Current concepts of HBV/HCV coinfection: Coexistence, but not necessarily in harmony

Current Hepatitis Reports

Volumn 9, Issue 4, 2010, Pages 260-269

  Jamma, Shailaja ^a   Hussain, Ghazi ^a   Lau, Daryl T Y ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Epidemiology; Hepatitis B virus; Hepatitis C virus; Natural history; Pathogenesis; Pegylated interferon

Indexed keywords

HEPATITIS B SURFACE ANTIGEN; HEPATITIS B(E) ANTIGEN; INTERFERON; LAMIVUDINE; NUCLEOSIDE ANALOG; PEGINTERFERON; RIBAVIRIN; VIRUS DNA; VIRUS RNA;

ADAPTIVE IMMUNITY; CANCER RISK; CELL CULTURE; DISEASE COURSE; DISEASE SURVEILLANCE; DRUG EFFICACY; DRUG POTENTIATION; DRUG RESEARCH; ECHOGRAPHY; HEPATITIS B; HEPATITIS B VIRUS; HEPATITIS C; HEPATITIS C VIRUS; HOST RESISTANCE; HUMAN; INNATE IMMUNITY; LIVER CELL; LIVER CELL CARCINOMA; LIVER TRANSPLANTATION; MIXED INFECTION; MORTALITY; OUTCOME ASSESSMENT; PATHOGENESIS; PATIENT CARE; PATIENT MONITORING; PATIENT REFERRAL; PATIENT SELECTION; PREOPERATIVE EVALUATION; REVIEW; SUPERINFECTION; TREATMENT OUTCOME; VIRUS CELL INTERACTION; VIRUS REACTIVATION; VIRUS REPLICATION; VIRUS TRANSMISSION;

EID: 77958111500     PISSN: 15403416     EISSN: 15410706     Source Type: Journal    
DOI: 10.1007/s11901-010-0060-4     Document Type: Review

References (58)

1. RS Koff 2001 Risks associated with hepatitis A and hepatitis B in patients with hepatitis C J Clin Gastroenterol 33 20 26 10.1097/00004836- 200107000-00006 11418785 1:STN:280:DC%2BD3MzlslOqtA%3D%3D (Pubitemid 32613573)
2. V Brass D Moradpour 2009 New insights into hepatitis B and C virus co-infection J Hepatol 51 423 425 10.1016/j.jhep.2009.06.003 19596479
3. YF Liaw SL Tsai JJ Chang, et al. 1994 Displacement of hepatitis B virus by hepatitis C virus as the cause of continuing chronic hepatitis Gastroenterology 106 1048 1053 8143971 1:STN:280:DyaK2c7pt12gug%3D%3D
4. JP Zarski B Bohn A Bastie, et al. 1998 Characteristics of patients with dual infection by hepatitis B and C viruses J Hepatol 28 27 33 10.1016/S0168-8278(98)80198-0 9537860 1:CAS:528:DyaK1cXmvVWgtrk%3D (Pubitemid 28122496)
5. C Pasquinelli JM Shoenberger J Chung, et al. 1997 Hepatitis C virus core and E2 protein expression in transgenic mice Hepatology 25 719 727 10.1002/hep.510250338 9049225 1:CAS:528:DyaK2sXisVansbg%3D (Pubitemid 27106460)
6. SY Chen CF Kao CM Chen, et al. 2003 Mechanisms for inhibition of hepatitis B virus gene expression and replication by hepatitis C virus core protein J Biol Chem 278 591 607 10.1074/jbc.M204241200 12401801 1:CAS:528:DC%2BD38XpvVWnsrY%3D (Pubitemid 36043613)
7. CG Schuttler N Fiedler K Schmidt, et al. 2002 Suppression of hepatitis B virus enhancer 1 and 2 by hepatitis C virus core protein J Hepatol 37 855 862 10.1016/S0168-8278(02)00296-9 12445429 1:CAS:528:DC%2BD38XoslCjtbY%3D (Pubitemid 35404227)
8. NS Eyre RJ Phillips S Bowden, et al. 2009 Hepatitis B virus and hepatitis C virus interaction in Huh-7 cells J Hepatol 51 446 457 10.1016/j.jhep.2009.04. 025 19596477 1:CAS:528:DC%2BD1MXpsFyhsrg%3D This study demonstrated absence of direct interference between HBV and HCV in a highly reproducible cell culture system
9. P Bellecave J Gouttenoire M Gajer, et al. 2009 Hepatitis B and C virus coinfection: a novel model system reveals the absence of direct viral interference Hepatology 50 46 55 10.1002/hep.22951 19333911 1:CAS:528: DC%2BD1MXpt1ShsL8%3D This study independently concluded that cells with replicating HBV could be infected by HCV without superinfection exclusion
10. GB Gaeta G Stornaiuolo DF Precone, et al. 2003 Epidemiological and clinical burden of chronic hepatitis B virus/hepatitis C virus infection. A multicenter Italian study J Hepatol 39 1036 1041 10.1016/S0168-8278(03)00470-7 14642623 (Pubitemid 37523777)
11. YF Liaw 1995 Role of hepatitis C virus in dual and triple hepatitis virus infection Hepatology 22 4 Pt 1 1101 1108 7557857 1:STN:280: DyaK28%2FivFCitA%3D%3D
12. S Semnani G Roshandel N Abdolahi, et al. 2007 Hepatitis B/C virus co-infection in Iran: a seroepidemiological study Turk J Gastroenterol 18 20 21 17450490
13. MJ Alter D Kruszon-Moran OV Nainan, et al. 1999 The prevalence of hepatitis C virus infection in the United States, 1988 through 1994 N Engl J Med 341 556 562 10.1056/NEJM199908193410802 10451460 1:STN:280:DyaK1Mzmt1Whsw%3D%3D (Pubitemid 29384163)
14. A El-Sherif M Abou-Shady H Abou-Zeid, et al. 2009 Antibody to hepatitis B core antigen as a screening test for occult hepatitis B virus infection in Egyptian chronic hepatitis C patients J Gastroenterol 44 359 364 10.1007/s00535-009-0020-3 19271112 1:CAS:528:DC%2BD1MXkt1yitb4%3D
15. A Helmy MI Al-Sebayel 2006 Isolated antibody to hepatitis B core antigen in patients with chronic hepatitis C virus infection World J Gastroenterol 12 4406 4410 16865787 1:CAS:528:DC%2BD28XptVals74%3D
16. L Kazemi-Shirazi D Petermann C Muller 2000 Hepatitis B virus DNA in sera and liver tissue of HBsAg negative patients with chronic hepatitis C J Hepatol 33 785 790 10.1016/S0168-8278(00)80311-6 11097488 1:STN:280: DC%2BD3Mzgtlertw%3D%3D
17. M Rodriguez CA Navascues A Martinez, et al. 1992 Hepatitis C virus infection in patients with acute hepatitis B Infection 20 316 319 10.1007/BF01710674 1284057 1:STN:280:DyaK3s7os1ansg%3D%3D (Pubitemid 23009988)
18. YF Liaw CM Chu CS Chang-Chien CS Wui 1982 Simultaneous acute infections with hepatitis non-A, non-B, and B viruses Dig Dis Sci 27 762 764 10.1007/BF01393772 6807662 1:STN:280:DyaL383jsFejtg%3D%3D (Pubitemid 12095579)
19. C Feray M Gigou D Samuel, et al. 1993 Hepatitis C virus RNA and hepatitis B virus DNA in serum and liver of patients with fulminant hepatitis Gastroenterology 104 549 555 8381098 1:STN:280:DyaK3s7ks1aqsA%3D%3D (Pubitemid 23033429)
20. JC Wu CL Chen MC Hou, et al. 1994 Multiple viral infection as the most common cause of fulminant and subfulminant viral hepatitis in an area endemic for hepatitis B: application and limitations of the polymerase chain reaction Hepatology 19 836 840 10.1002/hep.1840190406 8138254 1:STN:280: DyaK2c7os1Wmuw%3D%3D
21. LT Mimms JW Mosley FB Hollinger, et al. 1993 Effect of concurrent acute infection with hepatitis C virus on acute hepatitis B virus infection BMJ 307 1095 1097 10.1136/bmj.307.6912.1095 8251805 1:STN:280:DyaK2c%2Fnt12iuw%3D%3D
22. N Coppola C Marrocco D Di Caprio, et al. 2003 Acute hepatitis B and C virus coinfection: a virological and clinical study of 3 cases Clin Infect Dis 36 528 532 10.1086/367650 12567314 (Pubitemid 36241324)
23. CM Chu IS Sheen YF Liaw 1994 The role of hepatitis C virus in fulminant viral hepatitis in an area with endemic hepatitis A and B Gastroenterology 107 189 195 8020661 1:STN:280:DyaK2c3ptFymsA%3D%3D
24. P Pontisso MG Ruvoletto G Fattovich, et al. 1993 Clinical and virological profiles in patients with multiple hepatitis virus infections Gastroenterology 105 1529 1533 8224658 1:STN:280:DyaK2c%2FktVGisg%3D%3D
25. YF Liaw SM Lin IS Sheen CM Chu 1991 Acute hepatitis C virus superinfection followed by spontaneous HBeAg seroconversion and HBsAg elimination Infection 19 250 251 10.1007/BF01644957 1917039 1:STN:280: DyaK38%2FhtVaguw%3D%3D
26. BN Tandon M Irshad SK Acharya YK Joshi 1991 Hepatitis C virus infection is the major cause of severe liver disease in India Gastroenterol Jpn 26 Suppl 3 192 195 1909266
27. YF Liaw CT Yeh SL Tsai 2000 Impact of acute hepatitis B virus superinfection on chronic hepatitis C virus infection Am J Gastroenterol 95 2978 2980 10.1111/j.1572-0241.2000.02337.x 11051381 1:STN:280:DC%2BD3crgt12gug%3D%3D
28. E Sagnelli N Coppola M Pisaturo, et al. 2009 HBV superinfection in HCV chronic carriers: a disease that is frequently severe but associated with the eradication of HCV Hepatology 49 1090 1097 10.1002/hep.22794 19263473 1:CAS:528:DC%2BD1MXkslSqu78%3D This article describes a long-term follow-up Italian study on the outcome of hepatitis C after HBV superinfection. A proportion of patients had prolonged HCV RNA clearance after HBV superinfection
29. R Fukuda N Ishimura M Niigaki, et al. 1999 Serologically silent hepatitis B virus coinfection in patients with hepatitis C virus-associated chronic liver disease: clinical and virological significance J Med Virol 58 201 207 10.1002/(SICI)1096-9071(199907)58:3<201::AID-JMV3>3.0.CO;2-2 10447413 1:STN:280:DyaK1MzhsV2rtg%3D%3D (Pubitemid 29278020)
30. K Koike M Kobayashi M Gondo, et al. 1998 Hepatitis B virus DNA is frequently found in liver biopsy samples from hepatitis C virus-infected chronic hepatitis patients J Med Virol 54 249 255 10.1002/(SICI)1096-9071(199804)54: 4<249::AID-JMV3>3.0.CO;2-4 9557290 1:STN:280:DyaK1c3hvVSnsQ%3D%3D (Pubitemid 28185416)
31. T Pollicino G Squadrito G Cerenzia, et al. 2004 Hepatitis B virus maintains its pro-oncogenic properties in the case of occult HBV infection Gastroenterology 126 102 110 10.1053/j.gastro.2003.10.048 14699492 1:CAS:528:DC%2BD2cXhtFGntLs%3D (Pubitemid 38040728)
32. I Cacciola T Pollicino G Squadrito, et al. 1999 Occult hepatitis B virus infection in patients with chronic hepatitis C liver disease N Engl J Med 341 22 26 10.1056/NEJM199907013410104 10387938 1:STN:280:DyaK1M3psVeltA%3D%3D (Pubitemid 29293716)
33. R Colombari AP Dhillon E Piazzola, et al. 1993 Chronic hepatitis in multiple virus infection: histopathological evaluation Histopathology 22 319 325 10.1111/j.1365-2559.1993.tb00130.x 8514275 1:STN:280:DyaK3s3ptlWluw%3D%3D
34. JH Kao PJ Chen MY Lai DS Chen 2002 Occult hepatitis B virus infection and clinical outcomes of patients with chronic hepatitis C J Clin Microbiol 40 4068 4071 10.1128/JCM.40.11.4068-4071.2002 12409376 1:CAS:528:DC%2BD38XptVOisLw%3D (Pubitemid 35285791)
35. TL Fong AM Di Bisceglie JG Waggoner, et al. 1991 The significance of antibody to hepatitis C virus in patients with chronic hepatitis B Hepatology 14 64 67 10.1002/hep.1840140111 1648540 1:STN:280:DyaK3M3ptlOgsQ%3D%3D
36. S Mohamed Ael MA al Karawi GA Mesa 1997 Dual infection with hepatitis C and B viruses: clinical and histological study in Saudi patients Hepatogastroenterology 44 1404 1406 9356863
37. H Tanaka H Tsukuma H Yamano, et al. 2004 Prospective study on the risk of hepatocellular carcinoma among hepatitis C virus-positive blood donors focusing on demographic factors, alanine aminotransferase level at donation and interaction with hepatitis B virus Int J Cancer 112 1075 1080 10.1002/ijc.20507 15386355 1:CAS:528:DC%2BD2cXhtVSnsLfL (Pubitemid 39507017)
38. MC Kew MC Yu MA Kedda, et al. 1997 The relative roles of hepatitis B and C viruses in the etiology of hepatocellular carcinoma in southern African blacks Gastroenterology 112 184 187 10.1016/S0016-5085(97)70233-6 8978357 1:STN:280:DyaK2s7jt12qug%3D%3D
39. L Benvegnu G Fattovich F Noventa, et al. 1994 Concurrent hepatitis B and C virus infection and risk of hepatocellular carcinoma in cirrhosis. A prospective study Cancer 74 2442 2448 10.1002/1097-0142(19941101)74:9<2442:: AID-CNCR2820740909>3.0.CO;2-# 7922998 1:STN:280:DyaK2M%2Fgslersw%3D%3D (Pubitemid 24320846)
40. F Donato P Boffetta M Puoti 1998 A meta-analysis of epidemiological studies on the combined effect of hepatitis B and C virus infections in causing hepatocellular carcinoma Int J Cancer 75 347 354 10.1002/(SICI)1097- 0215(19980130)75:3<347::AID-IJC4>3.0.CO;2-2 9455792 1:STN:280: DyaK1c7hsFehtQ%3D%3D (Pubitemid 28100034)
41. M Chiaramonte T Stroffolini A Vian, et al. 1999 Rate of incidence of hepatocellular carcinoma in patients with compensated viral cirrhosis Cancer 85 2132 2137 10.1002/(SICI)1097-0142(19990515)85:10<2132::AID-CNCR6>3.0.CO;2- H 10326690 1:STN:280:DyaK1M3ls1KhsA%3D%3D (Pubitemid 29215551)
42. RC Guptan V Thakur V Raina SK Sarin 1999 Alpha-interferon therapy in chronic hepatitis due to active dual infection with hepatitis B and C viruses J Gastroenterol Hepatol 14 893 898 10.1046/j.1440-1746.1999.01952.x 10535471 1:CAS:528:DyaK1MXmsFOntL8%3D (Pubitemid 29459799)
43. I Hasegawa E Orito Y Tanaka, et al. 2005 Impact of occult hepatitis B virus infection on efficacy and prognosis of interferon-alpha therapy for patients with chronic hepatitis C Liver Int 25 247 253 10.1111/j.1478-3231.2005. 1096.x 15780046
44. YF Liaw RN Chien SM Lin, et al. 1997 Response of patients with dual hepatitis B virus and C virus infection to interferon therapy J Interferon Cytokine Res 17 449 452 10.1089/jir.1997.17.449 9282824 1:CAS:528: DyaK2sXlsFegtrg%3D
45. E Villa A Grottola P Buttafoco, et al. 2001 High doses of alpha-interferon are required in chronic hepatitis due to coinfection with hepatitis B virus and hepatitis C virus: long term results of a prospective randomized trial Am J Gastroenterol 96 2973 2977 11693335 1:CAS:528: DC%2BD3MXot1Cgsrg%3D
46. MD Weltman A Brotodihardjo EB Crewe, et al. 1995 Coinfection with hepatitis B and C or B, C and delta viruses results in severe chronic liver disease and responds poorly to interferon-alpha treatment J Viral Hepat 2 39 45 10.1111/j.1365-2893.1995.tb00070.x 7493293 1:STN:280:DyaK28%2FptFejtQ%3D%3D
47. AL Zignego R Fontana S Puliti, et al. 1997 Relevance of inapparent coinfection by hepatitis B virus in alpha interferon-treated patients with hepatitis C virus chronic hepatitis J Med Virol 51 313 318 10.1002/(SICI)1096- 9071(199704)51:4<313::AID-JMV9>3.0.CO;2-8 9093946 1:STN:280: DyaK2s3kslyhsQ%3D%3D (Pubitemid 27148581)
48. WL Chuang CY Dai WY Chang, et al. 2005 Viral interaction and responses in chronic hepatitis C and B coinfected patients with interferon-alpha plus ribavirin combination therapy Antivir Ther 10 125 133 15751770 1:CAS:528:DC%2BD2MXis1KmtbY%3D
49. P Fabris D Brown G Tositti, et al. 2004 Occult hepatitis B virus infection does not affect liver histology or response to therapy with interferon alpha and ribavirin in intravenous drug users with chronic hepatitis C J Clin Virol 29 160 166 10.1016/S1386-6532(03)00117-3 14962784 1:CAS:528: DC%2BD2cXhtFWlt7k%3D (Pubitemid 38201461)
50. CH Hung CM Lee SN Lu, et al. 2005 Combination therapy with interferon-alpha and ribavirin in patients with dual hepatitis B and hepatitis C virus infection J Gastroenterol Hepatol 20 727 732 10.1111/j.1440-1746.2005. 03791.x 15853986 1:CAS:528:DC%2BD2MXls1amu7w%3D (Pubitemid 40733367)
51. CJ Liu PJ Chen MY Lai, et al. 2003 Ribavirin and interferon is effective for hepatitis C virus clearance in hepatitis B and C dually infected patients Hepatology 37 568 576 10.1053/jhep.2003.50096 12601355 1:CAS:528: DC%2BD3sXit1yltr0%3D (Pubitemid 36258779)
52. S Mrani I Chemin K Menouar, et al. 2007 Occult HBV infection may represent a major risk factor of non-response to antiviral therapy of chronic hepatitis C J Med Virol 79 1075 1081 10.1002/jmv.20943 17596829 1:CAS:528:DC%2BD2sXotl2ktL0%3D (Pubitemid 47015405)
53. RP Myers V Thibault T Poynard 2003 The impact of prior hepatitis B virus infection on liver histology and the response to interferon therapy in chronic hepatitis C J Viral Hepat 10 103 110 10.1046/j.1365-2893.2003.00407.x 12614466 1:CAS:528:DC%2BD3sXjvFClsb4%3D (Pubitemid 36359847)
54. CJ Liu WL Chuang CM Lee, et al. 2009 Peginterferon alfa-2a plus ribavirin for the treatment of dual chronic infection with hepatitis B and C viruses Gastroenterology 136 496 504 e3 10.1053/j.gastro.2008.10.049 19084016 1:CAS:528:DC%2BD1MXislOhtLg%3D This article describes the largest prospective, randomized, controlled trial using pegylated interferon and ribavirin therapy on HBV and HCV coinfection. This Taiwanese study confirmed high HCV SVR but also high rate of HBV reactivation during combination therapy
55. A Potthoff H Wedemeyer WO Boecher, et al. 2008 The HEP-NET B/C co-infection trial: A prospective multicenter study to investigate the efficacy of pegylated interferon-alpha2b and ribavirin in patients with HBV/HCV co-infection J Hepatol 49 688 694 10.1016/j.jhep.2008.03.028 18490077 1:CAS:528:DC%2BD1cXht1eju7jK This study reported that HCV genotype 1 and non-1 patients both had excellent SVR in the setting of co-infection. They observed four patients with undetectable serum HBV DNA at baseline had reactivation of HBV after HCV RNA clearance
56. H Senturk V Tahan B Canbakan, et al. 2008 Chronic hepatitis C responds poorly to combination therapy in chronic hepatis B carriers Neth J Med 66 191 195 18490796 1:CAS:528:DC%2BD1cXnsFWgt7k%3D
57. JW Yu LJ Sun YH Zhao, et al. 2009 Analysis of the efficacy of treatment with peginterferon alpha-2a and ribavirin in patients coinfected with hepatitis B virus and hepatitis C virus Liver Int 29 1485 1493 10.1111/j.1478-3231.2009. 02080.x 19602134 1:CAS:528:DC%2BD1MXhtlGgtb%2FJ This study showed that HBV reactivation rate was significantly higher among those who achieved HCV SVR compared to those without SVR
58. A Marrone R Zampino M D'Onofrio, et al. 2004 Combined interferon plus lamivudine treatment in young patients with dual HBV (HBeAg positive) and HCV chronic infection J Hepatol 41 1064 1065 10.1016/j.jhep.2004.07.009 15582146 1:CAS:528:DC%2BD2cXhtVCgsLjO (Pubitemid 39575680)