Hepatitis E virus: Animal reservoirs and zoonotic risk

Veterinary Microbiology

Volumn 140, Issue 3-4, 2010, Pages 256-265

  Meng, X J ^a  

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

Author keywords

Avian HEV; Chickens; Cross species infection; Food safety; Hepatitis E virus (HEV); Pigs; Swine HEV; Zoonosis

Indexed keywords

ANIMAL DISEASE; DEVELOPING COUNTRY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIDEMIC; FOOD SAFETY; GENOME ANALYSIS; GENOTYPE; HAND WASHING; HEPATITIS E; HEPATITIS E VIRUS; HUMAN; NONHUMAN; OPEN READING FRAME; POLYMERASE CHAIN REACTION; PUBLIC HEALTH; REVIEW; RISK REDUCTION; SANITATION; SPLENOMEGALY; STRAIN DIFFERENCE; SYMPTOM; VIRUS CELL INTERACTION; VIRUS CHARACTERIZATION; VIRUS GENOME; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS STRAIN; VIRUS TRANSMISSION; VIRUS VIRULENCE; ZOONOSIS;

ANIMALS; CHICKENS; DISEASE RESERVOIRS; HEPATITIS E; HEPATITIS E VIRUS; HUMANS; RISK FACTORS; SWINE; ZOONOSES;

ANIMALIA; AVES; GALLUS GALLUS; HEPATITIS E VIRUS; HEPEVIRIDAE; MAMMALIA; MIRIDAE; RNA VIRUSES; SUIDAE;

EID: 74249112087     PISSN: 03781135     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetmic.2009.03.017     Document Type: Review

References (67)

1. Arankalle V.A., Tsarev S.A., Chadha M.S., Alling D.W., Emerson S.U., Banerjee K., and Purcell R.H. Age-specific prevalence of antibodies to hepatitis A and E viruses in Pune, India, 1982 and 1992. J. Infect. Dis. 171 (1995) 447-450
2. Balayan M.S., Andjaparidze A.G., Savinskaya S.S., Ketiladze E.S., Braginsky D.M., Savinov A.P., and Poleschuk V.F. Evidence for a virus in non-A, non-B hepatitis transmitted via the fecal-oral route. Intervirology 20 (1983) 23-31
3. Balayan M.S., Usmanov R.K., Zamyatina D.I., and Karas F.R. Brief report: experimental hepatitis E infection in domestic pigs. J. Med. Virol. 32 (1990) 58-59
4. Billam P., Huang F.F., Sun Z.F., Pierson F.W., Duncan R.B., Elvinger F., Guenette D.K., Toth T.E., and Meng X.J. Systematic pathogenesis and replication of avian hepatitis E virus in specific-pathogen-free adult chickens. J. Virol. 79 (2005) 3429-3437
5. Bouwknegt M., Frankena K., Rutjes S.A., Wellenberg G.J., de Roda Husman A.M., van der Poel W.H., and de Jong M.C. Estimation of hepatitis E virus transmission among pigs due to contact-exposure. Vet. Res. 39 (2008) 40
6. Clayson E.T., Myint K.S., Snitbhan R., Vaughn D.W., Innis B.L., Chan L., Cheung P., and Shrestha M.P. Viremia, fecal shedding, and IgM and IgG responses in patients with hepatitis E. J. Infect. Dis 172 (1995) 927-933
7. Clemente-Casares P., Pina S., Buti M., Jardi R., MartIn M., Bofill-Mas S., and Girones R. Hepatitis E virus epidemiology in industrialized countries. Emerg. Infect. Dis. 9 (2003) 448-454
8. de Deus N., Peralta B., Pina S., Allepuz A., Mateu E., Vidal D., Ruiz-Fons F., Martín M., Gortázar C., and Segalés J. Epidemiological study of hepatitis E virus infection in European wild boars (Sus scrofa) in Spain. Vet. Microbiol. 129 (2008) 163-170
9. Drobeniuc J., Favorov M.O., Shapiro C.N., Bell B.P., Mast E.E., Dadu A., Culver D., Iarovoi P., Robertson B.H., and Margolis H.S. Hepatitis E virus antibody prevalence among persons who work with swine. J. Infect. Dis. 184 (2001) 1594-1597
10. Emerson S.U., Anderson D., Arankalle V.A., Meng X.J., Purdy M., Schlauder G.G., and Tsarev S.A. Hepevirus. In: Fauquet C.M., Mayo M.A., Maniloff J., Desselberger U., and Ball L.A. (Eds). Virus Taxonomy, VIIIth Report of the ICTV (2004), Elsevier/Academic Press, London 851-855
11. Emerson S.U., Arankalle V.A., and Purcell R.H. Thermal stability of hepatitis E virus. J. Infect. Dis. 192 (2005) 930-933
12. Emerson S.U., Nguyen H., Torian U., and Purcell R.H. ORF3 protein of hepatitis E virus is not required for replication, virion assembly, or infection of hepatoma cells in vitro. J. Virol. 80 (2006) 10457-10464
13. Feagins A.R., Opriessnig T., Guenette D.K., Halbur P.G., and 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. 88 (2007) 912-917
14. Feagins A.R., Opriessnig T., Guenette D.K., Halbur P.G., and Meng X.J. 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
15. Feagins A.R., Opriessnig T., Huang Y.W., Halbur P.G., and Meng X.J. 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
16. Graff J., Torian U., Nguyen H., and Emerson S.U. A bicistronic subgenomic mRNA encodes both the ORF2 and ORF3 proteins of hepatitis E virus. J. Virol. 80 (2006) 5919-5926
17. Guo H., Zhou E.M., Sun Z.F., Meng X.J., and Halbur P.G. Identification of B-cell epitopes in the capsid protein of avian hepatitis E virus (avian HEV) that are common to human and swine HEVs or unique to avian HEV. J. Gen. Virol. 87 (2006) 217-223
18. Halbur P.G., Kasorndorkbua C., Gilbert C., Guenette D.K., Potters M.B., Purcell R.H., Emerson S.U., Toth T.E., and Meng X.J. Comparative pathogenesis of infection of pigs with hepatitis E viruses recovered from a pig and a human. J. Clin. Microbiol. 39 (2001) 918-923
19. Haqshenas G., Shivaprasad H.L., Woolcock P.R., Read D.H., and Meng X.J. 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
20. Herremans M., Bakker J., Duizer E., Vennema H., and Koopmans M.P. Use of serological assays for diagnosis of hepatitis E virus genotype 1 and 3 infections in a setting of low endemicity. Clin. Vaccine Immunol. 14 (2007) 562-568
21. Huang F.F., Sun Z.F., Emerson S.U., Purcell R.H., Shivaprasad H.L., Pierson F.W., Toth T.E., and Meng X.J. 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
22. Huang F.F., Haqshenas G., Shivaprasad H.L., Guenette D.K., Woolcock P.R., Larsen C.T., Pierson F.W., Elvinger F., Toth T.E., and Meng X.J. Heterogeneity and seroprevalence of a newly identified avian hepatitis E virus from chickens in the United States. J. Clin. Microbiol. 40 (2002) 4197-4202
23. Huang Y.W., Opriessnig T., Halbur P.G., and Meng X.J. Initiation at the third in-frame AUG codon of open reading frame 3 of the hepatitis E virus is essential for viral infectivity in vivo. J. Virol. 81 (2007) 3018-3026
24. Jothikumar N., Cromeans T.L., Robertson B.H., Meng X.J., and Hill V.R. A broadly reactive one-step real-time RT-PCR assay for rapid and sensitive detection of hepatitis E virus. J Virol. Methods 131 (2006) 65-71
25. Kabrane-Lazizi Y., Meng X.J., Purcell R.H., and Emerson S.U. Evidence that the genomic RNA of hepatitis E virus is capped. J. Virol. 73 (1999) 8848-8850
26. Kabrane-Lazizi Y., Fine J.B., Elm J., Glass G.E., Higa H., Diwan A., Gibbs Jr. C.J., Meng X.J., Emerson S.U., and Purcell R.H. Evidence for widespread infection of wild rats with hepatitis E virus in the United States. Am. J. Trop. Med. Hyg. 61 (1999) 331-335
27. Karetnyi Y.V., Gilchrist M.J., and Naides S.J. Hepatitis E virus infection prevalence among selected populations in Iowa. J. Clin. Virol. 14 (1999) 51-55
28. Kasorndorkbua C., Guenette D.K., Huang F.F., Thomas P.J., Meng X.J., and Halbur P.G. Routes of transmission of swine hepatitis E virus in pigs. J. Clin. Microbiol. 42 (2004) 5047-5052
29. Kuno A., Ido K., Isoda N., Satoh Y., Ono K., Satoh S., Inamori H., Sugano K., Kanai N., Nishizawa T., and Okamoto H. Sporadic acute hepatitis E of a 47-year-old man whose pet cat was positive for antibody to hepatitis E virus. Hepatol. Res. 26 (2003) 237-242
30. Li T.C., Takeda N., Miyamura T., Matsuura Y., Wang J.C., Engvall H., Hammar L., Xing L., and Cheng R.H. Essential elements of the capsid protein for self-assembly into empty virus-like particles of hepatitis E virus. J. Virol. 79 (2005) 12999-13006
31. Li T.C., Chijiwa K., Sera N., Ishibashi T., Etoh Y., Shinohara Y., Kurata Y., Ishida M., Sakamoto S., Takeda N., and Miyamura T. Hepatitis E virus transmission from wild boar meat. Emerg. Infect. Dis. 11 (2005) 1958-1960
32. Lu L., Drobeniuc J., Kobylnikov N., Usmanov R.K., Robertson B.H., Favorov M.O., and Margolis H.S. Complete sequence of a Kyrgyzstan swine hepatitis E virus (HEV) isolated from a piglet thought to be experimentally infected with human HEV. J. Med. Virol. 74 (2004) 556-562
33. Maneerat Y., Clayson E.T., Myint K.S., Young G.D., and Innis B.L. Experimental infection of the laboratory rat with the hepatitis E virus. J. Med. Virol. 48 (1996) 121-128
34. Masuda J., Yano K., Tamada Y., Takii Y., Ito M., Omagari K., and Kohno S. Acute hepatitis E of a man who consumed wild boar meat prior to the onset of illness in Nagasaki. Jpn. Hepatol. Res. 31 (2005) 178-183
35. Matsuda H., Okada K., Takahashi K., and Mishiro S. Severe hepatitis E virus infection after ingestion of uncooked liver from a wild boar. J. Infect. Dis. 188 (2003) 944
36. Meng X.J., Purcell R.H., Halbur P.G., Lehman J.R., Webb D.M., Tsareva T.S., Haynes J.S., Thacker B.J., and Emerson S.U. 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
37. Meng X.J., Halbur P.G., Shapiro M.S., Govindarajan S., Bruna J.D., Mushahwar I.K., Purcell R.H., and Emerson S.U. Genetic and experimental evidence for cross-species infection by swine hepatitis E virus. J. Virol. 72 (1998) 9714-9721
38. Meng X.J., Wiseman B., Elvinger F., Guenette D.K., Toth T.E., Engle R.E., Emerson S.U., and Purcell R.H. 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
39. Meng X.J. Swine hepatitis E virus: cross-species infection and risk in xenotransplantation. Curr. Top. Microbiol. Immunol. 278 (2003) 185-216
40. Meng X.J. Hepatitis E as a zoonosis. In: Thomas H., Zuckermann A., and Lemon S. (Eds). Viral Hepatitis. 3rd ed. (2006), Blackwell Publishing Ltd., Oxford, UK 611-623
41. Meng X.J., and Halbur P.G. Swine hepatitis E virus. In: Straw B.E., et al. (Ed). Diseases of Swine. 9th ed. (2006), Blackwell Publishing Press 537-545
42. Meng X.J. Hepatitis E virus (hepevirus). In: Mahy B.W.J., and van Regenmortel M.H.V. (Eds). Encyclopedia of Virology (5 vols). 3rd ed. (2008), Elsevier, Oxford 377-383
43. Meng X.J., Shivaprasad H.L., and Payne C. Hepatitis E virus infections. In: Saif M., et al. (Ed). Diseases of Poultry. 12th ed. (2008), Blackwell Publishing Press 443-452
44. Michitaka K., Takahashi K., Furukawa S., Inoue G., Hiasa Y., Horiike N., Onji M., Abe N., and Mishiro S. Prevalence of hepatitis E virus among wild boar in the Ehime area of western Japan. Hepatol. Res. 37 (2007) 214-220
45. Nakamura M., Takahashi K., Taira K., Taira M., Ohno A., Sakugawa H., Arai M., and 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. 34 (2006) 137-140
46. Nicand E., Armstrong G.L., Enouf V., Guthmann J.P., Guerin J.P., Caron M., Nizou J.Y., and Andraghetti R. Genetic heterogeneity of hepatitis E virus in Darfur, Sudan, and neighboring Chad. J. Med. Virol. 77 (2005) 519-521
47. Okamoto H. Genetic variability and evolution of hepatitis E virus. Virus Res. 127 (2007) 216-228
48. Payne C.J., Ellis T.M., Plant S.L., Gregory A.R., and Wilcox G.E. Sequence data suggests big liver and spleen disease virus (BLSV) is genetically related to hepatitis E virus. Vet. Microbiol. 68 (1999) 119-125
49. Peralta, B., Biarnés, M., Ordóñez, G., Porta, R., Martín, M., Mateu, E., Pina, S., Meng, X.J., 2008. Evidence of widespread infection of avian hepatitis E virus (avian HEV) in chickens from Spain. Vet. Microbiol. Dec 13 (Epub ahead of print).
50. Pudupakam R.S., Huang Y.W., Opriessnig T., Halbur P.G., Pierson F.W., and Meng X.J. Deletions of the hypervariable region (HVR) in open reading frame 1 of hepatitis E virus do not abolish virus infectivity: evidence for attenuation of HVR deletion mutants in vivo. J. Virol. 83 (2009) 384-395
51. Purcell R.H., and Emerson S.U. Hepatitis E virus. In: Knipe D., Howley P., Griffin D., Lamb R., Martin M., Roizman B., et al. (Eds). Fields Virology. 4th ed. (2001), Lippincott: Williams and Wilkins, Philadelphia, PA 3051-3061
52. Renou C., Cadranel J.F., Bourlière M., Halfon P., Ouzan D., Rifflet H., Carenco P., Harafa A., Bertrand J.J., Boutrouille A., Muller P., Igual J.P., Decoppet A., Eloit M., and Pavio N. Possible zoonotic transmission of hepatitis E from pet pig to its owner. Emerg. Infect. Dis. 13 (2007) 1094-1096
53. Saad M.D., Hussein H.A., Bashandy M.M., Kamel H.H., Earhart K.C., Fryauff D.J., Younan M., and Mohamed A.H. Hepatitis E virus infection in work horses in Egypt. Infect. Genet. Evol. 7 (2007) 368-373
54. Shrestha M.P., Scott R.M., Joshi D.M., Mammen Jr. M.P., Thapa G.B., Thapa N., Myint K.S., Fourneau M., Kuschner R.A., Shrestha S.K., David M.P., Seriwatana J., Vaughn D.W., Safary A., Endy T.P., and Innis B.L. Safety and efficacy of a recombinant hepatitis E vaccine. N. Engl. J. Med. 356 (2007) 895-903
55. Sonoda H., Abe M., Sugimoto T., Sato Y., Bando M., Fukui E., Mizuo H., Takahashi M., Nishizawa T., and Okamoto H. Prevalence of hepatitis E virus (HEV) Infection in wild boars and deer and genetic identification of a genotype 3 HEV from a boar in Japan. J. Clin. Microbiol. 42 (2004) 5371-5374
56. Stoszek S.K., Engle R.E., Abdel-Hamid M., Mikhail N., Abdel-Aziz F., Medhat A., Fix A.D., Emerson S.U., Purcell R.H., and Strickland G.T. Hepatitis E antibody seroconversion without disease in highly endemic rural Egyptian communities. Trans. R. Soc. Trop. Med. Hyg. 100 (2006) 89-94
57. Sun Z.F., Larsen C.T., Dunlop A., Huang F.F., Pierson F.W., Toth T.E., and Meng X.J. Genetic identification of avian hepatitis E virus (HEV) from healthy chicken flocks and characterization of the capsid gene of 14 avian HEV isolates from chickens with hepatitis-splenomegaly syndrome in different geographical regions of the United States. J. Gen. Virol. 85 (2004) 693-700
58. Sun Z.F., Larsen C.T., Huang F.F., Billam P., Pierson F.W., Toth T.E., and Meng X.J. 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
59. Takahashi K., Kitajima N., Abe N., and Mishiro S. Complete or near-complete nucleotide sequences of hepatitis E virus genome recovered from a wild boar, a deer, and four patients who ate the deer. Virology 330 (2004) 501-505
60. Takahashi M., Yamada K., Hoshino Y., Takahashi H., Ichiyama K., Tanaka T., and Okamoto H. Monoclonal antibodies raised against the ORF3 protein of hepatitis E virus (HEV) can capture HEV particles in culture supernatant and serum but not those in feces. Arch. Virol. 153 (2008) 1703-1713
61. Tam A.W., Smith M.M., Guerra M.E., Huang C.C., Bradley D.W., Fry K.E., and Reyes G.R. Hepatitis E virus (HEV): molecular cloning and sequencing of the full-length viral genome. Virology 185 (1991) 120-131
62. Tei S., Kitajima N., Takahashi K., and Mishiro S. Zoonotic transmission of hepatitis E virus from deer to human beings. Lancet 362 (2003) 371-373
63. Tsarev S.A., Tsareva T.S., Emerson S.U., Rippy M.K., Zack P., Shapiro M., and Purcell R.H. 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
64. Usmanov R.K., Balaian M.S., Dvoǐnikova O.V., Alymbaeva D.B., Zamiatina N.A., Kazachkov IuA., and Belov V.I. An experimental infection in lambs by the hepatitis E virus. Vopr. Virusol. 39 (1994) 165-168
65. Withers M.R., Correa M.T., Morrow M., Stebbins M.E., Seriwatana J., Webster W.D., Boak M.B., and Vaughn D.W. Antibody levels to hepatitis E virus in North Carolina swine workers, non-swine workers, swine, and murids. Am. J. Trop. Med. Hyg. 66 (2002) 384-388
66. Yazaki Y., Mizuo H., Takahashi M., Nishizawa T., Sasaki N., Gotanda Y., and Okamoto H. Sporadic acute or fulminant hepatitis E in Hokkaido, Japan, may be food-borne, as suggested by the presence of hepatitis E virus in pig liver as food. J. Gen. Virol 84 (2003) 2351-2357
67. Zafrullah M., Ozdener M.H., Panda S.K., and Jameel S. The ORF3 protein of hepatitis E virus is a phosphoprotein that associates with the cytoskeleton. J. Virol. 71 (1997) 9045-9053