Zoonotic origin of hepatitis e

Current Opinion in Virology

Volumn 10, Issue , 2015, Pages 34-41

  Pavio, Nicole ^a,b,c   Meng, Xiang Jin ^d   Doceul, Virginie ^a,b,c  

^a ANSES   (France)

^b INRA   (France)

^c UNIVERSITÉ PARIS EST   (France)

^d CENTER FOR MOLECULAR MEDICINE AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; FOOD CHAIN; FOOD CONTAMINATION; HEPATITIS E; HEPATITIS E VIRUS; HUMAN; NONHUMAN; PATHOGENESIS; PORK; PRIORITY JOURNAL; SWINE; VIRAL CONTAMINATION; VIRUS IDENTIFICATION; VIRUS STRAIN; VIRUS TRANSMISSION; ZOONOSIS; ANIMAL; DISEASE CARRIER; FOOD POISONING; GENETIC VARIABILITY; GENETICS; ISOLATION AND PURIFICATION; MEAT; PHYLOGENY; PHYSIOLOGY; PIG; TRANSMISSION; VIROLOGY;

ANIMALS; DISEASE RESERVOIRS; FOODBORNE DISEASES; GENETIC VARIATION; HEPATITIS E; HEPATITIS E VIRUS; HUMANS; MEAT; PHYLOGENY; SWINE; ZOONOSES;

EID: 84920700916     PISSN: 18796257     EISSN: 18796265     Source Type: Journal    
DOI: 10.1016/j.coviro.2014.12.006     Document Type: Review

References (80)

1. R.H. Purcell, and S.U. Emerson Hepatitis E: an emerging awareness of an old disease J Hepatol 48 2008 494 503
2. N. Kamar, F. Abravanel, S. Lhomme, L. Rostaing, and J. Izopet Hepatitis E virus: chronic infection, extra-hepatic manifestations, and treatment Clin Res Hepatol Gastroenterol 2014 10.1016/j.clinre.2014.07.005
3. S.U. Emerson, D. Anderson, A. Arankalle, X.J. Meng, M. Purdy, G.G. Schlauder, and S.A. Tsarey Hepevirus C.M. Fauquet, M.A. Mayo, J. Maniloff, U. Desselberger, L.A. Ball, Virus Taxonomy, VIIIth Report of the ICTV 2005 Elsevier/Academic Press London 851 855
4. D.B. Smith, M.A. Purdy, and P. Simmonds Genetic variability and the classification of hepatitis E virus J Virol 87 2013 4161 4169
5. X.-J. Meng Zoonotic and foodborne transmission of hepatitis E virus Semin Liver Dis 33 2013 41 49
6. X.J. Meng, D.A. Anderson, V.A. Arankalle, S.U. Emerson, T.J. Harrison, S. Jameel, and H. Okamoto Hepeviridae A.M.Q. King, M.J. Adams, E.B. Carstens, E.J. Lefkowitz, Virus Taxonomy, 9th Report of the ICTV 2012 Elsevier Academic Press London 1021 1028
7. D.B. Smith, P. Simmonds, S. Jameel, S.U. Emerson, T.J. Harrison, X.-J. Meng, H. Okamoto, W.H.M. Van der Poel, and M.A. Purdy Consensus proposals for classification of the family hepeviridae J Gen Virol 2014 10.1099/vir.0.068429-0
8. M.T. Pérez-Gracia, B. Suay, and M.L. Mateos-Lindemann Hepatitis E: an emerging disease Infect Genet Evol J Mol Epidemiol Evol Genet Infect Dis 22 2014 40 59
9. T.-C. Li, K. Chijiwa, N. Sera, T. Ishibashi, Y. Etoh, Y. Shinohara, Y. Kurata, M. Ishida, S. Sakamoto, and N. Takeda Hepatitis E virus transmission from wild boar meat Emerg Infect Dis 11 2005 1958 1960
10. S. Tei, N. Kitajima, K. Takahashi, and S. Mishiro Zoonotic transmission of hepatitis E virus from deer to human beings Lancet 362 2003 371 373
11. M. Riveiro-Barciela, B. Mínguez, R. Gironés, F. Rodriguez-Frías, J. Quer, and M. Buti Phylogenetic demonstration of hepatitis E infection transmitted by pork meat ingestion J Clin Gastroenterol 2014 10.1097/MCG.0000000000000113
12. C. Renou, A.M. Alfonso, and N. Pavio Foodborne transmission of HEV from raw pork liver sausage in France Emerg Infect Dis 2014 (in press)
13. N. Pavio, X.-J. Meng, and C. Renou Zoonotic hepatitis E: animal reservoirs and emerging risks Vet Res 41 2010 46
14. X.J. Meng, R.H. Purcell, P.G. Halbur, J.R. Lehman, D.M. Webb, T.S. Tsareva, J.S. Haynes, B.J. Thacker, and S.U. Emerson A novel virus in swine is closely related to the human hepatitis E virus Proc Natl Acad Sci U S A 94 1997 9860 9865
15. V. S de Paula, M. Wiele, A.H. Mbunkah, A.M. Daniel, M.T. Kingsley, and J. Schmidt-Chanasit Hepatitis E virus genotype 3 strains in domestic pigs, Cameroon Emerg Infect Dis 19 2013 666 668
16. R.W. Hakze-van der Honing, E. van Coillie, A.F.G. Antonis, and W.H.M. van der Poel First isolation of hepatitis E virus genotype 4 in Europe through swine surveillance in the Netherlands and Belgium PLoS ONE 6 2011 e22673
17. I. Monne, L. Ceglie, G. DI Martino, A. Natale, S. Zamprogna, A. Morreale, E. Rampazzo, G. Cattoli, and L. Bonfanti Hepatitis E virus genotype 4 in a pig farm, Italy, 2013 Epidemiol Infect 2014 10.1017/S0950268814001150
18. D.M. Yugo, and X.-J. Meng Hepatitis E virus: foodborne, waterborne and zoonotic transmission Int J Environ Res Public Health 10 2013 4507 4533
19. S. Lhomme, M. Dubois, F. Abravanel, S. Top, S. Bertagnoli, J.-L. Guerin, and J. Izopet Risk of zoonotic transmission of HEV from rabbits J Clin Virol Off Publ Pan Am Soc Clin Virol 58 2013 357 362
20. R. Johne, P. Dremsek, J. Reetz, G. Heckel, M. Hess, and R.G. Ulrich Hepeviridae: an expanding family of vertebrate viruses Infect Genet Evol J Mol Epidemiol Evol Genet Infect Dis 2014 10.1016/j.meegid.2014.06.024
21. M. Nakamura, K. Takahashi, K. Taira, M. Taira, A. Ohno, H. Sakugawa, M. Arai, and S. Mishiro Hepatitis E virus infection in wild mongooses of Okinawa, Japan: demonstration of anti-HEV antibodies and a full-genome nucleotide sequence Hepatol Res Off J Jpn Soc Hepatol 34 2006 137 140
22. T.-C. Li, M. Saito, G. Ogura, O. Ishibashi, T. Miyamura, and N. Takeda Serologic evidence for hepatitis E virus infection in mongoose Am J Trop Med Hyg 74 2006 932 936
23. D.M. Yugo, C.M. Cossaboom, and X.-J. Meng Naturally occurring animal models of human hepatitis E virus infection ILAR J Natl Res Counc Inst Lab Anim Resour 55 2014 187 199
24. K. Takahashi, S. Terada, H. Kokuryu, M. Arai, and S. Mishiro A wild boar-derived hepatitis E virus isolate presumably representing so far unidentified "genotype 5" Kanzo 51 2010 536 538
25. Y. Sato, H. Sato, K. Naka, S. Furuya, H. Tsukiji, K. Kitagawa, Y. Sonoda, T. Usui, H. Sakamoto, and S. Yoshino A nationwide survey of hepatitis E virus (HEV) infection in wild boars in Japan: identification of boar HEV strains of genotypes 3 and 4 and unrecognized genotypes Arch Virol 156 2011 1345 1358
26. P.C.Y. Woo, S.K.P. Lau, J.L.L. Teng, A.K.L. Tsang, M. Joseph, E.Y.M. Wong, Y. Tang, S. Sivakumar, J. Xie, and R. Bai New hepatitis E virus genotype in camels, the Middle East Emerg Infect Dis 20 2014 1044 1048
27. R. Bodewes, J. van der Giessen, B.L. Haagmans, A.D.M.E. Osterhaus, and S.L. Smits Identification of multiple novel viruses, including a parvovirus and a hepevirus, in feces of red foxes J Virol 87 2013 7758 7764
28. J. Lin, H. Norder, H. Uhlhorn, S. Belák, and F. Widén Novel hepatitis E like virus found in Swedish moose J Gen Virol 95 2014 557 570
29. C.J. Payne, T.M. Ellis, S.L. Plant, A.R. Gregory, and G.E. Wilcox Sequence data suggests big liver and spleen disease virus (BLSV) is genetically related to hepatitis E virus Vet Microbiol 68 1999 119 125
30. G. Haqshenas, H.L. Shivaprasad, P.R. Woolcock, D.H. Read, and X.J. Meng Genetic identification and characterization of a novel virus related to human hepatitis E virus from chickens with hepatitis-splenomegaly syndrome in the United States J Gen Virol 82 2001 2449 2462
31. A. Marek, I. Bilic, I. Prokofieva, and M. Hess Phylogenetic analysis of avian hepatitis E virus samples from European and Australian chicken flocks supports the existence of a different genus within the Hepeviridae comprising at least three different genotypes Vet Microbiol 145 2010 54 61
32. F.F. Huang, Z.F. Sun, S.U. Emerson, R.H. Purcell, H.L. Shivaprasad, F.W. Pierson, T.E. Toth, and X.J. Meng Determination and analysis of the complete genomic sequence of avian hepatitis E virus (avian HEV) and attempts to infect rhesus monkeys with avian HEV J Gen Virol 85 2004 1609 1618
33. R. Johne, G. Heckel, A. Plenge-Bönig, E. Kindler, C. Maresch, J. Reetz, A. Schielke, and R.G. Ulrich Novel hepatitis E virus genotype in Norway rats, Germany Emerg Infect Dis 16 2010 1452 1455
34. V.S. Raj, S.L. Smits, S.D. Pas, L.B.V. Provacia, H. Moorman-Roest, A.D.M.E. Osterhaus, and B.L. Haagmans Novel hepatitis E virus in ferrets, the Netherlands Emerg Infect Dis 18 2012 1369 1370
35. J.S. Krog, S.O. Breum, T.H. Jensen, and L.E. Larsen Hepatitis E virus variant in farmed mink, Denmark Emerg Infect Dis 19 2013 2028 2030
36. J.F. Drexler, A. Seelen, V.M. Corman, A. Fumie Tateno, V. Cottontail, R. Melim Zerbinati, F. Gloza-Rausch, S.M. Klose, Y. Adu-Sarkodie, and S.K. Oppong Bats worldwide carry hepatitis E virus-related viruses that form a putative novel genus within the family Hepeviridae J Virol 86 2012 9134 9147
37. C. Dong, J. Meng, X. Dai, J.-H. Liang, A.R. Feagins, X.-J. Meng, N.M. Belfiore, C. Bradford, J.L. Corn, and C. Cray Restricted enzooticity of hepatitis E virus genotypes 1-4 in the United States J Clin Microbiol 49 2011 4164 4172
38. M.D. Saad, H.A. Hussein, M.M. Bashandy, H.H. Kamel, K.C. Earhart, D.J. Fryauff, M. Younan, and A.H. Mohamed Hepatitis E virus infection in work horses in Egypt Infect Genet Evol J Mol Epidemiol Evol Genet Infect Dis 7 2007 368 373
39. W. Zhang, Q. Shen, J. Mou, G. Gong, Z. Yang, L. Cui, J. Zhu, G. Ju, and X. Hua Hepatitis E virus infection among domestic animals in eastern China Zoonoses Public Health 55 2008 291 298
40. B.J. Sanford, S.U. Emerson, R.H. Purcell, R.E. Engle, B.A. Dryman, T.E. Cecere, V. Buechner-Maxwell, D.P. Sponenberg, and X.J. Meng Serological evidence for a hepatitis E virus-related agent in goats in the United States Transbound Emerg Dis 60 2013 538 545
41. T.-C. Li, S. Yoshizaki, Y. Ami, Y. Suzaki, S.P. Yasuda, K. Yoshimatsu, J. Arikawa, N. Takeda, and T. Wakita Susceptibility of laboratory rats against genotypes 1, 3, 4, and rat hepatitis E viruses Vet Microbiol 163 2013 54 61
42. J. Bouquet, S. Tesse, A. Lunazzi, M. Eloit, N. Rose, E. Nicand, and N. Pavio Close similarity between sequences of hepatitis E virus recovered from humans and swine, France, 2008-2009 [Internet] Emerg Infect Dis 2011 17
43. L. Córdoba, A.R. Feagins, T. Opriessnig, C.M. Cossaboom, B.A. Dryman, Y.-W. Huang, and X.-J. Meng Rescue of a genotype 4 human hepatitis E virus from cloned cDNA and characterization of intergenotypic chimeric viruses in cultured human liver cells and in pigs J Gen Virol 93 2012 2183 2194
44. A.R. Feagins, L. Córdoba, B.J. Sanford, B.A. Dryman, Y.-W. Huang, T. LeRoith, S.U. Emerson, and X.-J. Meng Intergenotypic chimeric hepatitis E viruses (HEVs) with the genotype 4 human HEV capsid gene in the backbone of genotype 3 swine HEV are infectious in pigs Virus Res 156 2011 141 146
45. J. Izopet, M. Dubois, S. Bertagnoli, S. Lhomme, S. Marchandeau, S. Boucher, N. Kamar, F. Abravanel, and J.-L. Guérin Hepatitis E virus strains in rabbits and evidence of a closely related strain in humans, France Emerg Infect Dis 18 2012 1274 1281
46. C.M. Cossaboom, L. Córdoba, B.J. Sanford, P. Piñeyro, S.P. Kenney, B.A. Dryman, Y. Wang, and X.-J. Meng Cross-species infection of pigs with a novel rabbit, but not rat, strain of hepatitis E virus isolated in the United States J Gen Virol 93 2012 1687 1695
47. P. Liu, Q.-N. Bu, L. Wang, J. Han, R.-J. Du, Y.-X. Lei, Y.-Q. Ouyang, J. Li, Y.-H. Zhu, and F.-M. Lu Transmission of hepatitis E virus from rabbits to cynomolgus macaques Emerg Infect Dis 19 2013 559 565
48. J. Han, Y. Lei, L. Liu, P. Liu, J. Xia, Y. Zhang, H. Zeng, L. Wang, L. Wang, and H. Zhuang SPF rabbits infected with rabbit hepatitis E virus isolate experimentally showing the chronicity of hepatitis PLOS ONE 9 2014 e99861
49. H. Ma, L. Zheng, Y. Liu, C. Zhao, T.J. Harrison, Y. Ma, S. Sun, J. Zhang, and Y. Wang Experimental infection of rabbits with rabbit and genotypes 1 and 4 hepatitis E viruses PLoS ONE 5 2010 e9160
50. R.H. Purcell, R.E. Engle, M.P. Rood, Y. Kabrane-Lazizi, H.T. Nguyen, S. Govindarajan, M. St Claire, and S.U. Emerson Hepatitis E virus in rats, Los Angeles, California, USA Emerg Infect Dis 17 2011 2216 2222
51. Z.F. Sun, C.T. Larsen, F.F. Huang, P. Billam, F.W. Pierson, T.E. Toth, and X.J. Meng Generation and infectivity titration of an infectious stock of avian hepatitis E virus (HEV) in chickens and cross-species infection of turkeys with avian HEV J Clin Microbiol 42 2004 2658 2662
52. P. Colson, P. Borentain, B. Queyriaux, M. Kaba, V. Moal, P. Gallian, L. Heyries, D. Raoult, and R. Gerolami Pig liver sausage as a source of hepatitis E virus transmission to humans J Infect Dis 202 2010 825 834
53. O. Wichmann, S. Schimanski, J. Koch, M. Kohler, C. Rothe, A. Plentz, W. Jilg, and K. Stark Phylogenetic and case-control study on hepatitis E virus infection in Germany J Infect Dis 198 2008 1732 1741
54. A. Berto, F. Martelli, S. Grierson, and M. Banks Hepatitis E virus in pork food chain, United Kingdom, 2009-2010 Emerg Infect Dis 18 2012 1358 1360
55. I. Di Bartolo, M. Diez-Valcarce, P. Vasickova, P. Kralik, M. Hernandez, G. Angeloni, F. Ostanello, M. Bouwknegt, D. Rodríguez-Lázaro, and I. Pavlik Hepatitis E virus in pork production chain in Czech Republic, Italy, and Spain, 2010 Emerg Infect Dis 18 2012 1282 1289
56. N. Pavio, T. Merbah, and A. Thébault Foodborne hepatitis E: frequent detection of HEV in raw pork liver foods Emerg Infect Dis 20 11 2014 1925 1927 10.3201/eid2011.140891
57. A. Berto, S. Grierson, R. Hakze-van der Honing, F. Martelli, R. Johne, J. Reetz, R.G. Ulrich, N. Pavio, W.H.M. Van der Poel, and M. Banks Hepatitis E virus in pork liver sausage, France Emerg Infect Dis 19 2013 264 266
58. A.R. Feagins, T. Opriessnig, D.K. Guenette, P.G. Halbur, and X.-J. Meng Detection and characterization of infectious Hepatitis E virus from commercial pig livers sold in local grocery stores in the USA J Gen Virol 88 2007 912 917
59. N. Kamar, L. Rostaing, and J. Izopet Hepatitis E virus infection in immunosuppressed patients: natural history and therapy Semin Liver Dis 33 2013 62 70
60. B. Said, S. Ijaz, G. Kafatos, L. Booth, H.L. Thomas, A. Walsh, M. Ramsay, D. Morgan Hepatitis E Incident Investigation Team Hepatitis E outbreak on cruise ship Emerg Infect Dis 15 2009 1738 1744
61. M. Grodzki, J. Schaeffer, J.-C. Piquet, J.-C. Le Saux, J. Chevé, J. Ollivier, J. Le Pendu, and F.S. Le Guyader Bioaccumulation efficiency, tissue distribution, and environmental occurrence of hepatitis e virus in bivalve shellfish from France Appl Environ Microbiol 80 2014 4269 4276
62. C. Crossan, P.J. Baker, J. Craft, Y. Takeuchi, H.R. Dalton, and L. Scobie Hepatitis E virus genotype 3 in shellfish, United Kingdom Emerg Infect Dis 18 2012 2085 2087
63. C. Kasorndorkbua, T. Opriessnig, F.F. Huang, D.K. Guenette, P.J. Thomas, X.-J. Meng, and P.G. Halbur Infectious swine hepatitis E virus is present in pig manure storage facilities on United States farms, but evidence of water contamination is lacking Appl Environ Microbiol 71 2005 7831 7837
64. S.A. Rutjes, W.J. Lodder, F. Lodder-Verschoor, H.H.J.L. van den Berg, H. Vennema, E. Duizer, M. Koopmans, and A.M. de Roda Husman Sources of hepatitis E virus genotype 3 in The Netherlands Emerg Infect Dis 15 2009 381 387
65. J. Brassard, M.-J. Gagné, M. Généreux, and C. Côté Detection of human food-borne and zoonotic viruses on irrigated, field-grown strawberries Appl Environ Microbiol 78 2012 3763 3766
66. L. Maunula, A. Kaupke, P. Vasickova, K. Söderberg, I. Kozyra, S. Lazic, W.H.M. van der Poel, M. Bouwknegt, S. Rutjes, and K.A. Willems Tracing enteric viruses in the European berry fruit supply chain Int J Food Microbiol 167 2013 177 185
67. P. Kokkinos, I. Kozyra, S. Lazic, M. Bouwknegt, S. Rutjes, K. Willems, R. Moloney, A.M. de Roda Husman, A. Kaupke, and E. Legaki Harmonised investigation of the occurrence of human enteric viruses in the leafy green vegetable supply chain in three European countries Food Environ Virol 4 2012 179 191
68. A.R. Feagins, T. Opriessnig, D.K. Guenette, P.G. Halbur, and X.J. Meng Inactivation of infectious hepatitis E virus present in commercial pig livers sold in local grocery stores in the United States Int J Food Microbiol 123 2008 32 37
69. E. Barnaud, S. Rogée, P. Garry, N. Rose, and N. Pavio Thermal inactivation of infectious hepatitis E virus in experimentally contaminated food Appl Environ Microbiol 78 2012 5153 5159
70. X.J. Meng, B. Wiseman, F. Elvinger, D.K. Guenette, T.E. Toth, R.E. Engle, S.U. Emerson, and R.H. Purcell Prevalence of antibodies to hepatitis E virus in veterinarians working with swine and in normal blood donors in the United States and other countries J Clin Microbiol 40 2002 117 122
71. H. Chaussade, E. Rigaud, A. Allix, A. Carpentier, A. Touzé, D. Delzescaux, P. Choutet, N. Garcia-Bonnet, and P. Coursaget Hepatitis E virus seroprevalence and risk factors for individuals in working contact with animals J Clin Virol Off Publ Pan Am Soc Clin Virol 58 2013 504 508
72. S.A. Tsarev, T.S. Tsareva, S.U. Emerson, M.K. Rippy, P. Zack, M. Shapiro, and R.H. Purcell Experimental hepatitis E in pregnant rhesus monkeys: failure to transmit hepatitis E virus (HEV) to offspring and evidence of naturally acquired antibodies to HEV J Infect Dis 172 1995 31 37
73. X.J. Meng, P.G. Halbur, J.S. Haynes, T.S. Tsareva, J.D. Bruna, R.L. Royer, R.H. Purcell, and S.U. Emerson Experimental infection of pigs with the newly identified swine hepatitis E virus (swine HEV), but not with human strains of HEV Arch Virol 143 1998 1405 1415
74. X. Li, S. Kamili, and K. Krawczynski Quantitative detection of hepatitis E virus RNA and dynamics of viral replication in experimental infection J Viral Hepat 13 2006 835 839
75. J.C. Erker, S.M. Desai, G.G. Schlauder, G.J. Dawson, and I.K. Mushahwar A hepatitis E virus variant from the United States: molecular characterization and transmission in cynomolgus macaques J Gen Virol 80 Pt 3 1999 681 690
76. X.J. Meng, P.G. Halbur, M.S. Shapiro, S. Govindarajan, J.D. Bruna, I.K. Mushahwar, R.H. Purcell, and S.U. Emerson Genetic and experimental evidence for cross-species infection by swine hepatitis E virus J Virol 72 1998 9714 9721
77. H. Ma, X. Song, T.J. Harrison, R. Li, G. Huang, H. Zhang, W. Kong, and Y. Wang Immunogenicity and efficacy of a bacterially expressed HEV ORF3 peptide, assessed by experimental infection of primates Arch Virol 154 2009 1641 1648
78. A.R. Feagins, T. Opriessnig, Y.W. Huang, P.G. Halbur, and X.J. Meng Cross-species infection of specific-pathogen-free pigs by a genotype 4 strain of human hepatitis E virus J Med Virol 80 2008 1379 1386
79. V.A. Arankalle, L.P. Chobe, and M.S. Chadha Type-IV Indian swine HEV infects rhesus monkeys J Viral Hepat 13 2006 742 745
80. V.A. Arankalle, L.P. Chobe, M.V. Joshi, M.S. Chadha, B. Kundu, and A.M. Walimbe Human and swine hepatitis E viruses from Western India belong to different genotypes J Hepatol 36 2002 417 425