Epidemiology of mammalian hepatitis e virus infection

Intervirology

Volumn 56, Issue 2, 2013, Pages 67-83

  Kaba, Mamadou ^a,b   Moal, Valérie ^c   Gérolami, René ^c   Colson, Philippe ^a,b  

^a AIX MARSEILLE UNIVERSITY   (France)

^b TIMONE HOSPITAL   (France)

^c HÔPITAL DE LA CONCEPTION   (France)

Author keywords

Autochthonous hepatitis E; Epidemiology; Foodborne transmission; Hepatitis E virus; Pig; Prevention; Vaccine; Zoonosis; Zoonotic transmission

Indexed keywords

HEPATITIS E VACCINE; VIRUS PROTEIN; VIRUS RNA; HEPATITIS E ANTIBODY; IMMUNOGLOBULIN G;

BLOOD TRANSFUSION; DEVELOPED COUNTRY; DEVELOPING COUNTRY; DRUG EFFICACY; FOOD POISONING; GENOTYPE; GEOGRAPHIC DISTRIBUTION; HEPATITIS E; HUMAN; NONHUMAN; PHASE 3 CLINICAL TRIAL (TOPIC); PHYLOGENY; PRIORITY JOURNAL; REVIEW; SEROPREVALENCE; TAXONOMY; VERTICAL TRANSMISSION; VIRUS GENE; VIRUS TRANSMISSION; WATER CONTAMINATION; WATER SUPPLY; 3' UNTRANSLATED REGION; ELECTRON MICROSCOPY; ENDEMIC DISEASE; GENOME ANALYSIS; HEPATITIS E VIRUS; PROSPECTIVE STUDY; RETROSPECTIVE STUDY;

ANIMALS; HEPATITIS ANTIBODIES; HEPATITIS E; HEPATITIS E VIRUS; HUMANS; PREVALENCE; PROSPECTIVE STUDIES; RETROSPECTIVE STUDIES; SWINE; ZOONOSES;

HEPATITIS E VIRUS; MAMMALIA; NON-A, NON-B HEPATITIS VIRUS; SUIDAE; SUS;

EID: 84874391249     PISSN: 03005526     EISSN: 14230100     Source Type: Journal    
DOI: 10.1159/000342301     Document Type: Review

References (165)

1. Purcell RH, Emerson SU: Hepatitis E: an emerging awareness of an old disease. J Hepatol 2008; 48: 494-503.
2. Escriba JM, Nakoune E, Recio C, Massamba PM, Matsika-Claquin MD, Goumba C, Rose AM, Nicand E, Garcia E, Leklegban C, Koffi B: Hepatitis E, Central African Republic. Emerg Infect Dis 2008; 14: 681-683.
3. Verma V, Arankalle VA: Hepatitis E virusbased evaluation of a virion concentration method and detection of enteric viruses in environmental samples by multiplex nested RTPCR. J Appl Microbiol 2010; 108: 1630-1641.
4. Howard CM, Handzel T, Hill VR, Grytdal SP, Blanton C, Kamili S, Drobeniuc J, Hu D, Teshale E: Novel risk factors associated with hepatitis E virus infection in a large outbreak in northern Uganda: results from a case-control study and environmental analysis. Am J Trop Med Hyg 2010; 83: 1170-1173.
5. Teshale EH, Howard CM, Grytdal SP, Handzel TR, Barry V, Kamili S, Drobeniuc J, Okware S, Downing R, Tappero JW, Bakamutumaho B, Teo CG, Ward JW, Holmberg SD, Hu DJ: Hepatitis E epidemic, Uganda. Emerg Infect Dis 2010; 16: 126-129.
6. Velazquez O, Stetler HC, Avila C, Ornelas G, Alvarez C, Hadler SC, Bradley DW, Sepulveda J: Epidemic transmission of enterically transmitted non-A, non-B hepatitis in Mexico, 1986-1987. JAMA 1990; 263: 3281-3285.
7. Khuroo MS: Study of an epidemic of non-A, non-B hepatitis. Possibility of another human hepatitis virus distinct from post-transfusion non-A, non-B type. Am J Med 1980; 68: 818-824.
8. Wong DC, Purcell RH, Sreenivasan MA, Prasad SR, Pavri KM: Epidemic and endemic hepatitis in India: evidence for a non-A, non-B hepatitis virus aetiology. Lancet 1980; 2: 876-879.
9. Arankalle VA, Chadha MS, Tsarev SA, Emerson SU, Risbud AR, Banerjee K, Purcell RH: Seroepidemiology of water-borne hepatitis in India and evidence for a third enterically-transmitted hepatitis agent. Proc Natl Acad Sci USA 1994; 91: 3428-3432.
10. Skidmore SJ, Yarbough PO, Gabor KA, Reyes GR: Hepatitis E virus: the cause of a waterbourne hepatitis outbreak. J Med Virol 1992; 37: 58-60.
11. Balayan MS, Andjaparidze AG, Savinskaya SS, Ketiladze ES, Braginsky DM, Savinov AP, Poleschuk VF: Evidence for a virus in non-A, non-B hepatitis transmitted via the fecaloral route. Intervirology 1983; 20: 23-31.
12. Reyes GR, Purdy MA, Kim JP, Luk KC, Young LM, Fry KE, Bradley DW: Isolation of a cDNA from the virus responsible for enterically transmitted non-A, non-B hepatitis. Science 1990; 247: 1335-1339.
13. Balayan MS: Epidemiology of hepatitis E virus infection. J Viral Hepat 1997; 4: 155-165.
14. Lewis HC, Wichmann O, Duizer E: Transmission routes and risk factors for autochthonous hepatitis E virus infection in Europe: a systematic review. Epidemiol Infect 2010; 138: 145-166.
15. Wilhelm BJ, Rajic A, Greig J, Waddell L, Trottier G, Houde A, Harris J, Borden LN, Price C: A systematic review/meta-analysis of primary research investigating swine, pork or pork products as a source of zoonotic hepatitis E virus. Epidemiol Infect 2011; 139: 1127-1144.
16. Kamar N, Selves J, Mansuy JM, Ouezzani L, Peron JM, Guitard J, Cointault O, Esposito L, Abravanel F, Danjoux M, Durand D, Vinel JP, Izopet J, Rostaing L: Hepatitis E virus and chronic hepatitis in organ-transplant recipients. N Engl J Med 2008; 358: 811-817.
17. Gerolami R, Moal V, Colson P: Chronic hepatitis E with cirrhosis in a kidney-transplant recipient. N Engl J Med 2008; 358: 859-860.
18. Miyamura T: Hepatitis E virus infection in developed countries. Virus Res 2011; 161: 40-46.
19. Colson P, Moal V, Motte A, Borentain P, Henry M, Dhiver C, Ressiot E, Garcia S, Brouqui P, Tamalet C, Gerolami R: 39 PCRdocumented cases of acute or chronic hepatitis E over a 2-year period in Marseilles, South-eastern France. Hepatology 2008; 48: 1185A-1186A.
20. Renou C, Moreau X, Pariente A, Cadranel JF, Maringe E, Morin T, Causse X, Payen JL, Izopet J, Nicand E, Bourliere M, Penaranda G, Hardwigsen J, Gerolami R, Peron JM, Pavio N: A national survey of acute hepatitis E in France. Aliment Pharmacol Ther 2008; 27: 1086-1093.
21. Mansuy JM, Abravanel F, Miedouge M, Mengelle C, Merviel C, Dubois M, Kamar N, Rostaing L, Alric L, Moreau J, Peron JM, Izopet J: Acute hepatitis E in south-west France over a 5-year period. J Clin Virol 2009; 44: 74-77.
22. Dalton HR, Stableforth W, Thurairajah P, Hazeldine S, Remnarace R, Usama W, Farrington L, Hamad N, Sieberhagen C, Ellis V, Mitchell J, Hussaini SH, Banks M, Ijaz S, Bendall RP: Autochthonous hepatitis E in Southwest England: natural history, complications and seasonal variation, and hepatitis E virus IgG seroprevalence in blood donors, the elderly and patients with chronic liver disease. Eur J Gastroenterol Hepatol 2008; 20: 784-790.
23. Wichmann O, Schimanski S, Koch J, Kohler M, Rothe C, Plentz A, Jilg W, Stark K: Phylogenetic and case-control study on hepatitis E virus infection in Germany. J Infect Dis 2008; 198: 1732-1741.
24. 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.
25. Kaba M, Davoust B, Marie JL, Barthet M, Henry M, Tamalet C, Raoult D, Colson P: Frequent transmission of hepatitis E virus among piglets in farms in Southern France. J Med Virol 2009; 81: 1750-1759.
26. Kaba M, Colson P, Musongela JP, Tshilolo L, Davoust B: Detection of hepatitis E virus of genotype 3 in a farm pig in Kinshasa (Democratic Republic of the Congo). Infect Genet Evol 2010; 10: 154-157.
27. Kaba M, Davoust B, Marie JL, Colson P: Detection of hepatitis E virus in wild boar (Sus scrofa) livers. Vet J 2010; 186: 259-261.
28. Kaba M, Davoust B, Cabre O, Colson P: Hepatitis E virus genotype 3f in pigs in New Caledonia. Aust Vet J 2011; 89: 496-499.
29. Li TC, Chijiwa K, Sera N, Ishibashi T, Etoh Y, Shinohara Y, Kurata Y, Ishida M, Sakamoto S, Takeda N, Miyamura T: Hepatitis E virus transmission from wild boar meat. Emerg Infect Dis 2005; 11: 1958-1960.
30. Colson P, Dhiver C, Poizot-Martin I, Tamalet C, Gerolami R: Acute and chronic hepatitis E in patients infected with human immunodeficiency virus. J Viral Hepat 2011; 18: 227-228.
31. Mallet V, Nicand E, Sultanik P, Chakvetadze C, Tesse S, Thervet E, Mouthon L, Sogni P, Pol S: Brief communication: case reports of ribavirin treatment for chronic hepatitis E. Ann Intern Med 2010; 153: 85-89.
32. Colson P, Kaba M, Moreau J, Brouqui P: Hepatitis E in an HIV-infected patient. J Clin Virol 2009; 45: 269-271.
33. Dalton HR, Bendall RP, Keane FE, Tedder RS, Ijaz S: Persistent carriage of hepatitis E virus in patients with HIV infection. N Engl J Med 2009; 361: 1025-1027.
34. Kaba M, Richet H, Ravaux I, Moreau J, Poizot-Martin I, Motte A, Nicolino-Brunet C, Dignat-George F, Menard A, Dhiver C, Brouqui P, Colson P: Hepatitis E virus infection in patients infected with the human immunodeficiency virus. J Med Virol 2011; 83: 1704-1716.
35. Emerson SU, Anderson D, Arankalle A, Meng XJ, Purdy M, Schlauder GG, Tsarev SA: Hepevirus Virus Taxonomy: The Eighth Report of the International Committee on Taxonomy of Viruses. London, Elsevier, 2005, pp 853-857
36. Balayan MS: Type E hepatitis: state of the art. Int J Infect Dis 1997; 2: 113-120.
37. Koonin EV, Gorbalenya AE, Purdy MA, Rozanov MN, Reyes GR, Bradley DW: Computer-assisted assignment of functional domains in the nonstructural polyprotein of hepatitis E virus: delineation of an additional group of positive-strand RNA plant and animal viruses. Proc Natl Acad Sci USA 1992; 89: 8259-8263.
38. Tam AW, Smith MM, Guerra ME, Huang CC, Bradley DW, Fry KE, Reyes GR: Hepatitis E virus (HEV): molecular cloning and sequencing of the full-length viral genome. Virology 1991; 185: 120-131.
39. Ahmad I, Holla RP, Jameel S: Molecular virology of hepatitis E virus. Virus Res 2011; 161: 47-58.
40. Emerson SU, Clemente-Casares P, Moiduddin N, Arankalle VA, Torian U, Purcell RH: Putative neutralization epitopes and broad cross-genotype neutralization of Hepatitis E virus confirmed by a quantitative cell-culture assay. J Gen Virol 2006; 87: 697-704.
41. Lu L, Li C, Hagedorn CH: Phylogenetic analysis of global hepatitis E virus sequences: genetic diversity, subtypes and zoonosis. Rev Med Virol 2006; 16: 5-36.
42. Drexler JF, Seelen A, Corman VM, Fumie TA, Cottontail V, Melim ZR, Gloza-Rausch F, Klose SM, du-Sarkodie Y, Oppong SK, Kalko EK, Osterman A, Rasche A, Adam A, Muller MA, Ulrich RG, Leroy EM, Lukashev AN, Drosten C: Bats worldwide carry hepatitis E-related viruses that form a putative novel genus within the family Hepeviridae. J Virol 2012; 86: 9134-9147.
43. Vivek R, Nihal L, Illiayaraja J, Reddy PK, Sarkar R, Eapen CE, Kang G: Investigation of an epidemic of Hepatitis E in Nellore in South India. Trop Med Int Health 2010; 15: 1333-1339.
44. Delarocque-Astagneau E, Abravanel F, Moshen A, Le FL, Gad RR, El-Daly M, Ibrahim EM, El-Aidy S, Lashin T, El-Hoseiny M, Izopet J, Mohamed MK, Fontanet A, Abdel HM: Epidemiological and virological characteristics of symptomatic acute hepatitis E in Greater Cairo, Egypt. Clin Microbiol Infect 2012; 18: 982-988.
45. Kumar S, Ratho RK, Chawla YK, Chakraborti A: The incidence of sporadic viral hepatitis in North India: a preliminary study. Hepatobiliary Pancreat Dis Int 2007; 6: 596-599.
46. Patra S, Kumar A, Trivedi SS, Puri M, Sarin SK: Maternal and fetal outcomes in pregnant women with acute hepatitis E virus infection. Ann Intern Med 2007; 147: 28-33.
47. Mamun AM, Rahman S, Khan M, Karim F: HEV infection as an aetiologic factor for acute hepatitis: experience from a tertiary hospital in Bangladesh. J Health Popul Nutr 2009; 27: 14-19.
48. Pavio N, Meng XJ, Renou C: Zoonotic hepatitis E: animal reservoirs and emerging risks. Vet Res 2010; 41: 46.
49. Colson P, Swiader L, Motte A, Ferretti A, Borentain P, Gérolami R: Circulation of almost genetically-identical hepatitis E virus of genotype 4 in France. J Clin Virol 2012; 55: 181-183.
50. Dalton HR, Fellows HJ, Gane EJ, Wong P, Gerred S, Schroeder B, Croxson MC, Garkavenko O: Hepatitis E in New Zealand. J Gastroenterol Hepatol 2007; 22: 1236-1240.
51. Hakze-van der Honing RW, van CE, Antonis AF, van der Poel WH: First isolation of hepatitis E virus genotype 4 in Europe through swine surveillance in the Netherlands and Belgium. PLoS One 2011; 6:e22673.
52. Meng XJ, Purcell RH, Halbur PG, Lehman JR, Webb DM, Tsareva TS, Haynes JS, Thacker BJ, Emerson SU: A novel virus in swine is closely related to the human hepatitis E virus. Proc Natl Acad Sci USA 1997; 94: 9860-9865.
53. Purdy MA, Khudyakov YE: Evolutionary history and population dynamics of hepatitis E virus. PLoS One 2010; 5:e14376.
54. Xia H, Wahlberg N, Belak S, Meng XJ, Liu L: The emergence of genotypes 3 and 4 hepatitis E virus in swine and humans: a phylogenetic perspective. Arch Virol 2011; 156: 121-124.
55. Wang H, Zhang W, Ni B, Shen H, Song Y, Wang X, Shao S, Hua X, Cui L: Recombination analysis reveals a double recombination event in hepatitis E virus. Virol J 2010; 7: 129.
56. Moal V, Gerolami R, Colson P: First human case of co-infection with two different subtypes of hepatitis E virus. Intervirology 2012, E-pub ahead of print.
57. de Deus N, Casas M, Peralta B, Nofrarias M, Pina S, Martin M, Segales J: Hepatitis E virus infection dynamics and organic distribution in naturally infected pigs in a farrow-to-finish farm. Vet Microbiol 2008; 132: 19-28.
58. Grandadam M, Tebbal S, Caron M, Siriwardana M, Larouze B, Koeck JL, Buisson Y, Enouf V, Nicand E: Evidence for hepatitis E virus quasispecies. J Gen Virol 2004; 85: 3189-3194.
59. Corwin AL, Khiem HB, Clayson ET, Pham KS, Vo TT, Vu TY, Cao TT, Vaughn D, Merven J, Richie TL, Putri MP, He J, Graham R, Wignall FS, Hyams KC: A waterborne outbreak of hepatitis E virus transmission in Southwestern Vietnam. Am J Trop Med Hyg 1996; 54: 559-562.
60. Borgen K, Herremans T, Duizer E, Vennema H, Rutjes S, Bosman A, de Roda Husman AM, Koopmans M: Non-travel related hepatitis E virus genotype 3 infections in the Netherlands; a case series 2004-2006. BMC Infect Dis 2008; 8: 61.
61. Guthmann JP, Klovstad H, Boccia D, Hamid N, Pinoges L, Nizou JY, Tatay M, Diaz F, Moren A, Grais RF, Ciglenecki I, Nicand E, Guerin PJ: A large outbreak of hepatitis E among a displaced population in Darfur, Sudan, 2004: the role of water treatment methods. Clin Infect Dis 2006; 42: 1685-1691.
62. Matsubayashi K, Kang JH, Sakata H, Takahashi K, Shindo M, Kato M, Sato S, Kato T, Nishimori H, Tsuji K, Maguchi H, Yoshida J, Maekubo H, Mishiro S, Ikeda H: A case of transfusion-transmitted hepatitis E caused by blood from a donor infected with hepatitis E virus via zoonotic food-borne route. Transfusion 2008; 48: 1368-1375.
63. Colson P, Coze C, Gallian P, Henry M, De MP, Tamalet C: Transfusion-associated hepatitis E, France. Emerg Infect Dis 2007; 13: 648-649.
64. Khuroo MS, Kamili S, Khuroo MS: Clinical course and duration of viremia in vertically transmitted hepatitis E virus (HEV) infection in babies born to HEV-infected mothers. J Viral Hepat 2009; 16: 519-523.
65. Kumar RM, Uduman S, Rana S, Kochiyil JK, Usmani A, Thomas L: Sero-prevalence and mother-to-infant transmission of hepatitis E virus among pregnant women in the United Arab Emirates. Eur J Obstet Gynecol Reprod Biol 2001; 100: 9-15.
66. Kumar A, Beniwal M, Kar P, Sharma JB, Murthy NS: Hepatitis E in pregnancy. Int J Gynaecol Obstet 2004; 85: 240-244.
67. Romano L, Paladini S, Tagliacarne C, Canuti M, Bianchi S, Zanetti AR: Hepatitis E in Italy: a long-term prospective study. J Hepatol 2011; 54: 34-40.
68. Somani SK, Aggarwal R, Naik SR, Srivastava S, Naik S: A serological study of intrafamilial spread from patients with sporadic hepatitis E virus infection. J Viral Hepat 2003; 10: 446-449.
69. Siddiqui AR, Jooma RA, Smego RA Jr: Nosocomial outbreak of hepatitis E infection in Pakistan with possible parenteral transmission. Clin Infect Dis 2005; 40: 908-909.
70. Neogi DK, Bhattacharya N, De PN, Chakravarti T, Hati AK, Prakash C, Datta KK, Mukherjee KK: An institutional outbreak of hepatitis E-reported first time from Calcutta City. J Commun Dis 1995; 27: 229-233.
71. Schlosser B, Stein A, Neuhaus R, Pahl S, Ramez B, Kruger DH, 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.
72. Meng XJ, Halbur PG, Shapiro MS, Govindarajan S, Bruna JD, Mushahwar IK, Purcell RH, Emerson SU: Genetic and experimental evidence for cross-species infection by swine hepatitis E virus. J Virol 1998; 72: 9714-9721.
73. Hazam RK, Singla R, Kishore J, Singh S, Gupta RK, Kar P: Surveillance of hepatitis E virus in sewage and drinking water in a resettlement colony of Delhi: what has been the experience? Arch Virol 2010; 155; 1227-1233.
74. Martolia HC, Hutin Y, Ramachandran V, Manickam P, Murhekar M, Gupte M: An outbreak of hepatitis E tracked to a spring in the foothills of the Himalayas, India, 2005. Indian J Gastroenterol 2009; 28: 99-101.
75. Sarguna P, Rao A, Sudha Ramana KN: Outbreak of acute viral hepatitis due to hepatitis E virus in Hyderabad. Indian J Med Microbiol 2007; 25: 378-382.
76. El-Esnawy NA, Gamil MA, El-Wakkad AS: Detection of hepatitis E virus in greater Cairo. Two wastewater treatment plants and its prevalence among workers of these plants. J Egypt Public Health Assoc 1998; 73: 597-619.
77. Ceylan A, Ertem M, Ilcin E, Ozekinci T: A special risk group for hepatitis E infection: Turkish agricultural workers who use untreated waste water for irrigation. Epidemiol Infect 2003; 131: 753-756.
78. Kitajima M, Matsubara K, Sour S, Haramoto E, Katayama H, Ohgaki S: First detection of genotype 3 hepatitis E virus RNA in river water in Cambodia. Trans R Soc Trop Med Hyg 2009; 103: 955-957.
79. Rutjes SA, Lodder WJ, Lodder-Verschoor F, van den Berg HH, Vennema H, Duizer E, Koopmans M, de Roda Husman AM: Sources of hepatitis E virus genotype 3 in the Netherlands. Emerg Infect Dis 2009; 15: 381-387.
80. Clemente-Casares P, Rodriguez-Manzano J, Girones R: Hepatitis E virus genotype 3 and sporadically also genotype 1 circulate in the population of Catalonia, Spain. J Water Health 2009; 7: 664-673.
81. Song YJ, Jeong HJ, Kim YJ, Lee SW, Lee JB, Park SY, Song CS, Park HM, Choi IS: Analysis of complete genome sequences of swine hepatitis E virus and possible risk factors for transmission of HEV to humans in Korea. J Med Virol 2010; 82: 583-591.
82. Brassard J, Gagne MJ, Genereux M, Cote C: Detection of human food-borne and zoonotic viruses on irrigated, field-grown strawberries. Appl Environ Microbiol 2012; 78: 3763-3766.
83. Galiana C, Fernandez-Barredo S, Garcia A, Gomez MT, Perez-Gracia MT: Occupational exposure to hepatitis E virus (HEV) in swine workers. Am J Trop Med Hyg 2008; 78: 1012-1015.
84. Tumerelle E, Domart M: Hepatite E autochtone presummee professionnelle: a propos d'un cas. Arch Mal Prof 2000; 61: 318-323.
85. Bouwknegt M, Lodder-Verschoor F, van der Poel WH, Rutjes SA, de Roda Husman AM: Hepatitis E virus RNA in commercial porcine livers in the Netherlands. J Food Prot 2007; 70: 2889-2895.
86. Feagins AR, Opriessnig T, Guenette DK, Halbur PG, Meng XJ: Inactivation of infectious hepatitis E virus present in commercial pig livers sold in local grocery stores in the United States. Int J Food Microbiol 2008; 123: 32-37.
87. Miyashita K, Kang JH, Saga A, Takahashi K, Shimamura T, Yasumoto A, Fukushima H, Sogabe S, Konishi K, Uchida T, Fujinaga A, Matsui T, Sakurai Y, Tsuji K, Maguchi H, Taniguchi M, Abe N, Fazle Akbar SM, Arai M, Mishiro S: Three cases of acute or fulminant hepatitis E caused by ingestion of pork meat and entrails in Hokkaido, Japan: zoonotic food-borne transmission of hepatitis E virus and public health concerns. Hepatol Res 2012; 42: 870-878.
88. Legrand-Abravanel F, Kamar N, Sandres-Saune K, Garrouste C, Dubois M, Mansuy JM, Muscari F, Sallusto F, Rostaing L, Izopet J: Characteristics of autochthonous hepatitis E virus infection in solid-organ transplant recipients in France. J Infect Dis 2010; 202: 835-844.
89. Surya IG, Kornia K, Suwardewa TG, Mulyanto, Tsuda F, Mishiro S: Serological markers of hepatitis B, C, and E viruses and human immunodeficiency virus type-1 infections in pregnant women in Bali, Indonesia. J Med Virol 2005; 75: 499-503.
90. Toyoda K, Furusyo N, Takeoka H, Murata M, Sawayama Y, Hayashi J: Epidemiological study of hepatitis E virus infection in the general population of Okinawa, Kyushu, Japan. J Gastroenterol Hepatol 2008; 23: 1885-1890.
91. Colson P, Kaba M, Bernit E, Motte A, Tamalet C: Hepatitis E associated with surgical training on pigs. Lancet 2007; 370: 935.
92. Mansuy JM, Legrand-Abravanel F, Calot JP, Peron JM, Alric L, Agudo S, Rech H, Destruel F, Izopet J: High prevalence of anti-hepatitis E virus antibodies in blood donors from South West France. J Med Virol 2008; 80: 289-293.
93. Christensen PB, Engle RE, Hjort C, Homburg KM, Vach W, Georgsen J, Purcell RH: Time trend of the prevalence of hepatitis E antibodies among farmers and blood donors: a potential zoonosis in Denmark. Clin Infect Dis 2008; 47: 1026-1031.
94. Kuniholm MH, Purcell RH, McQuillan GM, Engle RE, Wasley A, Nelson KE: Epidemiology of hepatitis E virus in the United States: results from the Third National Health and Nutrition Examination Survey, 1988-1994. J Infect Dis 2009; 200: 48-56.
95. Ekser B, Ezzelarab M, Hara H, van der Windt DJ, Wijkstrom M, Bottino R, Trucco M, Cooper DK: Clinical xenotransplantation: the next medical revolution? Lancet 2012; 379: 672-683.
96. Said B, Ijaz S, Kafatos G, Booth L, Thomas HL, Walsh A, Ramsay M, Morgan D: Hepatitis E outbreak on cruise ship. Emerg Infect Dis 2009; 15: 1738-1744.
97. Li TC, Miyamura T, Takeda N: Detection of hepatitis E virus RNA from the bivalve Yamato-Shijimi ( Corbicula japonica ) in Japan. Am J Trop Med Hyg 2007; 76: 170-172.
98. Arankalle VA, Chobe LP: Retrospective analysis of blood transfusion recipients: evidence for post-transfusion hepatitis E. Vox Sang 2000; 79: 72-74.
99. Sakata H, Matsubayashi K, Takeda H, Sato S, Kato T, Hino S, Tadokoro K, Ikeda H: A nationwide survey for hepatitis E virus prevalence in Japanese blood donors with elevated alanine aminotransferase. Transfusion 2008; 48: 2568-2576.
100. Takeda H, Matsubayashi K, Sakata H, Sato S, Kato T, Hino S, Tadokoro K, Ikeda H: A nationwide survey for prevalence of hepatitis E virus antibody in qualified blood donors in Japan. Vox Sang 2010; 99: 307-313.
101. Mansuy JM, Bendall R, Legrand-Abravanel F, Saune K, Miedouge M, Ellis V, Rech H, Destruel F, Kamar N, Dalton HR, Izopet J: Hepatitis E virus antibodies in blood donors, France. Emerg Infect Dis 2011; 17: 2309-2312.
102. Khuroo MS, Kamili S, Yattoo GN: Hepatitis E virus infection may be transmitted through blood transfusions in an endemic area. J Gastroenterol Hepatol 2004; 19: 778-784.
103. Nicand E, Grandadam M, Teyssou R, Rey JL, Buisson Y: Viraemia and faecal shedding of HEV in symptom-free carriers. Lancet 2001; 357: 68-69.
104. Adlhoch C, Kaiser M, Pauli G, Koch J, Meisel H: Indigenous hepatitis E virus infection of a plasma donor in Germany. Vox Sang 2009; 97: 303-308.
105. Renou C, Pariente A, Cadranel JF, Nicand E, Pavio N: Clinically silent forms may partly explain the rarity of acute cases of autochthonous genotype 3c hepatitis E infection in France. J Clin Virol 2011; 51: 139-141.
106. Guo QS, Yan Q, Xiong JH, Ge SX, Shih JW, Ng MH, Zhang J, Xia NS: Prevalence of hepatitis E virus in Chinese blood donors. J Clin Microbiol 2010; 48: 317-318.
107. Baylis SA, Gartner T, Nick S, Ovemyr J, Blumel J: Occurrence of hepatitis E virus RNA in plasma donations from Sweden, Germany and the United States. Vox Sang 2012; 103: 89-90.
108. Baylis SA, Hanschmann KM, Blumel J, Nubling CM: Standardization of hepatitis E virus (HEV) nucleic acid amplification technique-based assays: an initial study to evaluate a panel of HEV strains and investigate laboratory performance. J Clin Microbiol 2011; 49: 1234-1239.
109. Ijaz S, Szypulska R, Tettmar KI, Kitchen A, Tedder RS: Detection of hepatitis E virus RNA in plasma mini-pools from blood donors in England. Vox Sang 2012; 102: 272.
110. Hosseini-Moghaddam SM, Zarei A, Alavian SM, Mansouri M: Hepatitis E virus infection: a general review with a focus on hemodialysis and kidney transplant patients. Am J Nephrol 2010; 31: 398-407.
111. Toyoda H, Honda T, Hayashi K, Katano Y, Goto H, Kumada T, Takahashi K, Abe N, Mishiro S, Takamatsu J: Prevalence of hepatitis E virus IgG antibody in Japanese patients with hemophilia. Intervirology 2008; 51: 21-25.
112. Kaba M, Brouqui P, Richet H, Badiaga S, Gallian P, Raoult D, Colson P: Hepatitis E virus infection in sheltered homeless persons, France. Emerg Infect Dis 2010; 16: 1761-1763.
113. Kasorndorkbua C, Thacker BJ, Halbur PG, Guenette DK, Buitenwerf RM, Royer RL, Meng XJ: Experimental infection of pregnant gilts with swine hepatitis E virus. Can J Vet Res 2003; 67: 303-306.
114. Chibber RM, Usmani MA, Al-Sibai MH: Should HEV infected mothers breast feed? Arch Gynecol Obstet 2004; 270: 15-20.
115. Bendall R, Ellis V, Ijaz S, Ali R, Dalton H: A comparison of two commercially available anti-HEV IgG kits and a re-evaluation of anti-HEV IgG seroprevalence data in developed countries. J Med Virol 2010; 82: 799-805.
116. Drobeniuc J, Meng J, Reuter G, Greene-Montfort T, Khudyakova N, Dimitrova Z, Kamili S, Teo CG: Serologic assays specific to immunoglobulin M antibodies against hepatitis E virus: pangenotypic evaluation of performances. Clin Infect Dis 2010; 51:e24-e27.
117. Khuroo MS, Kamili S, Dar MY, Moecklii R, Jameel S: Hepatitis E and long-term antibody status. Lancet 1993; 341: 1355.
118. Myint KS, Endy TP, Shrestha MP, Shrestha SK, Vaughn DW, Innis BL, Gibbons RV, Kuschner RA, Seriwatana J, Scott RM: Hepatitis E antibody kinetics in Nepalese patients. Trans R Soc Trop Med Hyg 2006; 100: 938-941.
119. Li RC, Ge SX, Li YP, Zheng YJ, Nong Y, Guo QS, Zhang J, Ng MH, Xia NS: Seroprevalence of hepatitis E virus infection, rural southern People's Republic of China. Emerg Infect Dis 2006; 12: 1682-1688.
120. Bryan JP, Iqbal M, Tsarev S, Malik IA, Duncan JF, Ahmed A, Khan A, Khan A, Rafiqui AR, Purcell RH, Legters LJ: Epidemic of hepatitis E in a military unit in Abbotrabad, Pakistan. Am J Trop Med Hyg 2002; 67: 662-668.
121. Inoue J, Ueno Y, Nagasaki F, Akahane T, Fukushima K, Kogure T, Kondo Y, Kakazu E, Tamai K, Kido O, Nakagome Y, Ninomiya M, Obara N, Wakui Y, Takahashi M, Okamoto H, Shimosegawa T: Sporadic acute hepatitis E occurred constantly during the last decade in northeast Japan. J Gastroenterol 2009; 44: 329-337.
122. Zhang S, Wang J, Yuan Q, Ge S, Zhang J, Xia N, Tian D: Clinical characteristics and risk factors of sporadic Hepatitis E in central China. Virol J 2011; 8: 152.
123. Fix AD, Abdel-Hamid M, Purcell RH, Shehata MH, bdel-Aziz F, Mikhail N, el SH, Nafeh M, Habib M, Arthur RR, Emerson SU, Strickland GT: Prevalence of antibodies to hepatitis E in two rural Egyptian communities. Am J Trop Med Hyg 2000; 62: 519-523.
124. Swain SK, Baral P, Hutin YJ, Rao TV, Murhekar M, Gupte MD: A hepatitis E outbreak caused by a temporary interruption in a municipal water treatment system, Baripada, Orissa, India, 2004. Trans R Soc Trop Med Hyg 2010; 104: 66-69.
125. Clayson ET, Vaughn DW, Innis BL, Shrestha MP, Pandey R, Malla DB: Association of hepatitis E virus with an outbreak of hepatitis at a military training camp in Nepal. J Med Virol 1998; 54: 178-182.
126. Aggarwal R, Kumar R, Pal R, Naik S, Semwal SN, Naik SR: Role of travel as a risk factor for hepatitis E virus infection in a disease-endemic area. Indian J Gastroenterol 2002; 21: 14-18.
127. Zhang X, Ke W, Xie J, Zhao Z, Xie D, Gao Z: Comparison of effects of hepatitis E or A viral superinfection in patients with chronic hepatitis B. Hepatol Int 2010; 4: 615-620.
128. Bose PD, Das BC, Kumar A, Gondal R, Kumar D, Kar P: High viral load and deregulation of progesterone receptor signaling pathway: association with hepatitis E related poor pregnancy outcome. J Hepatol 2011; 54: 1107-1113.
129. Navaneethan U, Al MM, Shata MT: Hepatitis E and pregnancy: understanding the pathogenesis. Liver Int 2008; 28: 1190-1199.
130. Baylis SA, Koc O, Nick S, Blumel J: Widespread distribution of hepatitis E virus in plasma fractionation pools. Vox Sang 2012; 102: 182-183.
131. Ijaz S, Vyse AJ, Morgan D, Pebody RG, Tedder RS, Brown D: Indigenous hepatitis E virus infection in England: more common than it seems. J Clin Virol 2009; 44: 272-276.
132. Reuter G, Fodor D, Forgach P, Katai A, Szucs G: Characterization and zoonotic potential of endemic hepatitis E virus (HEV) strains in humans and animals in Hungary. J Clin Virol 2009; 44: 277-281.
133. Bouquet J, Tesse S, Lunazzi A, Eloit M, Rose N, Nicand E, Pavio N: Close similarity between sequences of hepatitis E virus recovered from humans and swine, France, 2008-2009. Emerg Infect Dis 2011; 17: 2018-2025.
134. Peron JM, Bureau C, Poirson H, Mansuy JM, Alric L, Selves J, Dupuis E, Izopet J, Vinel JP: Fulminant liver failure from acute autochthonous hepatitis E in France: description of seven patients with acute hepatitis E and encephalopathy. J Viral Hepat 2007; 14: 298-303.
135. Dalton HR, Bendall RP, Pritchard C, Henley W, Melzer D: National mortality rates from chronic liver disease and consumption of alcohol and pig meat. Epidemiol Infect 2010; 138: 174-182.
136. Anty R, Ollier L, Peron JM, Nicand E, Cannavo I, Bongain A, Giordanengo V, Tran A: First case report of an acute genotype 3 hepatitis E infected pregnant woman living in South-Eastern France. J Clin Virol 2012; 54: 76-78.
137. Andersson MI, Hughes J, Gordon FH, Ijaz S, Donati M: Of pigs and pregnancy. Lancet 2008; 372: 1192.
138. Aikawa T, Yamagata K, Miyamoto K, Tsuda F, Takahashi M, Okamoto H: A first case of pregnant woman who contracted infection of indigenous genotype 3 hepatitis E virus in Japan. Kanzo 2009; 50: 163-165.
139. Boutrouille A, Bakkali-Kassimi L, Cruciere C, Pavio N: Prevalence of anti-hepatitis E virus antibodies in French blood donors. J Clin Microbiol 2007; 45: 2009-2010.
140. Curry JA, Adams N, Crum-Cianflone NF: Acute hepatitis E virus infection in an HIVinfected person in the United States. Ann Intern Med 2009; 150: 226-227.
141. Pischke S, Wedemeyer H: Chronic hepatitis E in liver transplant recipients: a significant clinical problem? Minerva Gastroenterol Dietol 2010; 56: 121-128.
142. Abravanel F, Mansuy JM, Huynh A, Kamar N, Alric L, Peron JM, Recher C, Izopet J: Low risk of hepatitis E virus reactivation after haematopoietic stem cell transplantation. J Clin Virol 2012; 54: 152-155.
143. Legrand-Abravanel F, Thevenet I, Mansuy JM, Saune K, Vischi F, Peron JM, Kamar N, Rostaing L, Izopet J: Good performance of immunoglobulin M assays in diagnosing genotype 3 hepatitis E virus infections. Clin Vaccine Immunol 2009; 16: 772-774.
144. Zhao C, Ma Z, Harrison TJ, Feng R, Zhang C, Qiao Z, Fan J, Ma H, Li M, Song A, Wang Y: A novel genotype of hepatitis E virus prevalent among farmed rabbits in China. J Med Virol 2009; 81: 1371-1379.
145. Nakamura M, Takahashi K, Taira K, Taira M, Ohno A, Sakugawa H, Arai M, Mishiro S: Hepatitis E virus infection in wild mongooses of Okinawa, Japan: demonstration of anti-HEV antibodies and a full-genome nucleotide sequence. Hepatol Res 2006; 34: 137-140.
146. Rutjes SA, Lodder-Verschoor F, Lodder WJ, van der Giessen J, Reesink H, Bouwknegt M, de Roda Husman AM: Seroprevalence and molecular detection of hepatitis E virus in wild boar and red deer in the Netherlands. J Virol Methods 2010; 168: 197-206.
147. Nakai I, Kato K, Miyazaki A, Yoshii M, Li TC, Takeda N, Tsunemitsu H, Ikeda H: Different fecal shedding patterns of two common strains of hepatitis E virus at three Japanese swine farms. Am J Trop Med Hyg 2006; 75: 1171-1177.
148. Casas M, Pujols J, Rosell R, de Deus N, Peralta B, Pina S, Casal J, Martin M: Retrospective serological study on hepatitis E infection in pigs from 1985 to 1997 in Spain. Vet Microbiol 2009; 135: 248-252.
149. Arankalle VA, Chobe LP, Walimbe AM, Yergolkar PN, Jacob GP: Swine HEV infection in south India and phylogenetic analysis (1985-1999). J Med Virol 2003; 69: 391-396.
150. Chandler JD, Riddell MA, Li F, Love RJ, Anderson DA: Serological evidence for swine hepatitis E virus infection in Australian pig herds. Vet Microbiol 1999; 68: 95-105.
151. Li TC, Saito M, Ogura G, Ishibashi O, Miyamura T, Takeda N: Serologic evidence for hepatitis E virus infection in mongoose. Am J Trop Med Hyg 2006; 74: 932-936.
152. Johne R, Dremsek P, Kindler E, Schielke A, Plenge-Bonig A, Gregersen H, Wessels U, Schmidt K, Rietschel W, Groschup MH, Guenther S, Heckel G, Ulrich RG: Rat hepatitis E virus: Geographical clustering within Germany and serological detection in wild Norway rats ( Rattus norvegicus ). Infect Genet Evol 2012; 12: 947-956.
153. Kanai Y, Miyasaka S, Uyama S, Kawami S, Kato-Mori Y, Tsujikawa M, Yunoki M, Nishiyama S, Ikuta K, Hagiwara K: Hepatitis E virus in Norway rats ( Rattus norvegicus ) captured around a pig farm. BMC Res Notes 2012; 5: 4.
154. Li TC, Yoshimatsu K, Yasuda SP, Arikawa J, Koma T, Kataoka M, Ami Y, Suzaki Y, Mai le TQ, Hoa NT, Yamashiro T, Hasebe F, Takeda N, Wakita T: Characterization of self-assembled virus-like particles of rat hepatitis E virus generated by recombinant baculoviruses. J Gen Virol 2011; 92: 2830-2837.
155. Kabrane-Lazizi Y, Fine JB, Elm J, Glass GE, Higa H, Diwan A, Gibbs CJ Jr, Meng XJ, Emerson SU, Purcell RH: Evidence for widespread infection of wild rats with hepatitis E virus in the United States. Am J Trop Med Hyg 1999; 61: 331-335.
156. Cossaboom CM, Cordoba L, Dryman BA, Meng XJ: Hepatitis E virus in rabbits, Virginia, USA. Emerg Infect Dis 2011; 17: 2047-2049.
157. Geng Y, Zhao C, Song A, Wang J, Zhang X, Harrison TJ, Zhou Y, Wang W,
158. Yamamoto H, Li TC, Koshimoto C, Ito K, Kita M, Miyashita N, Arikawa J, Yagami K, Asano M, Tezuka H, Suzuki N, Kurosawa T, Shibahara T, Furuya M, Mohri S, Sato H, Ohsawa K, Ibuki K, Takeda N: Serological evidence for hepatitis E virus infection in laboratory monkeys and pigs in animal facilities in Japan. Exp Anim 2008; 57: 367-376.
159. Li SW, Zhang J, Li YM, Ou SH, Huang GY, He ZQ, Ge SX, Xian YL, Pang SQ, Ng MH, Xia NS: A bacterially expressed particulate hepatitis E vaccine: antigenicity, immunogenicity and protectivity on primates. Vaccine 2005; 23: 2893-2901.
160. Purcell RH, Nguyen H, Shapiro M, Engle RE, Govindarajan S, Blackwelder WC, Wong DC, Prieels JP, Emerson SU: Preclinical immunogenicity and efficacy trial of a recombinant hepatitis E vaccine. Vaccine 2003; 21: 2607-2615.
161. Zhu FC, Zhang J, Zhang XF, Zhou C, Wang ZZ, Huang SJ, Wang H, Yang CL, Jiang HM, Cai JP, Wang YJ, Ai X, Hu YM, Tang Q, Yao X, Yan Q, Xian YL, Wu T, Li YM, Miao J, Ng MH, Shih JW, Xia NS: 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.
162. Shrestha MP, Scott RM, Joshi DM, Mammen MP Jr, Thapa GB, Thapa N, Myint KS, Fourneau M, Kuschner RA, Shrestha SK, David MP, Seriwatana J, Vaughn DW, Safary A, Endy TP, Innis BL: Safety and efficacy of a recombinant hepatitis E vaccine. N Engl J Med 2007; 356: 895-903.
163. Proffitt A: First HEV vaccine approved. Nat Biotechnol 2012; 30: 300.
164. Gerolami R, Borentain P, Raissouni F, Motte A, Solas C, Colson P: Treatment of severe acute hepatitis E by ribavirin. J Clin Virol 2011; 52: 60-62.
165. Zhang L, Wilson DP: Trends in notifiable infectious diseases in China: implications for surveillance and population health policy. PLoS One 2012; 7:e31076.