Hepatitis E virus (HEV)—The Future
Abstract
:1. Introduction
2. HEV-3 in the Pig Population and Other Wild Animals
3. Transmission of HEV to Humans
4. Measures to Prevent HEV Transmission
5. HEV and Xenotransplantation
6. HEV and the One Health Concept
7. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Purdy, M.A.; Harrison, T.J.; Jameel, S.; Meng, X.J.; Okamoto, H.; Van der Poel, W.H.M.; Smith, D.B. Ictv Report Consortium. ICTV Virus Taxonomy Profile: Hepeviridae. J. Gen. Virol. 2017, 98, 2645–2646. [Google Scholar] [CrossRef] [PubMed]
- Johne, R.; Dremsek, P.; Reetz, J.; Heckel, G.; Hess, M.; Ulrich, R.G. Hepeviridae: An expanding family of vertebrate viruses. Infect. Genet. Evol. 2014, 27, 212–229. [Google Scholar] [CrossRef] [PubMed]
- Kamar, N.; Izopet, J.; Pavio, N.; Aggarwal, R.; Labrique, A.; Wedemeyer, H.; Dalton, H.R. Hepatitis E virus infection. Nat. Rev. Dis. Primers 2017, 3, 17086. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rein, D.B.; Stevens, G.A.; Theaker, J.; Wittenborn, J.S.; Wiersma, S.T. The global burden of hepatitis E virus genotypes 1 and 2 in 2005. Hepatology 2012, 55, 988–997. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Colson, P.; Borentain, P.; Queyriaux, B.; Kaba, M.; Moal, V.; Gallian, P.; Heyries, L.; Raoult, D.; Gerolami, R. Pig liver sausage as a source of hepatitis E virus transmission to humans. J. Infect. Dis. 2010, 202, 825–834. [Google Scholar] [CrossRef]
- Guillois, Y.; Abravanel, F.; Miura, T.; Pavio, N.; Vaillant, V.; Lhomme, S.; Le Guyader, F.S.; Rose, N.; Le Saux, J.C.; King, L.A.; et al. High Proportion of Asymptomatic Infections in an Outbreak of Hepatitis E Associated with a Spit-Roasted Piglet, France, 2013. Clin. Infect. Dis. 2016, 62, 351–357. [Google Scholar] [CrossRef] [PubMed]
- Dremsek, P.; Wenzel, J.J.; Johne, R.; Ziller, M.; Hofmann, J.; Groschup, M.H.; Werdermann, S.; Mohn, U.; Dorn, S.; Motz, M.; et al. Seroprevalence study in forestry workers from eastern Germany using novel genotype 3- and rat hepatitis E virus-specific immunoglobulin G ELISAs. Med. Microbiol. Immunol. 2012, 201, 189–200. [Google Scholar] [CrossRef]
- Chaussade, H.; Rigaud, E.; Allix, A.; Carpentier, A.; Touzé, A.; Delzescaux, D.; Choutet, P.; Garcia-Bonnet, N.; Coursaget, P. Hepatitis E virus seroprevalence and risk factors for individuals in working contact with animals. J. Clin. Virol. 2013, 58, 504–508. [Google Scholar] [CrossRef]
- Pavio, N.; Renou, C.; Di Liberto, G.; Boutrouille, A.; Eloit, M. Hepatitis E: A curious zoonosis. Front. Biosci. 2008, 13, 7172–7183. [Google Scholar] [CrossRef]
- Riveiro-Barciela, M.; Mínguez, B.; Gironés, R.; Rodriguez-Frías, F.; Quer, J.; Buti, M. Phylogenetic demonstration of hepatitis E infection transmitted by pork meat ingestion. J. Clin. Gastroenterol. 2015, 49, 165–168. [Google Scholar] [CrossRef]
- Hewitt, P.E.; Ijaz, S.; Brailsford, S.R.; Brett, R.; Dicks, S.; Haywood, B.; Kennedy, I.T.; Kitchen, A.; Patel, P.; Poh, J.; et al. Hepatitis E virus in blood components: A prevalence and transmission study in southeast England. Lancet 2014, 384, 1766–1773. [Google Scholar] [CrossRef]
- Gallian, P.; Lhomme, S.; Piquet, Y.; Sauné, K.; Abravanel, F.; Assal, A.; Tiberghien, P.; Izopet, J. Hepatitis E virus infections in blood donors, France. Emerg. Infect. Dis. 2014, 20, 1914–1917. [Google Scholar] [CrossRef]
- Baylis, S.A.; Gärtner, T.; Nick, S.; Ovemyr, J.; Blümel, J. Occurrence of hepatitis E virus RNA in plasma donations from Sweden, Germany and the United States. Vox Sang. 2012, 103, 89–90. [Google Scholar] [CrossRef]
- Sauleda, S.; Ong, E.; Bes, M.; Janssen, A.; Cory, R.; Babizki, M.; Shin, T.; Lindquist, A.; Hoang, A.; Vang, L.; et al. Seroprevalence of hepatitis E virus (HEV) and detection of HEV RNA with a transcription-mediated amplification assay in blood donors from Catalonia (Spain). Transfusion 2015, 55, 972–979. [Google Scholar] [CrossRef]
- Hogema, B.M.; Molier, M.; Sjerps, M.; de Waal, M.; van Swieten, P.; van de Laar, T.; Molenaar-de Backer, M.; Zaaijer, H.L. Incidence and duration of hepatitis E virus infection in Dutch blood donors. Transfusion 2016, 56, 722–728. [Google Scholar] [CrossRef]
- Stramer, S.L. Current perspectives in transfusion-transmitted infectious diseases: Emerging and re-emerging infections. ISBT Sci. Ser. 2014, 9, 30–36. [Google Scholar] [CrossRef]
- Juhl, D.; Baylis, S.A.; Blümel, J.; Görg, S.; Hennig, H. Seroprevalence and incidence of hepatitis E virus infection in German blood donors. Transfusion 2014, 54, 49–56. [Google Scholar] [CrossRef]
- Horvatits, T.; Ozga, A.K.; Westhölter, D.; Hartl, J.; Manthey, C.F.; Lütgehetmann, M.; Rauch, G.; Kriston, L.; Lohse, A.W.; Bendall, R.; et al. Hepatitis E seroprevalence in the Americas: A systematic review and meta-analysis. Liver Int. 2018, 38, 1951–1964. [Google Scholar] [CrossRef]
- Westhölter, D.; Hiller, J.; Denzer, U.; Polywka, S.; Ayuk, F.; Rybczynski, M.; Horvatits, T.; Gundlach, S.; Blöcker, J.; Schulze Zur Wiesch, J.; et al. HEV-positive blood donations represent a relevant infection risk for immunosuppressed recipients. J. Hepatol. 2018, 69, 36–42. [Google Scholar] [CrossRef]
- Niederhauser, C.; Widmer, N.; Hotz, M.; Tinguely, C.; Fontana, S.; Allemann, G.; Borri, M.; Infanti, L.; Sarraj, A.; Sigle, J.; et al. Current hepatitis E virus seroprevalence in Swiss blood donors and apparent decline from 1997 to 2016. Euro Surveill. 2018, 23, 1700616. [Google Scholar] [CrossRef]
- Beale, M.A.; Tettmar, K.; Szypulska, R.; Tedder, R.S.; Ijaz, S. Is there evidence of recent hepatitis E virus infection in English and North Welsh blood donors? Vox Sang. 2011, 100, 340–342. [Google Scholar] [CrossRef]
- Boxall, E.; Herborn, A.; Kochethu, G.; Pratt, G.; Adams, D.; Ijaz, S.; Teo, C.G. Transfusion-transmitted hepatitis E in a ‘nonhyperendemic’ country. Transfus. Med. 2006, 16, 79–83. [Google Scholar] [CrossRef]
- Dreier, J.; Knabbe, C.; Vollmer, T. Transfusion-Transmitted Hepatitis E: NAT Screening of Blood Donations and Infectious Dose. Front. Med. 2018, 5, 5. [Google Scholar] [CrossRef]
- Tedder, R.S.; Ijaz, S.; Kitchen, A.; Ushiro-Lumb, I.; Tettmar, K.I.; Hewitt, P.; Andrews, N. Hepatitis E risks: Pigs or blood-that is the question. Transfusion 2017, 57, 267–272. [Google Scholar] [CrossRef]
- Vollmer, T.; Diekmann, J.; Johne, R.; Eberhardt, M.; Knabbe, C.; Dreier, J. Novel approach for detection of hepatitis E virus infection in German blood donors. J. Clin. Microbiol. 2012, 50, 2708–2713. [Google Scholar] [CrossRef]
- Schlosser, B.; Stein, A.; Neuhaus, R.; Pahl, S.; Ramez, B.; Krüger, D.H.; Berg, T.; Hofmann, J. Liver transplant from a donor with occult HEV infection induced chronic hepatitis and cirrhosis in the recipient. J. Hepatol. 2012, 56, 500–502. [Google Scholar] [CrossRef] [Green Version]
- Pischke, S.; Suneetha, P.V.; Baechlein, C.; Barg-Hock, H.; Heim, A.; Kamar, N.; Schlue, J.; Strassburg, C.P.; Lehner, F.; Raupach, R.; et al. Hepatitis E virus infection as a cause of graft hepatitis in liver transplant recipients. Liver Transplant. 2010, 16, 74–82. [Google Scholar] [CrossRef] [Green Version]
- Pischke, S.; Greer, M.; Hardtke, S.; Bremer, B.; Gisa, A.; Lehmann, P.; Haverich, A.; Welte, T.; Manns, M.P.; Wedemeyer, H.; et al. Hepatitis E study group. Course and treatment of chronic hepatitis E virus infection in lung transplant recipients. Transplant. Infect. Dis. 2014, 16, 333–339. [Google Scholar] [CrossRef]
- Ankcorn, M.J.; Ijaz, S.; Poh, J.; Elsharkawy, A.M.; Smit, E.; Cramb, R.; Ravi, S.; Martin, K.; Tedder, R.; Neuberger, J. Toward Systematic Screening for Persistent Hepatitis E Virus Infections in Transplant Patients. Transplantation 2018, 102, 1139–1147. [Google Scholar] [CrossRef]
- Lhomme, S.; Lhomme, S.; Abravanel, F.; Dubois, M.; Sandres-Saune, K.; Rostaing, L.; Kamar, N.; Izopet, J. Hepatitis E virus quasispecies and the outcome of acute hepatitis E in solid-organ transplant patients. J. Virol. 2012, 86, 10006–10014. [Google Scholar] [CrossRef]
- Lhomme, S.; Marion, O.; Abravanel, F.; Chapuy-Regaud, S.; Kamar, N.; Izopet, J. Hepatitis E Pathogenesis. Viruses 2016, 8, 212. [Google Scholar] [CrossRef]
- Slot, E.; Zaaijer, H.L.; Molier, M.; Van den Hurk, K.; Prinsze, F.; Hogema, B.M. Meat consumption is a major risk factor for hepatitis E virus infection. PLoS ONE 2017, 12, e0176414. [Google Scholar] [CrossRef]
- Van Cauteren, D.; Le Strat, Y.; Sommen, C.; Bruyand, M.; Tourdjman, M.; Da Silva, N.J.; Couturier, E.; Fournet, N.; de Valk, H.; Desenclos, J.C. Estimated Annual Numbers of Foodborne Pathogen-Associated Illnesses, Hospitalizations, and Deaths, France, 2008–2013. Emerg. Infect. Dis. 2017, 23, 1486–1492. [Google Scholar] [CrossRef]
- Aspinall, E.J.; Couturier, E.; Faber, M.; Said, B.; Ijaz, S.; Tavoschi, L.; Takkinen, J.; Adlhoch, C. On Behalf of the Country Experts. Hepatitis E virus infection in Europe: Surveillance and descriptive epidemiology of confirmed cases, 2005 to 2015. Euro Surveill. 2017, 22, 30561. [Google Scholar] [CrossRef]
- Takahashi, M.; Nishizawa, T.; Sato, H.; Sato, Y.; Jirintai Nagashima, S.; Okamoto, H. Analysis of the full-length genome of a hepatitis E virus isolate obtained from a wild boar in Japan that is classifiable into a novel genotype. J. Gen. Virol. 2011, 92 Pt 4, 902–908. [Google Scholar] [CrossRef] [Green Version]
- Lee, G.H.; Tan, B.H.; Teo, E.C.; Lim, S.G.; Dan, Y.Y.; Wee, A.; Aw, P.P.; Zhu, Y.; Hibberd, M.L.; Tan, C.K.; et al. Chronic Infection with Camelid Hepatitis E Virus in a Liver Transplant Recipient Who Regularly Consumes Camel Meat and Milk. Gastroenterology 2016, 150, 55–57. [Google Scholar] [CrossRef]
- Woo, P.C.; Lau, S.K.; Teng, J.L.; Cao, K.Y.; Wernery, U.; Schountz, T.; Chiu, T.H.; Tsang, A.K.; Wong, P.C.; Wong, E.Y.; et al. New Hepatitis E Virus. Genotype in Bactrian Camels, Xinjiang, China, 2013. Emerg. Infect. Dis. 2016, 22, 2219–2221. [Google Scholar] [CrossRef]
- Pavio, N.; Doceul, V.; Bagdassarian, E.; Johne, R. Recent knowledge on hepatitis E virus in Suidae reservoirs and transmission routes to human. Vet. Res. 2017, 48, 78. [Google Scholar] [CrossRef]
- Bouamra, Y.; Gérolami, R.; Arzouni, J.P.; Grimaud, J.C.; Lafforgue, P.; Nelli, M.; Tivoli, N.; Ferretti, A.; Motte, A.; Colson, P. Emergence of autochthonous infections with hepatitis E virus of genotype 4 in Europe. Intervirology 2014, 57, 43–48. [Google Scholar] [CrossRef]
- Williams, T.P.; Kasorndorkbua, C.; Halbur, P.G.; Haqshenas, G.; Guenette, D.K.; Toth, T.E.; Meng, X.J. Evidence of extrahepatic sites of replication of the hepatitis E virus in a swine model. J. Clin. Microbiol. 2001, 39, 3040–3046. [Google Scholar] [CrossRef]
- Berto, A.; Backer, J.A.; Mesquita, J.R.; Nascimento, M.S.; Banks, M.; Martelli, F.; Ostanello, F.; Angeloni, G.; Di Bartolo, I.; Ruggeri, F.M.; et al. Prevalence and transmission of hepatitis E virus in domestic swine populations in different European countries. BMC Res. Notes 2012, 5, 190. [Google Scholar] [CrossRef]
- Salines, M.; Barnaud, E.; Andraud, M.; Eono, F.; Renson, P.; Bourry, O.; Pavio, N.; Rose, N. Hepatitis E virus chronic infection of swine co-infected with Porcine Reproductive and Respiratory Syndrome Virus. Vet. Res. 2015, 46, 55. [Google Scholar] [CrossRef]
- Yang, Y.; Shi, R.; She, R.; Mao, J.; Zhao, Y.; Du, F.; Liu, C.; Liu, J.; Cheng, M.; Zhu, R.; et al. Fatal disease associated with Swine Hepatitis E virus and Porcine circovirus 2 co-infection in four weaned pigs in China. BMC Vet. Res. 2015, 11, 77. [Google Scholar] [CrossRef] [Green Version]
- Jäckel, S.; Muluneh, A.; Pöhle, D.; Ulber, C.; Dähnert, L.; Vina-Rodriguez, A.; Groschup, M.H.; Eiden, M. Co-infection of pigs with Hepatitis E and porcine circovirus 2, Saxony 2016. Res. Vet. Sci. 2018, 123, 35–38. [Google Scholar] [CrossRef]
- Cao, D.; Cao, Q.M.; Subramaniam, S.; Yugo, D.M.; Heffron, C.L.; Rogers, A.J.; Kenney, S.P.; Tian, D.; Matzinger, S.R.; Overend, C.; et al. Pig model mimicking chronic hepatitis E virus infection in immunocompromised patients to assess immune correlates during chronicity. Proc. Natl. Acad. Sci. USA 2017, 114, 6914–6923. [Google Scholar] [CrossRef] [Green Version]
- Neumann, S.; Hackl, S.S.; Piepenschneider, M.; Vina-Rodriguez, A.; Dremsek, P.; Ulrich, R.G.; Groschup, M.H.; Eiden, M. Serologic and Molecular Survey of Hepatitis E Virus in German Deer Populations. J. Wildl. Dis. 2016, 52, 106–113. [Google Scholar] [CrossRef] [Green Version]
- Anheyer-Behmenburg, H.E.; Szabo, K.; Schotte, U.; Binder, A.; Klein, G.; Johne, R. Hepatitis E Virus in Wild Boars and Spillover Infection in Red and Roe Deer, Germany, 2013–2015. Emerg. Infect. Dis. 2017, 23, 130–133. [Google Scholar] [CrossRef] [Green Version]
- Spahr, C.; Knauf-Witzens, T.; Vahlenkamp, T.; Ulrich, R.G.; Johne, R. Hepatitis E virus and related viruses in wild, domestic and zoo animals: A review. Zoonoses Public Health 2018, 65, 11–29. [Google Scholar] [CrossRef]
- Izopet, J.; Dubois, M.; Bertagnoli, S.; Lhomme, S.; Marchandeau, S.; Boucher, S.; Kamar, N.; Abravanel, F.; Guérin, J.L. Hepatitis E virus strains in rabbits and evidence of a closely related strain in humans, France. Emerg. Infect. Dis. 2012, 18, 1274–1281. [Google Scholar] [CrossRef]
- García-Bocanegra, I.; Rivero, A.; Caballero-Gómez, J.; López-López, P.; Cano-Terriza, D.; Frías, M.; Jiménez-Ruiz, S.; Risalde, M.A.; Gómez-Villamandos, J.C.; Rivero-Juarez, A. Hepatitis E virus infection in equines in Spain. Transbound. Emerg. Dis. 2019, 66, 66–71. [Google Scholar] [CrossRef]
- Fenaux, H.; Chassaing, M.; Berger, S.; Gantzer, C.; Bertrand, I.; Schvoerer, E. Transmission of hepatitis E virus by water: An issue still pending in industrialized countries. Water Res. 2019, 151, 144–157. [Google Scholar] [CrossRef] [PubMed]
- Takahashi, H.; Tanaka, T.; Jirintai, S.; Nagashima, S.; Takahashi, M.; Nishizawa, T.; Mizuo, H.; Yazaki, Y.; Okamoto, H. A549 and PLC/PRF/5 cells can support the efficient propagation of swine and wild boar hepatitis E virus (HEV) strains: Demonstration of HEV infectivity of porcine liver sold as food. Arch. Virol. 2012, 157, 235–246. [Google Scholar] [CrossRef] [PubMed]
- Berto, A.; Van der Poel, W.H.; Hakze-van der Honing, R.; Martelli, F.; La Ragione, R.M.; Inglese, N.; Collins, J.; Grierson, S.; Johne, R.; Reetz, J.; et al. Replication of hepatitis E virus in three-dimensional cell culture. J. Virol. Methods 2013, 187, 327–332. [Google Scholar] [CrossRef] [PubMed]
- Feagins, A.R.; Opriessnig, T.; Guenette, D.K.; Halbur, P.G.; Meng, X.J. Detection and characterization of infectious Hepatitis E virus from commercial pig livers sold in local grocery stores in the USA. J. Gen. Virol. 2007, 88 Pt 3, 912–917. [Google Scholar] [CrossRef] [Green Version]
- Tei, S.; Kitajima, N.; Takahashi, K.; Mishiro, S. Zoonotic transmission of hepatitis E virus from deer to human beings. Lancet 2003, 362, 371–373. [Google Scholar] [CrossRef]
- Tritz, S.E.; Khounvisith, V.; Pommasichan, S.; Ninnasopha, K.; Keosengthong, A.; Phoutana, V.; Camoin, M.; Hübschen, J.M.; Black, A.P.; Muller, C.P. Evidence of increased Hepatitis E virus exposure in Lao villagers with contact to ruminants. Zoonoses Public Health 2018, 65, 690–701. [Google Scholar] [CrossRef]
- Geng, Y.; Zhao, C.; Geng, K.; Wang, C.; Wang, X.; Liu, H.; Wang, Y. High seroprevalence of hepatitis E virus in rabbit slaughterhouse workers. Transbound. Emerg. Dis. 2019. [Google Scholar] [CrossRef] [PubMed]
- Denner, J.; Pischke, S.; Steinmann, E.; Blümel, J.; Glebe, D. Why all blood donations should be tested for hepatitis E virus (HEV). BMC Infect. Dis. (under processing).
- Riveiro-Barciela, M.; Bes, M.; Quer, J.; Valcarcel, D.; Piriz, S.; Gregori, J.; Llorens, M.; Salcedo, M.T.; Piron, M.; Esteban, R.; et al. Thrombotic thrombocytopenic purpura relapse induced by acute hepatitis E transmitted by cryosupernatant plasma and successfully controlled with ribavirin. Transfusion 2018, 58, 2501–2505. [Google Scholar] [CrossRef]
- Grewal, P.; Kamili, S.; Motamed, D. Chronic hepatitis E in an immunocompetent patient: A case report. Hepatology 2014, 59, 347–348. [Google Scholar] [CrossRef]
- Domanović, D.; Tedder, R.; Blümel, J.; Zaaijer, H.; Gallian, P.; Niederhauser, C.; Sauleda Oliveras, S.; O’Riordan, J.; Boland, F.; Harritshøj, L.; et al. Hepatitis E and blood donation safety in selected European countries: A shift to screening? Euro Surveill. 2017, 22, 30514. [Google Scholar]
- Grodzki, M.; Schaeffer, J.; Piquet, J.C.; Le Saux, J.C.; Chevé, J.; Ollivier, J.; Le Pendu, J.; Le Guyader, F.S. Bioaccumulation efficiency, tissue distribution, and environmental occurrence of hepatitis E virus in bivalve shellfish from France. Appl. Environ. Microbiol. 2014, 80, 4269–4276. [Google Scholar]
- O’Hara, Z.; Crossan, C.; Craft, J.; Scobie, L. First Report of the Presence of Hepatitis E Virus in Scottish-Harvested Shellfish Purchased at Retail Level. Food Environ. Virol. 2018, 10, 217–221. [Google Scholar] [Green Version]
- Kokkinos, P.; Kozyra, I.; Lazic, S.; Bouwknegt, M.; Rutjes, S.; Willems, K.; Moloney, R.; de Roda Husman, A.M.; Kaupke, A.; Legaki, E.; et al. Harmonised investigation of the occurrence of human enteric viruses in the leafy green vegetable supply chain in three European countries. Food Environ. Virol. 2012, 4, 179–191. [Google Scholar]
- Morozov, V.A.; Morozov, A.V.; Rotem, A.; Barkai, U.; Bornstein, S.; Denner, J. Extended Microbiological Characterization of Göttingen Minipigs in the Context of Xenotransplantation: Detection and Vertical Transmission of Hepatitis E Virus. PLoS ONE 2015, 10, e0139893. [Google Scholar]
- Dalton, H.R.; Kamar, N. Treatment of hepatitis E virus. Curr. Opin. Infect. Dis. 2016, 29, 639–644. [Google Scholar]
- Kamar, N.; Izopet, J.; Tripon, S.; Bismuth, M.; Hillaire, S.; Dumortier, J.; Radenne, S.; Coilly, A.; Garrigue, V.; D’Alteroche, L.; et al. Ribavirin for chronic hepatitis E virus infection in transplant recipients. N. Engl. J. Med. 2014, 370, 1111–1120. [Google Scholar]
- Lee, D.U.; Je, S.H.; Yoo, S.J.; Kwon, T.; Shin, J.Y.; Byun, J.J.; Park, J.H.; Jeong, K.W.; Ku, J.M.; Lyoo, Y.S. Hematological adverse effects and pharmacokinetics of ribavirin in pigs following intramuscular administration. J. Vet. Pharmacol. Ther. 2017, 40, 561–568. [Google Scholar]
- Kim, Y.; Lee, C. Ribavirin efficiently suppresses porcine nidovirus replication. Virus Res. 2013, 171, 44–53. [Google Scholar]
- Kaushik, N.; Subramani, C.; Anang, S.; Muthumohan, R.; Shalimar Nayak, B.; Ranjith-Kumar, C.T.; Surjit, M. Zinc Salts Block Hepatitis E Virus Replication by Inhibiting the Activity of Viral RNA-Dependent RNA Polymerase. J. Virol. 2017, 91, e00754. [Google Scholar]
- Van der Valk, M.; Zaaijer, H.L.; Kater, A.P.; Schinkel, J. Sofosbuvir shows antiviral activity in a patient with chronic hepatitis E virus infection. J. Hepatol. 2017, 66, 242–243. [Google Scholar]
- Zhu, F.C.; Zhang, J.; Zhang, X.F.; Zhou, C.; Wang, Z.Z.; Huang, S.J.; Wang, H.; Yang, C.L.; Jiang, H.M.; Cai, J.P.; et al. Efficacy and safety of a recombinant hepatitis E vaccine in healthy adults: A large-scale, randomised, double-blind placebo-controlled, phase 3 trial. Lancet 2010, 376, 895–902. [Google Scholar]
- Wu, T.; Li, S.W.; Zhang, J.; Ng, M.H.; Xia, N.S.; Zhao, Q. Hepatitis E vaccine development: A 14 year odyssey. Hum Vaccin Immunother. 2012, 8, 823–827. [Google Scholar]
- Li, S.W.; Zhao, Q.; Wu, T.; Chen, S.; Zhang, J.; Xia, N.S. The development of a recombinant hepatitis E vaccine HEV 239. Hum. Vaccin Immunother. 2015, 11, 908–914. [Google Scholar] [Green Version]
- Zhang, J.; Zhang, X.F.; Huang, S.J.; Wu, T.; Hu, Y.M.; Wang, Z.Z.; Wang, H.; Jiang, H.M.; Wang, Y.J.; Yan, Q.; et al. Long-term efficacy of a hepatitis E vaccine. N. Engl. J. Med. 2015, 372, 914–922. [Google Scholar]
- Sanford, B.J.; Opriessnig, T.; Kenney, S.P.; Dryman, B.A.; Córdoba, L.; Meng, X.J. Assessment of the cross-protective capability of recombinant capsid proteins derived from pig, rat, and avian hepatitis E viruses (HEV) against challenge with a genotype 3 HEV in pigs. Vaccine 2012, 30, 6249–6255. [Google Scholar] [Green Version]
- Freuling, C.M.; Eggerbauer, E.; Finke, S.; Kaiser, C.; Kaiser, C.; Kretzschmar, A.; Nolden, T.; Ortmann, S.; Schröder, C.; Teifke, J.P.; et al. Efficacy of the oral rabies virus vaccine strain SPBN GASGAS in foxes and raccoon dogs. Vaccine 2017, in press. [Google Scholar] [CrossRef]
- Andonov, A.; Robbins, M.; Borlang, J.; Cao, J.; Hattchete, T.; Stueck, A.; Deschaumbault, Y.; Murnaghan, K.; Varga, J.; Johnston, B. Rat hepatitis E virus linked to severe acute hepatitis in an immunocompetent patient. J. Infect. Dis. 2019. [Google Scholar] [CrossRef]
- Sridhar, S.; Yip, C.C.Y.; Wu, S.; Cai, J.; Zhang, A.J.; Leung, K.H.; Chung, T.W.H.; Chan, J.F.W.; Chan, W.M.; Teng, J.L.L.; et al. Rat Hepatitis E Virus as Cause of Persistent Hepatitis after Liver Transplant. Emerg. Infect. Dis. 2018, 24, 2241–2250. [Google Scholar]
- Realpe-Quintero, M.; Mirazo, S.; Viera-Segura, O.; Copado-Villagrana, E.D.; Panduro, A.; Roman, S.; Arbiza, J.; Fierro, N.A. Hepatitis E Virus Genotype 1 and Hepatitis A Virus Dual Infection in Pediatric Patients with a Low Socioeconomic Status from Mexico. Intervirology 2018, 61, 105–110. [Google Scholar]
- Cooper, D.K.; Satyananda, V.; Ekser, B.; van der Windt, D.J.; Hara, H.; Ezzelarab, M.B.; Schuurman, H.J. Progress in pig-to-non-human primate transplantation models (1998–2013): A comprehensive review of the literature. Xenotransplantation 2014, 21, 397–419. [Google Scholar]
- Denner, J. Recent progress in xenotransplantation, with emphasis on virological safety. Ann. Transplant. 2016, 21, 717–727. [Google Scholar]
- Längin, M.; Mayr, T.; Reichart, B.; Michel, S.; Buchholz, S.; Guethoff, S.; Dashkevich, A.; Baehr, A.; Egerer, S.; Bauer, A.; et al. Consistent success in life-supporting porcine cardiac xenotransplantation. Nature 2018, 564, 430–433. [Google Scholar]
- Shin, J.S.; Kim, J.M.; Kim, J.S.; Min, B.H.; Kim, Y.H.; Kim, H.J.; Jang, J.Y.; Yoon, I.H.; Kang, H.J.; Kim, J.; et al. Long-term control of diabetes in immunosuppressed nonhuman primates (NHP) by the transplantation of adult porcine islets. Am. J. Transplant. 2015, 15, 2837–2850. [Google Scholar]
- Denner, J. Xenotransplantation and Hepatitis E virus. Xenotransplantation 2015, 22, 167–173. [Google Scholar]
- Morozov, V.A.; Ludwig, S.; Ludwig, B.; Rotem, A.; Barkai, U.; Bornstein, S.R.; Denner, J. Islet cell transplantation from Göttingen minipigs to cynomolgus monkeys: Analysis of virus safety. Xenotransplantation 2016, 3, 320–327. [Google Scholar]
- Garkavenko, O.; Muzina, M.; Muzina, Z.; Powels, K.; Elliott, R.B.; Croxson, M.C. Monitoring for potentially xenozoonotic viruses in New Zealand pigs. J. Med. Virol. 2004, 72, 338–344. [Google Scholar]
- Wynyard, S.; Nathu, D.; Garkavenko, O.; Denner, J.; Elliott, R. Microbiological safety of the first clinical pig islet xenotransplantation trial in New Zealand. Xenotransplantation 2014, 21, 309–323. [Google Scholar] [Green Version]
- Morozov, V.A.; Wynyard, S.; Matsumoto, S.; Abalovich, A.; Denner, J.; Elliott, R. No PERV transmission during a clinical trial of pig islet cell transplantation. Virus Res. 2017, 227, 34–40. [Google Scholar]
- Denner, J. Xenotransplantation—A special case of One Health. One Health 2017, 3, 17–22. [Google Scholar]
© 2019 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Denner, J. Hepatitis E virus (HEV)—The Future. Viruses 2019, 11, 251. https://doi.org/10.3390/v11030251
Denner J. Hepatitis E virus (HEV)—The Future. Viruses. 2019; 11(3):251. https://doi.org/10.3390/v11030251
Chicago/Turabian StyleDenner, Joachim. 2019. "Hepatitis E virus (HEV)—The Future" Viruses 11, no. 3: 251. https://doi.org/10.3390/v11030251
APA StyleDenner, J. (2019). Hepatitis E virus (HEV)—The Future. Viruses, 11(3), 251. https://doi.org/10.3390/v11030251