Current knowledge on Hepatitis E virus infection

REFERENCES

Walsh SR. Hepatitis E virus. In: Bennett JE, Dolin R, Blaser MJ, editors. Mandell, Douglas, and Bennett's Principles and Prac-tice of Infectious Diseases. 8th ed. Philadelphia, USA: Elsevier Saunders; 2015. p. 2131–41.

Khuroo MS. Study of an epidemic of non-A, non-B hepatitis. Pos¬sibility of another human hepatitis virus distinct from post-transfusion non-A, non-B type. Am J Med 1980; 68(6): 818–24.

Wong DC, Purcell RH, Sreenivasan MA, Prasad SR, Pavri KM. Epi¬demic and endemic hepatitis in India: Evidence for a non-A, non-B hepatitis virus aetiology. Lancet 1980; 316(8200): 876–9.

Meng XJ, Purcell RH, Halbur PG, Lehman JR, Webb DM, Tsareva TS, et al. A novel virus in swine is closely related to the human hepatitis E virus. Proc Natl Acad Sci U.S.A. 1997; 94(18): 9860–5.

Kwo PY, Schlauder GG, Carpenter HA, Murphy PJ, Rosenblatt JE, Dawson GJ, et al. Acute hepatitis E by a new isolate acquired in the United States. Mayo Clin Proc 1997; 72(12): 1133–6.

Schlauder GG, Dawson GJ, Erker JC, Kwo PY, Knigge MF, Smalley DL, et al. The sequence and phylogenetic analysis of a novel hepatitis E virus isolated from a patient with acute hepatitis reported in the United States. J Gen Virol 1998; 79( Pt 3): 447–56.

Hoofnagle JH, Nelson KE, Purcell RH. Hepatitis E. N Engl J Med 2012; 367(13): 1237–44.

Smith DB, Simmonds P, Jameel S, Emerson SU, Harrison TJ, Meng XJ, et al. Consensus proposals for classification of the family Hepeviridae. J Gen Virol 2014; 95(Pt 10): 2223–32.

Clemente-Casares P, Ramos-Romero C, Ramirez-Gonzalez E, Mas A. Hepatitis E virus in industrialized countries: The silent threat. BioMed Res Int 2016; 2016: 9838041.

Hartl J, Wehmeyer MH, Pischke S. Acute hepatitis E: Two sides of the same coin. Viruses 2016; 8(11). pii: E299.

Doceul V, Bagdassarian E, Demange A, Pavio N. Zoonotic hepati¬tis E virus: Classification, animal reservoirs and transmission routes. Viruses 2016; 8(10). pii: E270

Khuroo MS, Khuroo MS, Khuroo NS. Hepatitis E: Discovery, global impact, control and cure. World J Gastroenterol 2016; 22(31): 7030–45.

Nan Y, Zhang YJ. Molecular biology and infection of hepatitis E virus. Front Microbiol 2016; 7: 1419.

Aggarwal R, Jameel S. Hepatitis E. Hepatology 2011; 54(6): 2218–26.

Hazam RK, Singla R, Kishore J, Singh S, Gupta RK, Kar P. Surveil¬lance of hepatitis E virus in sewage and drinking water in a re¬settlement colony of Delhi: What has been the experience? Arch Virol 2010; 155(8): 1227–33.

Howard CM, Handzel T, Hill VR, Grytdal SP, Blanton C, Kamili S, et al. Novel risk factors associated with hepatitis E virus infec¬tion in a large outbreak in Northern Uganda: Results from a case-control study and environmental analysis. Am J Trop Med Hyg 2010; 83(5): 1170–3.

Pavio N, Meng XJ, Renou C. Zoonotic hepatitis E: Animal reser¬voirs and emerging risks. Vet Res 2010; 41(6): 46.

Feagins AR, Opriessnig T, Guenette DK, Halbur PG, Meng XJ. De¬tection 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): 912–7.

Colson P, Borentain P, Queyriaux B, Kaba M, Moal V, Gallian P, et al. Pig liver sausage as a source of hepatitis E virus transmis¬sion to humans. J Infect Dis 2010; 202(6): 825–34.

Berto A, Grierson S, Hakze-Honing R, Martelli F, Johne R, Reetz J, et al. Hepatitis E virus in pork liver sausage, France. Emerging Infect Dis 2013; 19(2): 264–6.

Kmush BL, Nelson KE, Labrique AB. Risk factors for hepatitis E virus infection and disease. Expert Rev Anti Infect Ther 2015; 13(1): 41–53.

Lhomme S, Marion O, Abravanel F, Chapuy-Regaud S, Kamar N, Izopet J. Hepatitis E pathogenesis. Viruses 2016; 8(8). pii: E212.

Pérez-Gracia MT, García M, Suay B, Mateos-Lindemann ML. Cur¬rent Knowledge on Hepatitis E. J Clin Transl Hepatol 2015; 3(2): 117–26.

Wedemeyer H, Pischke S, Manns MP. Pathogenesis and treatment of hepatitis E virus infection. Gastroenterology 2012; 142(6): 1388–1397.e1

Paula VS, Wiele M, Mbunkah AH, Daniel AM, Kingsley MT, Schmidt-Chanasit J. Hepatitis E virus genotype 3 strains in do-mestic pigs, Cameroon. Emerg Infect Dis 2013; 19(4): 666–8.

Hsieh SY, Yang PY, Ho YP, Chu CM, Liaw YF. Identification of a novel strain of hepatitis E virus responsible for sporadic acute hepatitis in Taiwan. J Med Virol 1998; 55(4): 300–4.

Hsieh SY, Meng XJ, Wu YH, Liu ST, Tam AW, Lin DY, et al. Identity of a novel swine hepatitis E virus in Taiwan forming a monophyletic group with Taiwan isolates of human hepatitis E virus. J Clin Microbiol 1999; 37(12): 3828–34.

Liu P, Li L, Wang L, Bu Q, Fu H, Han J, et al. Phylogenetic analysis of 626 hepatitis E virus (HEV) isolates from humans and animals in China (1986-2011) showing genotype diversity and zoonotic transmission. Infect Genet Evol 2012; 12(2): 428–34.

Geng Y, Zhao C, Fan J, Harrison TJ, Zhang H, Lian H, et al. Ge-notype analysis of hepatitis E virus from sporadic hepatitis E cases in Northern China. Infect Genet Evol 2013; 20: 413–7.

Sato Y, Sato H, Naka K, Furuya S, Tsukiji H, Kitagawa K, et al. A nationwide survey of hepatitis E virus (HEV) infection in wild boars in Japan: Identification of boar HEV strains of geno¬types 3 and 4 and unrecognized genotypes. Arch Virol 2011; 156(8): 1345–58.

Dremsek P, Joel S, Baechlein C, Pavio N, Schielke A, Ziller M, et al. Hepatitis E virus seroprevalence of domestic pigs in Germany determined by a novel in-house and two reference ELISAs. J Virol Methods 2013; 190(1–2): 11–6.

Krumbholz A, Joel S, Neubert A, Dremsek P, Dürrwald R, Johne R, et al. Age-related and regional differences in the prevalence of hepatitis E virus-specific antibodies in pigs in Germany. Vet Microbiol 2013; 167(3–4): 394–402.

Li T, Chijiwa K, Sera N, Ishibashi T, Etoh Y, Shinohara Y, et al. Hepatitis E virus transmission from wild boar meat. Emerging Infect. Dis 2005; 11(12): 1958–60.

Miyashita K, Kang J, Saga A, Takahashi K, Shimamura T, Yasumoto A, et al. 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(9): 870–8.

Matsuda H, Okada K, Takahashi K, Mishiro S. Severe hepatitis E virus infection after ingestion of uncooked liver from a wild boar. J Infect Dis 2003; 188(6): 944.

Nakano T, Takahashi K, Arai M, Okano H, Kato H, Ayada M, et al. Identification of European-type hepatitis E virus subtype 3e isolates in Japanese wild boars: Molecular tracing of HEV from swine to wild boars. Infect Genet Evol 2013; 18: 287–98.

Meng XJ, Wiseman B, Elvinger F, Guenette DK, Toth TE, Engle RE, et al. Prevalence of antibodies to hepatitis E virus in vet-erinarians working with swine and in normal blood donors in the United States and other countries. J Clin Microbiol 2002; 40(1): 117–22.

Lewis HC, Wichmann O, Duizer E. Transmission routes and risk factors for autochthonous hepatitis E virus infection in Eu-rope: A systematic review. Epidemiol Infect 2010; 138(2): 145–66.

Crossan C, Scobie L, Godwin J, Hunter JG, Hawkes T, Dalton HR, et al. Hepatitis E virus and porcine-derived heparin. Emerging Infect Dis 2013; 19(4): 686–8.

Kasorndorkbua C, Opriessnig T, Huang FF, Guenette DK, Thomas PJ, Meng XJ, et al. 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 Mi-crobiol 2005; 71(12): 7831–7.

Takahashi M, Okamoto H. Features of hepatitis E virus infec-tion in humans and animals in Japan. Hepatol Res 2014; 44(1): 43–58.

Wichmann O, Schimanski S, Koch J, Kohler M, Rothe C, Plentz A, et al. Phylogenetic and case-control study on hepatitis E virus in¬fection in Germany. J Infect Dis 2008; 198(12): 1732–41.

Schielke A, Sachs K, Lierz M, Appel B, Jansen A, Johne R. Detec-tion of hepatitis E virus in wild boars of rural and urban re-gions in Germany and whole genome characterization of an endemic strain. Virol J 2009; 6(1): 58.

Macedo G, Pinto T, Sarmento JA, Vale AM, Ribeiro T. The first as¬sessment of hepatitis E virus seroprevalence in northern Portugal. Acta Med Port 1998; 11(12): 1065–8. (Portugal)

Tarragó D, López-Vélez R, Turrientes C, Baquero F, Mateos ML. Prevalence of Hepatitis E Antibodies in Immigrants from De-veloping Countries. Eur J Clin Microbiol Infect Dis 2000; 19(4): 309–11.

Olsen B, Axelsson-Olsson D, Thelin A, Weiland O. Unexpected high prevalence of IgG-antibodies to hepatitis E virus in Swe-dish pig farmers and controls. Scand J Infect Dis 2006; 38(1): 55–8.

Boutrouille A, Bakkali-Kassimi L, Crucière C, Pavio N. Prevalence of anti-hepatitis E virus antibodies in French blood donors. J Clin Microbiol 2007; 45(6): 2009–10.

Dalton HR, Stableforth W, Thurairajah P, Hazeldine S, Remnarace R, Usama W, et al. 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 Gastro¬enterol Hepatol 2008; 20(8): 784–90.

Mansuy JM, Legrand-Abravanel F, Calot JP, Peron JM, Alric L, Agudo S, et al. High prevalence of anti-hepatitis E virus anti-bodies in blood donors from South West France. J Med Virol 2008; 80(2): 289–93.

Christensen PB, Engle RE, Hjort C, Homburg KM, Vach W, Georgsen J, et al. Time trend of the prevalence of hepatitis E antibodies among farmers and blood donors: A potential zoonosis in Denmark. Clin Infect Dis 2008; 47(8): 1026–31.

Mansuy J, Bendall R, Legrand-Abravanel F, Sauné K, Miédouge M, Ellis V, et al. Hepatitis E virus antibodies in blood donors, France. Emerging Infect. Dis 2011; 17(12): 2309–12.

Kaufmann A, Kenfak-Foguena A, André C, Canellini G, Bürgisser P, Moradpour D, et al. Hepatitis E virus seroprevalence among blood donors in southwest Switzerland. PLoS ONE 2011; 6(6): e21150.

Dremsek P, Wenzel JJ, Johne R, Ziller M, Hofmann J, Groschup MH, 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(2): 189–200.

Fogeda M, Avellón A, Echevarría JM. Prevalence of specific anti-body to hepatitis E virus in the general population of the community of Madrid, Spain. J Med Virol 2012; 84(1): 71–4.

Cleland A, Smith L, Crossan C, Blatchford O, Dalton HR, Scobie L, et al. Hepatitis E virus in Scottish blood donors. Vox Sang 2013; 105(4): 283–9.

Slot E, Hogema BM, Riezebos-Brilman A, Kok TM, Molier M, Zaai¬jer HL. Silent hepatitis E virus infection in Dutch blood do¬nors, 2011 to 2012. Euro Surveill 2013; 18(31): pii: 20550.

Juhl D, Baylis SA, Blümel J, Görg S, Hennig H. Seroprevalence and incidence of hepatitis E virus infection in German blood donors. Transfusion 2014; 54(1): 49–56.

Petrović T, Lupulović D, Jiménez ON, Vojvodić S, Blázquez A, Es-cri¬bano-Romero E, et al. Prevalence of hepatitis E virus (HEV) an¬tibodies in Serbian blood donors. J Infect Dev Ctries 2014; 8(10): 1322–7.

Fischer C, Hofmann M, Danzer M, Hofer K, Kaar J, Gabriel C. Sero¬prevalence and Incidence of hepatitis E in blood donors in Upper Austria. PLoS ONE 2015; 10(3): e0119576.

Holm DK, Moessner BK, Engle RE, Zaaijer HL, Georgsen J, Purcell RH, et al. Declining prevalence of hepatitis E antibodies among Danish blood donors. Transfusion 2015; 55(7): 1662–7.

Mansuy JM, Saune K, Rech H, Abravanel F, Mengelle C, Homme LS, et al. Seroprevalence in blood donors reveals widespread, multi-source exposure to hepatitis E virus, southern France, October 2011. Euro Surveill 2015; 20(19): 27–34.

Puttini C, Riccio ML, Redi D, Tordini G, Cenerini M, Romanello F, et al. Seroprevalence of hepatitis E virus (HEV) infection in blood donors and renal transplant recipients: A retrospective study from central Italy. Infez Med 2015; 23(3): 253–6.

Aydın NN, Ergünay K, Karagül A, Pınar A, Us D. Investigation of the hepatitis E virus seroprevalence in cases admitted to Hacettepe University Medical Faculty Hospital. Mikrobiyol Bul 2015; 49(4): 554–64. (Turkish)

Ricco G, Bonino F, Lanza M, Scatena F, Alfieri CM, Messa P, et al. New immunoassays for total, IgA and IgM antibodies against hepatitis E virus: Prevalence in Italian blood donors and pa¬tients with chronic liver or kidney diseases. Dig Liver Dis 2016; 48(5): 536–41.

Mansuy JM, Gallian P, Dimeglio C, Saune K, Arnaud C, Pelletier B, et al. A nationwide survey of hepatitis E viral infection in French blood donors. Hepatology 2016; 63(4): 1145–54.

Lucarelli C, Spada E, Taliani G, Chionne P, Madonna E, Marcanto¬nio C, et al. High prevalence of anti-hepatitis E virus antibodies among blood donors in central Italy, February to March 2014. Euro Surveill 2016; 21(30). doi: 10.2807/1560-7917.ES.2016.21.30.30299.

Lange H, Øverbø J, Borgen K, Dudman S, Hoddevik G, Urdahl AM, et al. Hepatitis E in Norway: Seroprevalence in humans and swine. Epidemiol Infect 2017; 145(1): 181–6.

Meng XJ. Hepatitis E virus: Animal reservoirs and zoonotic risk. Vet Microbiol 2010; 140(3–4): 256–65.

Savuta G, Anita A, Anita D, Ludu L, Pavio N. Preliminary epi-de¬miological investigations regarding hepatitis E virus in-fection in swine from the North-East of Romania. Bulletin USAMV-CN 2007;64(1-2):356-358.

Savuta GH, Anita A, Anita D, Ludu L, Duca E, Pavio N. Seroe-pi¬demiological researches regarding swine and human hepatitis E in Romania. Lucrari Stiintifice Med Vet (Timisoara) 2008; 41: 309–13.

Asimoula S, Tzika E, Alexopoulos C, Kyriakis SC, Froesner G. First report of serological evidence of hepatitis E virus infection in swine in Northern Greece. Acta Vet Beograd 2009; 59(2–3): 205–11.

Lupulovic D, Lazic S, Prodanov-Radulovic J, de Oya JN, Escribano-Ro¬mero E, Saiz JC, et al. First serological study of hepatitis E virus infection in backyard pigs from Serbia. Food Environ Vi¬rol 2010; 2(2): 110–13.

Martinelli N, Luppi A, Cordioli P, Lombardi G, Lavazza A. Preva¬lence of hepatitis E virus antibodies in pigs in Northern Italy. Infect Ecol Epidemiol 2011; 1. doi: 10.3402/iee.v1i0.7331.

de Oya JN, de Blas I, Blazquez AB, Martin-Acebes MA, Halaihel N, Girones O, et al. Widespread distribution of hepatitis E virus in Spanish pig herds. BMC Res Notes 2011; 4: 412.

O’Connor M, Roche S, Sammin D. Seroprevalence of Hepatitis E virus infection in the Irish pig population. Ir Vet J 2015; 68(1): 8.

Weiner M, Tokarska-Rodak M, Plewik D, Panczuk A, Szepeluk A, Krajewska M. Preliminary study on the detection of hepatitis E virus (HEV) antibodies in pigs and wild boars in Poland. J Vet Res 2016; 60(4): 385–9.

Caruso C, Peletto S, Rosamilia A, Modesto P, Chiavacci L, Sona B, et al. Hepatitis E virus: A cross-sectional serological and virologi¬cal study in pigs and humans at zoonotic risk within a high-density pig farming area. Transbound Emerg Dis 2017; 64(5): 1443–53.

Pishmisheva M, Baymakova M, Golkocheva-Markova E, Kundurzhiev T, Pepovich R, Popov GT, et al. First serological study of hepatitis E virus infection in pigs in Bulgaria. C R Acad Bulg Sci 2018; 71(7): 1001–8.

Khuroo MS, Teli MR, Skidmore S, Sofi MA, Khuroo MI. Inci-dence and severity of viral hepatitis in pregnancy. Am J Med 1981; 70(2): 252–5.

Viswanathan R, Sidhu AS, Pradhan SK, Magar NG. Infectious hepatitis; clinical findings. Indian J Med Res 1957; 45(Suppl): 49–58.

Borgen K, Herremans T, Duizer E, Vennema H, Rutjes S, Bosman A, et al. Non-travel related Hepatitis E virus genotype 3 infec¬tions in the Netherlands: A case series 2004-2006. BMC Infect Dis 2008; 8: 61.

Mansuy JM, Peron JM, Abravanel F, Poirson H, Dubois M, Miedouge M, et al. Hepatitis E in the south west of France in individuals who have never visited an endemic area. J Med Virol 2004; 74(3): 419–24.

Baymakova M, Sakem B, Plochev K, Popov GT, Mihaylova-Garnizova R, Kovaleva V, et al. Epidemiological characteristics and clinical manifestations of hepatitis E virus infection in Bulgaria: A re¬port on 20 patients. Srp Arh Celok Lek 2016; 144(1–2): 63–8.

Kamar N, Selves J, Mansuy J, Ouezzani L, Péron J, Guitard J, et al. Hepatitis E virus and chronic hepatitis in organ-transplant re¬cipients. N Engl J Med 2008; 358(8): 811–7.

Tamura A, Shimizu YK, Tanaka T, Kuroda K, Arakawa Y, Taka-ha¬shi K, et al. Persistent infection of hepatitis E virus transmitted by blood transfusion in a patient with T-cell lym-phoma. Hepatol Res 2007; 37(2): 113–20.

Dalton HR, Bendall RP, Keane FE, Tedder RS, Ijaz S. Persistent car¬riage of hepatitis E virus in patients with HIV infection. N Engl J Med 2009; 361(10): 1025–7.

Gérolami R, Moal V, Colson P. Chronic hepatitis E with cirrhosis in a kidney-transplant recipient. N Engl J Med 2008; 358(8): 859–60.

Casas M, Cortés R, Pina S, Peralta B, Allepuz A, Cortey M, et al. Longitudinal study of hepatitis E virus infection in Spanish farrow-to-finish swine herds. Vet Microbiol 2011; 148(1): 27–34.

Wacheck S, Werres C, Mohn U, Dorn S, Soutschek E, Fredriksson-Ahomaa M, et al. Detection of IgM and IgG against hepatitis E virus in serum and meat juice samples from pigs at slaughter in Bavaria, Germany. Foodborne Pathog Dis 2012; 9(7): 655–60.

Legrand-Abravanel F, Thevenet I, Mansuy J, Saune K, Vischi F, Peron J, et al. Good performance of immunoglobulin M assays in di¬agnosing genotype 3 hepatitis E virus infections. Clin Vaccine Immunol 2009; 16(5): 772–4.

Drobeniuc J, Meng J, Reuter G, Greene-Montfort T, Khudyakova N, Dimitrova Z, et al. Serologic assays specific to immunoglobulin M antibodies against hepatitis E virus: Pangenotypic evaluation of performances. Clin Infect Dis 2010; 51(3): e24–7.

Leblanc D, Ward P, Gagné M, Poitras E, Müller P, Trottier Y, et al. Presence of hepatitis E virus in a naturally infected swine herd from nursery to slaughter. Int J Food Microbiol 2007; 117(2): 160–6.

Deus N, Casas M, Peralta B, Nofrarías M, Pina S, Martín M, et al. Hepatitis E virus infection dynamics and organic distribution in naturally infected pigs in a farrow-to-finish farm. Vet Mi¬crobiol 2008; 132(1–2): 19–28.

Gupta E, Pandey P, Pandey S, Sharma MK, Sarin SK. Role of he-pa¬titis E virus antigen in confirming active viral replication in patients with acute viral hepatitis E infection. J Clin Virol 2013; 58(2): 374–7.

Majumdar M, Singh MP, Pujhari SK, Bhatia D, Chawla Y, Ratho RK. Hepatitis E virus antigen detection as an early diagnostic marker: Report from India. J Med Virol 2013; 85(5): 823–7.

Vollmer T, Knabbe C, Dreier J. Comparison of real-time PCR and antigen assays for detection of hepatitis E virus in blood donors. J Clin Microbiol 2014; 52(6): 2150–6.

Ha S, Chae C. Immunohistochemistry for the detection of swine hepatitis E virus in the liver. J Viral Hepat 2004; 11(3): 263–7.

Gupta P, Jagya N, Pabhu SB, Durgapal H, Acharya SK, Panda SK. Immunohistochemistry for the diagnosis of hepatitis E virus infection. J Viral Hepat 2012; 19(2): e177–83.

Somani SK, Aggarwal R, Naik SR, Srivastava S, Naik S. A sero-logi¬cal study of intrafamilial spread from patients with sporad-ic hepatitis E virus infection. J Viral Hepat 2003; 10(6): 446–9.

Kamar N, Rostaing L, Abravanel F, Garrouste C, Esposito L, Cardeau-Desangles I, et al. Pegylated interferon-alpha for treating chronic hepatitis E virus infection after liver transplantation. Clin Infect Dis 2010; 50(5): e30–3.

Kamar N, Rostaing L, Abravanel F, Garrouste C, Lhomme S, Esposito L, et al. Ribavirin therapy inhibits viral replication on patients with chronic hepatitis e virus infection. Gastroen-terology 2010; 139(5): 1612–8.

Zhu F, Zhang J, Zhang X, Zhou C, Wang Z, Huang S, et al. Effi-cacy and safety of a recombinant hepatitis E vaccine in healthy adults: a large-scale, randomised, double-blind pla-cebo-controlled, phase 3 trial. Lancet 2010; 376(9744): 895–902.