f. Altogether, the findings of this study confirm that HEV largely circulates in the setting investigated.
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Affiliation(s)
| | - Irene Melegari
- Faculty of Veterinary Medicine, Università degli Studi di Teramo, Italy
| | - Andrea Palombieri
- Faculty of Veterinary Medicine, Università degli Studi di Teramo, Italy
| | - Vittorio Sarchese
- Faculty of Veterinary Medicine, Università degli Studi di Teramo, Italy
| | - Alessio Arbuatti
- Faculty of Veterinary Medicine, Università degli Studi di Teramo, Italy
| | - Paola Fruci
- Faculty of Veterinary Medicine, Università degli Studi di Teramo, Italy
| | - Fulvio Marsilio
- Faculty of Veterinary Medicine, Università degli Studi di Teramo, Italy
| | - Vito Martella
- Department of Veterinary Medicine, Università Aldo Moro di Bari, Valenzano, Italy
| | - Barbara Di Martino
- Faculty of Veterinary Medicine, Università degli Studi di Teramo, Italy.
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Primadharsini PP, Nagashima S, Okamoto H. Genetic Variability and Evolution of Hepatitis E Virus. Viruses 2019; 11:E456. [PMID: 31109076 PMCID: PMC6563261 DOI: 10.3390/v11050456] [Citation(s) in RCA: 80] [Impact Index Per Article: 13.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/26/2019] [Revised: 05/15/2019] [Accepted: 05/16/2019] [Indexed: 12/16/2022] Open
Abstract
Hepatitis E virus (HEV) is a single-stranded positive-sense RNA virus. HEV can cause both acute and chronic hepatitis, with the latter usually occurring in immunocompromised patients. Modes of transmission range from the classic fecal-oral route or zoonotic route, to relatively recently recognized but increasingly common routes, such as via the transfusion of blood products or organ transplantation. Extrahepatic manifestations, such as neurological, kidney and hematological abnormalities, have been documented in some limited cases, typically in patients with immune suppression. HEV has demonstrated extensive genomic diversity and a variety of HEV strains have been identified worldwide from human populations as well as growing numbers of animal species. The genetic variability and constant evolution of HEV contribute to its physiopathogenesis and adaptation to new hosts. This review describes the recent classification of the Hepeviridae family, global genotype distribution, clinical significance of HEV genotype and genomic variability and evolution of HEV.
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Affiliation(s)
- Putu Prathiwi Primadharsini
- Division of Virology, Department of Infection and Immunity, Jichi Medical University School of Medicine, Tochigi 329-0498, Japan.
| | - Shigeo Nagashima
- Division of Virology, Department of Infection and Immunity, Jichi Medical University School of Medicine, Tochigi 329-0498, Japan.
| | - Hiroaki Okamoto
- Division of Virology, Department of Infection and Immunity, Jichi Medical University School of Medicine, Tochigi 329-0498, Japan.
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The Current Host Range of Hepatitis E Viruses. Viruses 2019; 11:v11050452. [PMID: 31108942 PMCID: PMC6563279 DOI: 10.3390/v11050452] [Citation(s) in RCA: 68] [Impact Index Per Article: 11.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/24/2019] [Revised: 05/08/2019] [Accepted: 05/14/2019] [Indexed: 01/01/2023] Open
Abstract
Hepatitis E virus (HEV) is an emerging zoonotic pathogen transmitting both human to human via the fecal oral route and from animals to humans through feces, direct contact, and consumption of contaminated meat products. Understanding the host range of the virus is critical for determining where potential threats to human health may be emerging from and where potential reservoirs for viral persistence in the environment may be hiding. Initially thought to be a human specific disease endemic to developing countries, the identification of swine as a primary host for genotypes 3 and 4 HEV in industrialized countries has begun a long journey of discovering novel strains of HEV and their animal hosts. As we continue identifying new strains of HEV in disparate animal species, it is becoming abundantly clear that HEV has a broad host range and many of these HEV strains can cross between differing animal species. These cross-species transmitting strains pose many unique challenges to human health as they are often unrecognized as sources of viral transmission.
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Transmission of a Novel Genotype of Hepatitis E Virus from Bactrian Camels to Cynomolgus Macaques. J Virol 2019; 93:JVI.02014-18. [PMID: 30700602 DOI: 10.1128/jvi.02014-18] [Citation(s) in RCA: 54] [Impact Index Per Article: 9.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/20/2018] [Accepted: 01/18/2019] [Indexed: 12/15/2022] Open
Abstract
Hepatitis E virus (HEV) is zoonotic and a major cause of acute viral hepatitis worldwide. Recently, we identified a novel HEV genotype 8 (HEV8) in Bactrian camels in Xinjiang, China. However, the epidemiology, pathogenicity, and zoonotic potential of HEV8 are unclear. Here, we present the prevalence of HEV8 in China and investigate its pathogenicity and cross-species transmission in cynomolgus macaques. Fresh fecal and milk samples from Bactrian camels collected from four provinces/regions in China were screened for HEV RNA by reverse transcriptase PCR (RT-PCR). An HEV8-positive sample was used to inoculate two cynomolgus macaques to examine the potential for cross-species infection. The pathogenicity of HEV8 was analyzed by testing HEV markers and liver function during the study period and histopathology of liver biopsy specimens at 3, 13, and 25 weeks postinoculation. Extrahepatic replication was tested by using reverse transcriptase quantitative PCR (RT-qPCR) and immunofluorescence assays. The overall prevalence of HEV8 RNA in Chinese Bactrian camels was 1.4% (4/295), and positive samples were found in three different provinces/regions in China. Histopathology confirmed acute and chronic HEV8 infections in the two monkeys. Multiple tissues were positive for HEV RNA and ORF2 proteins. Renal pathology was observed in the monkey with chronic hepatitis. Whole-genome sequencing showed only 1 to 3 mutations in the HEV8 in the fecal samples from the two monkeys compared to that from the camel. HEV8 is circulating in multiple regions in China. Infection of two monkeys with HEV8 induced chronic and systemic infections, demonstrating the high potential zoonotic risk of HEV8.IMPORTANCE It is estimated that one-third of the world population have been exposed to hepatitis E virus (HEV). In developed countries and China, zoonotic HEV strains are responsible for almost all acute and chronic HEV infection cases. It is always of immediate interest to investigate the zoonotic potential of novel HEV strains. In 2016, we discovered a novel HEV genotype, HEV8, in Bactrian camels, but the epidemiology, zoonotic potential, and pathogenicity of the virus were unknown. In the present study, we demonstrated that HEV8 was circulating in multiple regions in China and was capable of infecting cynomolgus macaques, a surrogate for humans, posing high risk of zoonosis. Chronic hepatitis, systemic infection, and renal pathology were observed. Collectively, these data indicate that HEV8 exhibits a high potential for zoonotic transmission. Considering the importance of Bactrian camels as livestock animals, risk groups, such as camelid meat and milk consumers, should be screened for HEV8 infection.
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Sarchese V, Di Profio F, Melegari I, Palombieri A, Sanchez SB, Arbuatti A, Ciuffetelli M, Marsilio F, Martella V, Di Martino B. Hepatitis E virus in sheep in Italy. Transbound Emerg Dis 2019; 66:1120-1125. [PMID: 30811818 DOI: 10.1111/tbed.13157] [Citation(s) in RCA: 37] [Impact Index Per Article: 6.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/10/2018] [Revised: 02/21/2019] [Accepted: 02/22/2019] [Indexed: 11/30/2022]
Abstract
Hepatitis E virus (HEV) is the leading cause of human enterically transmitted viral hepatitis occurring around the world both as outbreaks and as sporadic cases. The accumulating 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. In this study, the role of sheep as potential host of hepatitis E virus (HEV) was investigated. By screening 192 sheep from seven farms located in Abruzzo Region (Southern Italy), HEV-specific antibodies were detected in the sera of 41 animals (21.3%) whilst the RNA of HEV, genotype 3, was detected in 20 faecal (10.4%) and three serum samples (1.6%). Upon sequence analyses of a partial ORF2 gene region of eight HEV positive samples, the sheep sequences all grouped together within HEV genotype 3 subtype c, being most closely related to HEV strains identified in goat and wild boar from Abruzzo. This is the first study that demonstrates, serologically and molecularly, the presence of HEV in sheep population in a European country.
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Affiliation(s)
- Vittorio Sarchese
- Faculty of Veterinary Medicine, Università degli Studi di Teramo, Teramo, Italy
| | - Federica Di Profio
- Faculty of Veterinary Medicine, Università degli Studi di Teramo, Teramo, Italy
| | - Irene Melegari
- Faculty of Veterinary Medicine, Università degli Studi di Teramo, Teramo, Italy
| | - Andrea Palombieri
- Faculty of Veterinary Medicine, Università degli Studi di Teramo, Teramo, Italy
| | | | - Alessio Arbuatti
- Faculty of Veterinary Medicine, Università degli Studi di Teramo, Teramo, Italy
| | | | - Fulvio Marsilio
- Faculty of Veterinary Medicine, Università degli Studi di Teramo, Teramo, Italy
| | - Vito Martella
- Faculty of Veterinary Medicine, Università Aldo Moro di Bari, Valenzano, Italy
| | - Barbara Di Martino
- Faculty of Veterinary Medicine, Università degli Studi di Teramo, Teramo, Italy
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Hepatitis E virus was not detected in feces and milk of cows in Hebei province of China: No evidence for HEV prevalence in cows. Int J Food Microbiol 2019; 291:5-9. [DOI: 10.1016/j.ijfoodmicro.2018.11.002] [Citation(s) in RCA: 11] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/31/2018] [Revised: 10/03/2018] [Accepted: 11/04/2018] [Indexed: 01/10/2023]
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41
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Kosoltanapiwat N, Reamtong O, Okabayashi T, Ampawong S, Rungruengkitkun A, Thiangtrongjit T, Thippornchai N, Leaungwutiwong P, Mahittikorn A, Mori H, Yoohanngoa T, Yamwong P. Mass spectrometry-based identification and whole-genome characterisation of the first pteropine orthoreovirus isolated from monkey faeces in Thailand. BMC Microbiol 2018; 18:135. [PMID: 30332986 PMCID: PMC6192116 DOI: 10.1186/s12866-018-1302-9] [Citation(s) in RCA: 11] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/19/2017] [Accepted: 10/04/2018] [Indexed: 12/28/2022] Open
Abstract
Background The pteropine orthoreovirus (PRV) was isolated from monkey (Macaca fascicularis) faecal samples collected from human-inhabited areas in Lopburi Province, Thailand. These samples were initially obtained to survey for the presence of hepatitis E virus (HEV). Results Two virus isolates were retrieved by virus culture of 55 monkey faecal samples. Liquid chromatography-tandem mass spectrometry (LC-MS/MS) was successfully used to identify the viruses as the segmented dsRNA orthoreovirus. Phylogenetic analysis of the Lopburi orthoreovirus whole-genomes revealed relationships with the well-characterised PRVs Pulau (segment L1), Cangyuan (segments L2, M3 and S3), Melaka (segments L3 and M2), Kampar (segments M1 and S2) and Sikamat (segments S1 and S4) of Southeast Asia and China with nucleotide sequence identities of 93.5–98.9%. RT-PCR showed that PRV was detected in 10.9% (6/55) and HEV was detected in 25.5% (14/55) of the monkey faecal samples. Conclusions PRV was isolated from monkey faeces for the first time in Thailand via viral culture and LC-MS/MS. The genetic diversity of the virus genome segments suggested a re-assortment within the PRV species group. The overall findings emphasise that monkey faeces can be sources of zoonotic viruses, including PRV and HEV, and suggest the need for active virus surveillance in areas of human and monkey co-habitation to prevent and control emerging zoonotic diseases in the future. Electronic supplementary material The online version of this article (10.1186/s12866-018-1302-9) contains supplementary material, which is available to authorized users.
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Affiliation(s)
- Nathamon Kosoltanapiwat
- Department of Microbiology and Immunology, Faculty of Tropical Medicine, Mahidol University, 420/6 Ratchawithi Road, Ratchathewi, Bangkok, 10400, Thailand.
| | - Onrapak Reamtong
- Department of Molecular Tropical Medicine and Genetics, Faculty of Tropical Medicine, Mahidol University, 420/6 Ratchawithi Road, Ratchathewi, Bangkok, 10400, Thailand
| | - Tamaki Okabayashi
- Department of Veterinary Sciences, Faculty of Agriculture, University of Miyazaki, Gakuen-kibanadai-nishi-1-1, Miyazaki, 889-2192, Japan.,Mahidol-Osaka Center for Infectious Diseases (MOCID), Research Institute for Microbial Diseases, Osaka University, 3-1 Yamadaoka, Suita, Osaka, 565-0871, Japan
| | - Sumate Ampawong
- Department of Tropical Pathology, Faculty of Tropical Medicine, Mahidol University, 420/6 Ratchawithi Road, Ratchathewi, Bangkok, 10400, Thailand
| | - Amporn Rungruengkitkun
- Department of Microbiology and Immunology, Faculty of Tropical Medicine, Mahidol University, 420/6 Ratchawithi Road, Ratchathewi, Bangkok, 10400, Thailand
| | - Tipparat Thiangtrongjit
- Department of Molecular Tropical Medicine and Genetics, Faculty of Tropical Medicine, Mahidol University, 420/6 Ratchawithi Road, Ratchathewi, Bangkok, 10400, Thailand
| | - Narin Thippornchai
- Department of Microbiology and Immunology, Faculty of Tropical Medicine, Mahidol University, 420/6 Ratchawithi Road, Ratchathewi, Bangkok, 10400, Thailand
| | - Pornsawan Leaungwutiwong
- Department of Microbiology and Immunology, Faculty of Tropical Medicine, Mahidol University, 420/6 Ratchawithi Road, Ratchathewi, Bangkok, 10400, Thailand
| | - Aongart Mahittikorn
- Department of Protozoology, Faculty of Tropical Medicine, Mahidol University, 420/6 Ratchawithi Road, Ratchathewi, Bangkok, 10400, Thailand
| | - Hirotake Mori
- Department of Protozoology, Faculty of Tropical Medicine, Mahidol University, 420/6 Ratchawithi Road, Ratchathewi, Bangkok, 10400, Thailand
| | - Thanada Yoohanngoa
- Department of Microbiology and Immunology, Faculty of Tropical Medicine, Mahidol University, 420/6 Ratchawithi Road, Ratchathewi, Bangkok, 10400, Thailand
| | - Prechaya Yamwong
- Department of Microbiology and Immunology, Faculty of Tropical Medicine, Mahidol University, 420/6 Ratchawithi Road, Ratchathewi, Bangkok, 10400, Thailand
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Lopez-Lopez P, Risalde MDLA, Frias M, García-Bocanegra I, Brieva T, Caballero-Gomez J, Camacho A, Fernández-Molera V, Machuca I, Gomez-Villamandos JC, Rivero A, Rivero-Juarez A. Risk factors associated with hepatitis E virus in pigs from different production systems. Vet Microbiol 2018; 224:88-92. [PMID: 30269796 DOI: 10.1016/j.vetmic.2018.08.020] [Citation(s) in RCA: 23] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/02/2018] [Revised: 08/14/2018] [Accepted: 08/20/2018] [Indexed: 01/19/2023]
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Smith DB, Simmonds P. Classification and Genomic Diversity of Enterically Transmitted Hepatitis Viruses. Cold Spring Harb Perspect Med 2018; 8:a031880. [PMID: 29530950 PMCID: PMC6120691 DOI: 10.1101/cshperspect.a031880] [Citation(s) in RCA: 69] [Impact Index Per Article: 9.9] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/28/2022]
Abstract
Hepatitis A virus (HAV) and hepatitis E virus (HEV) are significant human pathogens and are responsible for a substantial proportion of cases of severe acute hepatitis worldwide. Genetically, both viruses are heterogeneous and are classified into several genotypes that differ in their geographical distribution and risk group association. There is, however, little evidence that variants of HAV or HEV differ antigenically or in their propensity to cause severe disease. Genetically more divergent but primarily hepatotropic variants of both HAV and HEV have been found in several mammalian species, those of HAV being classified into eight species within the genus Hepatovirus in the virus family Picornaviridae. HEV is classified as a member of the species Orthohepevirus A in the virus family Hepeviridae, a species that additionally contains viruses infecting pigs, rabbits, and a variety of other mammalian species. Other species (Orthohepevirus B-D) infect a wide range of other mammalian species including rodents and bats.
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Affiliation(s)
- Donald B Smith
- Centre for Immunity, Infection and Evolution, University of Edinburgh, Edinburgh EH9 3JT, United Kingdom
- Nuffield Department of Medicine, University of Oxford, Oxford OX1 3SY, United Kingdom
| | - Peter Simmonds
- Nuffield Department of Medicine, University of Oxford, Oxford OX1 3SY, United Kingdom
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King NJ, Hewitt J, Perchec-Merien AM. Hiding in Plain Sight? It's Time to Investigate Other Possible Transmission Routes for Hepatitis E Virus (HEV) in Developed Countries. FOOD AND ENVIRONMENTAL VIROLOGY 2018; 10:225-252. [PMID: 29623595 DOI: 10.1007/s12560-018-9342-8] [Citation(s) in RCA: 24] [Impact Index Per Article: 3.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 12/17/2017] [Accepted: 03/29/2018] [Indexed: 06/08/2023]
Abstract
Historically in developed countries, reported hepatitis E cases were typically travellers returning from countries where hepatitis E virus (HEV) is endemic, but now there are increasing numbers of non-travel-related ("autochthonous") cases being reported. Data for HEV in New Zealand remain limited and the transmission routes unproven. We critically reviewed the scientific evidence supporting HEV transmission routes in other developed countries to inform how people in New Zealand may be exposed to this virus. A substantial body of indirect evidence shows domesticated pigs are a source of zoonotic human HEV infection, but there is an information bias towards this established reservoir. The increasing range of animals in which HEV has been detected makes it important to consider other possible animal reservoirs of HEV genotypes that can or could infect humans. Foodborne transmission of HEV from swine and deer products has been proven, and a large body of indirect evidence (e.g. food surveys, epidemiological studies and phylogenetic analyses) support pig products as vehicles of HEV infection. Scarce data from other foods suggest we are neglecting other potential sources of foodborne HEV infection. Moreover, other transmission routes are scarcely investigated in developed countries; the role of infected food handlers, person-to-person transmission via the faecal-oral route, and waterborne transmission from recreational contact or drinking untreated or inadequately treated water. People have become symptomatic after receiving transfusions of HEV-contaminated blood, but it is unclear how important this is in the overall hepatitis E disease burden. There is need for broader research efforts to support establishing risk-based controls.
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Affiliation(s)
- Nicola J King
- Institute of Environmental Science and Research, 34 Kenepuru Drive, Kenepuru, Porirua, 5022, New Zealand
| | - Joanne Hewitt
- Institute of Environmental Science and Research, 34 Kenepuru Drive, Kenepuru, Porirua, 5022, New Zealand.
| | - Anne-Marie Perchec-Merien
- New Zealand Ministry for Primary Industries, Pastoral House, 25 The Terrace, Wellington, New Zealand
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45
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Tritz SE, Khounvisith V, Pommasichan S, Ninnasopha K, Keosengthong A, Phoutana V, Camoin M, Hübschen JM, Black AP, Muller CP, Snoeck CJ, Pauly M. Evidence of increased Hepatitis E virus exposure in Lao villagers with contact to ruminants. Zoonoses Public Health 2018; 65:690-701. [PMID: 29888475 DOI: 10.1111/zph.12483] [Citation(s) in RCA: 21] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/21/2017] [Revised: 03/28/2018] [Accepted: 05/03/2018] [Indexed: 02/06/2023]
Abstract
Although pigs are the main reservoir, ruminants have also been shown to be susceptible to hepatitis E virus (HEV). We investigated zoonotic transmission of HEV in rural settings of Lao People's Democratic Republic (Lao PDR) where humans are in close contacts with ruminants and where pigs are rare. Villagers with (n = 171, risk group) and without (n = 155, control group) cattle were recruited in seven villages in Vientiane Capital. Owners of pigs were excluded. Blood, as well as information on socio-demographics, animal contact, dietary habits and awareness of zoonoses were collected to assess risk factors. Blood and rectal swabs were collected from cattle (n = 173) and other ruminants (27 goat, 5 buffaloes) to measure anti-HEV antibody and virus prevalence. A similar anti-HEV antibody seroprevalence was found in cattle (6.8%) and other ruminants (8%). HEV RNA was detected in none of the animal rectal swabs and human sera. Anti-HEV IgG seroprevalence was higher in cattle farmers than in the control group (59.1% vs. 43.9%, p = 0.008) and increased significantly with age. Other risk factors included male gender, close contact with cattle and consumption of undercooked meat. We find that HEV is highly endemic in rural Laos and provide first evidence that HEV circulates in free-roaming ruminants with open access to village water sources. Despite some awareness about hygiene, villagers are likely constantly exposed to zoonotic diseases by dietary and lifestyle habits. Cattle farmers had a higher risk of HEV infection than other villagers. Our study highlights the need to raise the awareness of the rural population about water- and food-borne pathogens, and about the role of cattle as a possible source of infection. The knowledge gained on local risk factors and husbandry conditions should guide future awareness raising campaigns and promote appropriate hygienic measures including handwashing and the consumption of safe food and water.
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Affiliation(s)
- Silvia E Tritz
- Department of Infection and Immunity, Luxembourg Institute of Health, Esch-sur-Alzette, Grand-Duchy of Luxembourg
| | - Vilaysone Khounvisith
- Lao-Lux-Laboratory, Institute Pasteur du Laos, Vientiane, Lao People's Democratic Republic
| | - Sisavath Pommasichan
- The Faculty of Agriculture, National University of Laos - Nabong Campus, Vientiane, Lao People's Democratic Republic
| | - Khampasong Ninnasopha
- The Faculty of Agriculture, National University of Laos - Nabong Campus, Vientiane, Lao People's Democratic Republic
| | - Amphone Keosengthong
- The Faculty of Agriculture, National University of Laos - Nabong Campus, Vientiane, Lao People's Democratic Republic
| | - Vannaphone Phoutana
- The Faculty of Agriculture, National University of Laos - Nabong Campus, Vientiane, Lao People's Democratic Republic
| | - Margot Camoin
- Veterinarians without Borders-Canada, Ottawa, Ontario, Canada
| | - Judith M Hübschen
- Department of Infection and Immunity, Luxembourg Institute of Health, Esch-sur-Alzette, Grand-Duchy of Luxembourg
| | - Antony P Black
- Lao-Lux-Laboratory, Institute Pasteur du Laos, Vientiane, Lao People's Democratic Republic
| | - Claude P Muller
- Department of Infection and Immunity, Luxembourg Institute of Health, Esch-sur-Alzette, Grand-Duchy of Luxembourg.,Lao-Lux-Laboratory, Institute Pasteur du Laos, Vientiane, Lao People's Democratic Republic.,Laboratoire National de Santé, Dudelange, Luxembourg
| | - Chantal J Snoeck
- Department of Infection and Immunity, Luxembourg Institute of Health, Esch-sur-Alzette, Grand-Duchy of Luxembourg
| | - Maude Pauly
- Department of Infection and Immunity, Luxembourg Institute of Health, Esch-sur-Alzette, Grand-Duchy of Luxembourg
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46
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Melegari I, Di Profio F, Marsilio F, Sarchese V, Palombieri A, Friedrich KG, Coccia F, Di Martino B. Serological and molecular investigation for hepatitis E virus (HEV) in captive non-human primates, Italy. Virus Res 2018; 251:17-21. [DOI: 10.1016/j.virusres.2018.04.017] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/16/2018] [Revised: 04/25/2018] [Accepted: 04/27/2018] [Indexed: 02/02/2023]
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Detection and Characterization of Hepatitis E Virus in Goats at Slaughterhouse in Tai'an Region, China. BIOMED RESEARCH INTERNATIONAL 2017; 2017:3723650. [PMID: 29379797 PMCID: PMC5742876 DOI: 10.1155/2017/3723650] [Citation(s) in RCA: 27] [Impact Index Per Article: 3.4] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 09/07/2017] [Accepted: 11/26/2017] [Indexed: 12/11/2022]
Abstract
Background Hepatitis E virus (HEV) is a significant pathogen of viral hepatitis and can be transmitted through fecal-oral route. Epidemiological data concerning HEV in goats, however, are relatively sparse to date. Here, the prevalence and characteristics of HEV isolated from goats at slaughterhouse were investigated in Tai'an region, China. Methods Anti-HEV immunoglobulin G (IgG) in blood samples and HEV RNA in the liver samples were determined by using an enzyme-linked immunosorbent assay (ELISA) and a nested reverse transcription polymerase chain reaction (RT-PCR), respectively. In addition, partial nucleotide sequences of open reading frame 2 (ORF-2) of HEV isolates were analyzed. Results Fifty goat blood samples (46.7%, 50/120) were masculine for anti-HEV IgG. HEV RNA was detected in 2 liver samples (4.0%, 2/50) and belonged to genotype 4 subtype 4 h, with high identity (91.2-93%) with cow HEV strains detected in the same province, China. Conclusions These findings demonstrated that goats may be an important reservoir for HEV and can become a major source of HEV infection in humans via food chain.
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48
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Nan Y, Wu C, Zhao Q, Zhou EM. Zoonotic Hepatitis E Virus: An Ignored Risk for Public Health. Front Microbiol 2017; 8:2396. [PMID: 29255453 PMCID: PMC5723051 DOI: 10.3389/fmicb.2017.02396] [Citation(s) in RCA: 54] [Impact Index Per Article: 6.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/17/2017] [Accepted: 11/20/2017] [Indexed: 12/27/2022] Open
Abstract
Hepatitis E virus (HEV) is a quasi-enveloped, single-stranded positive-sense RNA virus. HEV belongs to the family Hepeviridae, a family comprised of highly diverse viruses originating from various species. Since confirmation of HEV's zoonosis, HEV-induced hepatitis has been a public health concern both for developing and developed countries. Meanwhile, the demonstration of a broad host range for zoonotic HEV suggests the existence of a variety of transmission routes that could lead to human infection. Moreover, anti-HEV antibody serosurveillance worldwide demonstrates a higher than expected HEV prevalence rate that conflicts with the rarity and sporadic nature of reported acute hepatitis E cases. In recent years, chronic HEV infection, HEV-related acute hepatic failure, and extrahepatic manifestations caused by HEV infection have been frequently reported. These observations suggest a significant underestimation of the number and complexity of transmission routes previously predicted to cause HEV-related disease, with special emphasis on zoonotic HEV as a public health concern. Significant research has revealed details regarding the virology and infectivity of zoonotic HEV in both humans and animals. In this review, the discovery of HEV zoonosis, recent progress in our understanding of the zoonotic HEV host range, and classification of diverse HEV or HEV-like isolates from various hosts are reviewed in a historic context. Ultimately, this review focuses on current understanding of viral pathogenesis and cross-species transmission of zoonotic HEV. Moreover, host factors and viral determinants influencing HEV host tropism are discussed to provide new insights into HEV transmission and prevalence mechanisms.
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Affiliation(s)
- Yuchen Nan
- Department of Preventive Veterinary Medicine, College of Veterinary Medicine, Northwest A&F University, Xianyang, China
- Scientific Observing and Experimental Station of Veterinary Pharmacology and Diagnostic Technology, Ministry of Agriculture, Xianyang, China
| | - Chunyan Wu
- Department of Preventive Veterinary Medicine, College of Veterinary Medicine, Northwest A&F University, Xianyang, China
- Scientific Observing and Experimental Station of Veterinary Pharmacology and Diagnostic Technology, Ministry of Agriculture, Xianyang, China
| | - Qin Zhao
- Department of Preventive Veterinary Medicine, College of Veterinary Medicine, Northwest A&F University, Xianyang, China
- Scientific Observing and Experimental Station of Veterinary Pharmacology and Diagnostic Technology, Ministry of Agriculture, Xianyang, China
| | - En-Min Zhou
- Department of Preventive Veterinary Medicine, College of Veterinary Medicine, Northwest A&F University, Xianyang, China
- Scientific Observing and Experimental Station of Veterinary Pharmacology and Diagnostic Technology, Ministry of Agriculture, Xianyang, China
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49
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Spahr C, Knauf-Witzens T, Vahlenkamp T, Ulrich RG, Johne R. Hepatitis E virus and related viruses in wild, domestic and zoo animals: A review. Zoonoses Public Health 2017; 65:11-29. [PMID: 28944602 DOI: 10.1111/zph.12405] [Citation(s) in RCA: 85] [Impact Index Per Article: 10.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/09/2017] [Indexed: 01/15/2023]
Abstract
Hepatitis E is a human disease mainly characterized by acute liver illness, which is caused by infection with the hepatitis E virus (HEV). Large hepatitis E outbreaks have been described in developing countries; however, the disease is also increasingly recognized in industrialized countries. Mortality rates up to 25% have been described for pregnant women during outbreaks in developing countries. In addition, chronic disease courses could be observed in immunocompromised transplant patients. Whereas the HEV genotypes 1 and 2 are mainly confined to humans, genotypes 3 and 4 are also found in animals and can be zoonotically transmitted to humans. Domestic pig and wild boar represent the most important reservoirs for these genotypes. A distinct subtype of genotype 3 has been repeatedly detected in rabbits and a few human patients. Recently, HEV genotype 7 has been identified in dromedary camels and in an immunocompromised transplant patient. The reservoir animals get infected with HEV without showing any clinical symptoms. Besides these well-known animal reservoirs, HEV-specific antibodies and/or the genome of HEV or HEV-related viruses have also been detected in many other animal species, including primates, other mammals and birds. In particular, genotypes 3 and 4 infections are documented in many domestic, wildlife and zoo animal species. In most cases, the presence of HEV in these animals can be explained by spillover infections, but a risk of virus transmission through contact with humans cannot be excluded. This review gives a general overview on the transmission pathways of HEV to humans. It particularly focuses on reported serological and molecular evidence of infections in wild, domestic and zoo animals with HEV or HEV-related viruses. The role of these animals for transmission of HEV to humans and other animals is discussed.
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Affiliation(s)
- C Spahr
- Wilhelma Zoological-Botanical Gardens, Stuttgart, Germany.,Faculty of Veterinary Medicine, Institute of Virology, University of Leipzig, Leipzig, Germany
| | | | - T Vahlenkamp
- Faculty of Veterinary Medicine, Institute of Virology, University of Leipzig, Leipzig, Germany
| | - R G Ulrich
- Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Institute of Novel and Emerging Infectious Diseases, Greifswald-Insel Riems, Germany.,German Center for Infection Research (DZIF), partner site Hamburg-Luebeck-Borstel-Insel Riems, Braunschweig, Germany
| | - R Johne
- Department Biological Safety, German Federal Institute for Risk Assessment, Berlin, Germany
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Mauceri C, Grazia Clemente M, Castiglia P, Antonucci R, Schwarz KB. Hepatitis E in Italy: A silent presence. J Infect Public Health 2017; 11:1-8. [PMID: 28864359 DOI: 10.1016/j.jiph.2017.08.004] [Citation(s) in RCA: 10] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/03/2017] [Revised: 07/03/2017] [Accepted: 08/04/2017] [Indexed: 01/18/2023] Open
Abstract
Hepatitis E virus (HEV) was discovered in the 1980s and has been considered as being confined to developing countries. The purpose of this critical review was to determine the reported HEV seroprevalence rates in Italy, to identify predisposing factors and individuals at risk and to assess possible importation of HEV by immigrants. A critical review of 159 articles published in PubMed from 1994 to date was done. Only 27 original reports of 50 or more subjects, written in the English or Italian language, were included. Over three decades, the HEV seroprevalence varied from 0.12% to 49%, with the highest rates being reported from the central region of Italy. Risk factors included ingestion of raw pork or potentially contaminated food. The seroprevalence among immigrants ranged from 15.3% to 19.7% in Apulia. Italy has a population of 60656000; the total number of individuals surveyed was only 21.882 (0.036%). A national epidemiological survey program is needed to capture more comprehensive seroprevalence data.
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Affiliation(s)
- Carlo Mauceri
- Pediatric Clinic, Department of Surgical, Microsurgical and Medical Sciences, University of Sassari Medical School, 07100 Sassari, Italy.
| | - Maria Grazia Clemente
- Pediatric Clinic, Department of Surgical, Microsurgical and Medical Sciences, University of Sassari Medical School, 07100 Sassari, Italy.
| | - Paolo Castiglia
- Department of Biomedical Sciences-Hygiene and Preventive Medicine Unit, University-AOU of Sassari, 07100 Sassari, Italy.
| | - Roberto Antonucci
- Pediatric Clinic, Department of Surgical, Microsurgical and Medical Sciences, University of Sassari Medical School, 07100 Sassari, Italy.
| | - Kathleen B Schwarz
- Pediatric Liver Center, Johns Hopkins University School of Medicine, Baltimore 21287, MD, USA.
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