Hepatitis E Virus Superinfection and Clinical Progression in Hepatitis B Patients

EBioMedicine

Volumn 2, Issue 12, 2015, Pages 2080-2086

  Hoan, Nghiem Xuan ^a   Tong, Hoang Van ^a   Hecht, Nicole ^b   Sy, Bui Tien ^b,c   Marcinek, Patrick ^a   Meyer, Christian G ^a   Song, Le Huu ^c   Toan, Nguyen Linh ^d   Kurreck, Jens ^e   Kremsner, Peter G ^a   Bock, C Thomas ^b   Velavan, Thirumalaisamy P ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b ROBERT KOCH INSTITUTE   (Germany)

^c Tran Hung Dao Hospital   (Viet Nam)

^d VIETNAM MILITARY MEDICAL UNIVERSITY   (Viet Nam)

^e TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

Author keywords

HBV infection; HBV related liver diseases; Hepatitis E virus; HEV seroprevalence; HEV superinfection

Indexed keywords

ALANINE AMINOTRANSFERASE; ALBUMIN; ALPHA FETOPROTEIN; ASPARTATE AMINOTRANSFERASE; BILIRUBIN; HEPATITIS E ANTIBODY; PROTHROMBIN; HEPATITIS ANTIBODY; VIRUS RNA;

ACUTE HEPATITIS B; ADOLESCENT; ADULT; AGED; ARTICLE; CHILD; CHRONIC HEPATITIS B; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DISEASE COURSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HEPATITIS E; HEPATITIS E VIRUS; HEPATITIS E VIRUS GENOTYPE 3; HUMAN; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LIVER FUNCTION TEST; MAJOR CLINICAL STUDY; MALE; PHYLOGENY; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; SEROPREVALENCE; SUPERINFECTION; THROMBOCYTE COUNT; VIETNAMESE; VIRUS LOAD; CASE CONTROL STUDY; CLINICAL TRIAL; COMPLICATION; GENOTYPE; HEPATITIS B; HEPATITIS B VIRUS; LIVER NEOPLASMS; MIDDLE AGED; MIXED INFECTION; MULTICENTER STUDY; OUTCOME ASSESSMENT; PHYSIOLOGY; PREVALENCE; SEROEPIDEMIOLOGY; VERY ELDERLY; VIET NAM; VIROLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; CASE-CONTROL STUDIES; CHILD; COINFECTION; CROSS-SECTIONAL STUDIES; FEMALE; GENOTYPE; HEPATITIS ANTIBODIES; HEPATITIS B; HEPATITIS B VIRUS; HEPATITIS E; HEPATITIS E VIRUS; HUMANS; LIVER CIRRHOSIS; LIVER NEOPLASMS; MALE; MIDDLE AGED; PATIENT OUTCOME ASSESSMENT; PREVALENCE; RNA, VIRAL; SEROEPIDEMIOLOGIC STUDIES; SUPERINFECTION; VIETNAM; YOUNG ADULT;

EID: 84958889796     PISSN: None     EISSN: 23523964     Source Type: Journal    
DOI: 10.1016/j.ebiom.2015.11.020     Document Type: Article

References (45)

1. Abravanel F., Lhomme S., Chapuy-Regaud S., Mansuy J.M., Muscari F., Sallusto F., Rostaing L., Kamar N., Izopet J. Hepatitis E virus reinfections in solid-organ-transplant recipients can evolve into chronic infections. J. Infect. Dis. 2014, 209:1900-1906.
2. Atiq M., Shire N.J., Barrett A., Rouster S.D., Sherman K.E., Shata M.T. Hepatitis E virus antibodies in patients with chronic liver disease. Emerg. Infect. Dis. 2009, 15:479-481.
3. Avellon A., Morago L., Garcia-Galera Del C.M., Munoz M., Echevarria J.M. Comparative sensitivity of commercial tests for hepatitis E genotype 3 virus antibody detection. J. Med. Virol. 2015, 87:1934-1939.
4. Bayram A., Eksi F., Mehli M., Sozen E. Prevalence of hepatitis E virus antibodies in patients with chronic hepatitis B and chronic hepatitis C. Intervirology 2007, 50:281-286.
5. 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.
6. Boccia D., Guthmann J.P., Klovstad H., Hamid N., Tatay M., Ciglenecki I., Nizou J.Y., Nicand E., Guerin P.J. High mortality associated with an outbreak of hepatitis E among displaced persons in Darfur, Sudan. Clin. Infect. Dis. 2006, 42:1679-1684.
7. 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.
8. Cao D., Meng X.J. Molecular biology and replication of hepatitis E virus. Emerg. Microbes Infect. 2012, 1.
9. Cheng S.H., Mai L., Zhu F.Q., Pan X.F., Sun H.X., Cao H., Shu X., Ke W.M., Li G., Xu Q.H. Influence of chronic HBV infection on superimposed acute hepatitis E. World J. Gastroenterol. 2013, 19:5904-5909.
10. Cholongitas E., Papatheodoridis G.V., Vangeli M., Terreni N., Patch D., Burroughs A.K. Systematic review: the model for end-stage liver disease-should it replace Child-Pugh's classification for assessing prognosis in cirrhosis?. Aliment. Pharmacol. Ther. 2005, 22:1079-1089.
11. Chow C.W., Tsang S.W., Tsang O.T., Leung V.K., Fung K.S., Luk W.K., Chau T.N. Comparison of acute hepatitis E infection outcome in patients with and without chronic hepatitis B infection: A 10 year retrospective study in three regional hospitals in Hong Kong. J. Clin. Virol. 2014, 60:4-10.
12. Christensen P.B., Engle R.E., Hjort C., Homburg K.M., Vach W., Georgsen J., Purcell R.H. 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.
13. Cleland A., Smith L., Crossan C., Blatchford O., Dalton H.R., Scobie L., Petrik J. Hepatitis E virus in Scottish blood donors. Vox Sang. 2013, 105:283-289.
14. Dalton H.R. Hepatitis: hepatitis E and decompensated chronic liver disease. Nat. Rev. Gastroenterol. Hepatol. 2012, 9:430-432.
15. Dalton H.R., Bendall R.P., Keane F.E., Tedder R.S., Ijaz S. Persistent carriage of hepatitis E virus in patients with HIV infection. N. Engl. J. Med. 2009, 361:1025-1027.
16. Dalton H.R., Hunter J.G., Bendall R.P. Hepatitis E. Curr. Opin. Infect. Dis. 2013, 26:471-478.
17. Dunford L., Carr M.J., Dean J., Nguyen L.T., Ta Thi T.H., Nguyen B.T., Connell J., Coughlan S., Nguyen H.T., Hall W.W., Thi L.A. A multicentre molecular analysis of hepatitis B and blood-borne virus coinfections in Viet Nam. PLoS One 2012, 7.
18. Feldt T., Sarfo F.S., Zoufaly A., Phillips R.O., Burchard G., van L.J., Jochum J., Chadwick D., Awasom C., Claussen L., Drosten C., Drexler J.F., Eis-Hubinger A.M. Hepatitis E virus infections in HIV-infected patients in Ghana and Cameroon. J. Clin. Virol. 2013, 58:18-23.
19. Gallian P., Lhomme S., Piquet Y., Saune K., Abravanel F., Assal A., Tiberghien P., Izopet J. Hepatitis E virus infections in blood donors, France. Emerg. Infect. Dis. 2014, 20:1914-1917.
20. Gerolami R., Moal V., Colson P. Chronic hepatitis E with cirrhosis in a kidney-transplant recipient. N. Engl. J. Med. 2008, 358:859-860.
21. Guo Q.S., Yan Q., Xiong J.H., Ge S.X., Shih J.W., Ng M.H., Zhang J., Xia N.S. Prevalence of hepatitis E virus in Chinese blood donors. J. Clin. Microbiol. 2010, 48:317-318.
22. Hamid S.S., Atiq M., Shehzad F., Yasmeen A., Nissa T., Salam A., Siddiqui A., Jafri W. Hepatitis E virus superinfection in patients with chronic liver disease. Hepatology 2002, 36:474-478.
23. Hau C.H., Hien T.T., Tien N.T., Khiem H.B., Sac P.K., Nhung V.T., Larasati R.P., Laras K., Putri M.P., Doss R., Hyams K.C., Corwin A.L. Prevalence of enteric hepatitis A and E viruses in the Mekong River Delta region of Vietnam. Am. J.Trop. Med. Hyg. 1999, 60:277-280.
24. Juhl D., Baylis S.A., Blumel J., Gorg S., Hennig H. Seroprevalence and incidence of hepatitis E virus infection in German blood donors. Transfusion 2014, 54:49-56.
25. Kamar N., Selves J., Mansuy J.M., Ouezzani L., Peron J.M., Guitard J., Cointault O., Esposito L., Abravanel F., Danjoux M., Durand D., Vinel J.P., Izopet J., Rostaing L. Hepatitis E virus and chronic hepatitis in organ-transplant recipients. N. Engl. J. Med. 2008, 358:811-817.
26. Kamar N., Bendall R., Legrand-Abravanel F., Xia N.S., Ijaz S., Izopet J., Dalton H.R. Hepatitis E. Lancet 2012, 379:2477-2488.
27. Kamar N., Dalton H.R., Abravanel F., Izopet J. Hepatitis E virus infection. Clin. Microbiol. Rev. 2014, 27:116-138.
28. Kumar A.S., Kumar S.P., Singh R., Kumar M.S., Madan K., Kumar J.J., Kumar P.S. Hepatitis E virus (HEV) infection in patients with cirrhosis is associated with rapid decompensation and death. J. Hepatol. 2007, 46:387-394.
29. Mansuy J.M., Bendall R., Legrand-Abravanel F., Saune K., Miedouge M., Ellis V., Rech H., Destruel F., Kamar N., Dalton H.R., Izopet J. Hepatitis E virus antibodies in blood donors, France. Emerg. Infect. Dis. 2011, 17:2309-2312.
30. Marion-Audibert A.M., Tesse S., Graillot E., Phelip G., Radenne S., Duperret S., Durieux M., Rode A., Mabrut J.Y., Souquet J.C., Nicand E. Lethal acute HEV superinfection on hepatitis B cirrhosis. Gastroenterol. Clin. Biol. 2010, 34:334-336.
31. Monga R., Garg S., Tyagi P., Kumar N. Superimposed acute hepatitis E infection in patients with chronic liver disease. Indian J. Gastroenterol. 2004, 23:50-52.
32. Nguyen V.T. Hepatitis B infection in Vietnam: current issues and future challenges. Asia Pac. J. Public Health 2012, 24:361-373.
33. Pas S.D., Streefkerk R.H., Pronk M., de Man R.A., Beersma M.F., Osterhaus A.D., van der Eijk A.A. Diagnostic performance of selected commercial HEV IgM and IgG ELISAs for immunocompromised and immunocompetent patients. J. Clin. Virol. 2013, 58:629-634.
34. Pischke S., Gisa A., Suneetha P.V., Wiegand S.B., Taubert R., Schlue J., Wursthorn K., Bantel H., Raupach R., Bremer B., Zacher B.J., Schmidt R.E., Manns M.P., Rifai K., Witte T., Wedemeyer H. Increased HEV seroprevalence in patients with autoimmune hepatitis. PLoS One 2014, 9.
35. Pittaras T., Valsami S., Mavrouli M., Kapsimali V., Tsakris A., Politou M. Seroprevalence of hepatitis E virus in blood donors in Greece. Vox Sang. 2014, 106:387.
36. 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.
37. Ren F., Zhao C., Wang L., Wang Z., Gong X., Song M., Zhuang H., Huang Y., Shan H., Wang J., Liu Q., Ness P., Nelson K.E., Wang Y. Hepatitis E virus seroprevalence and molecular study among blood donors in China. Transfusion 2014, 54:910-917.
38. Shukla P., Nguyen H.T., Torian U., Engle R.E., Faulk K., Dalton H.R., Bendall R.P., Keane F.E., Purcell R.H., Emerson S.U. Cross-species infections of cultured cells by hepatitis E virus and discovery of an infectious virus-host recombinant. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:2438-2443.
39. Song L.H., Binh V.Q., Duy D.N., Kun J.F., Bock T.C., Kremsner P.G., Luty A.J. Serum cytokine profiles associated with clinical presentation in Vietnamese infected with hepatitis B virus. J. Clin. Virol. 2003, 28:93-103.
40. Wenzel J.J., Preiss J., Schemmerer M., Huber B., Jilg W. Test performance characteristics of anti-HEV IgG assays strongly influence hepatitis E seroprevalence estimates. J. Infect. Dis. 2013, 207:497-500.
41. WHO Hepatitis B. Fact sheet N° 204 2013, (Ref Type: Report).
42. WHO Hepatitis E. Fact sheet N° 280 2014, (Ref Type: Report).
43. Wu T., Huang S.J., Zhu F.C., Zhang X.F., Ai X., Yan Q., Wang Z.Z., Yang C.L., Jiang H.M., Liu X.H., Guo M., Du H.L., Ng M.H., Zhang J., Xia N.S. Immunogenicity and safety of hepatitis E vaccine in healthy hepatitis B surface antigen positive adults. Hum. Vaccin. Immunother. 2013, 9:2474-2479.
44. Wu W.C., Su C.W., Yang J.Y., Lin S.F., Chen J.Y., Wu J.C. Application of serologic assays for diagnosing acute hepatitis E in national surveillance of a nonendemic area. J. Med. Virol. 2014, 86:720-728.
45. 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., Guo M., Liu X.H., Li J.X., Yang C.L., Tang Q., Jiang R.J., Pan H.R., Li Y.M., Shih J.W., Ng M.H., Zhu F.C., Xia N.S. Long-term efficacy of a hepatitis E vaccine. N. Engl. J. Med. 2015, 372:914-922.