Chronic Hepatitis B virus infection

Journal of Clinical Gastroenterology

Volumn 50, Issue 4, 2016, Pages 286-294

  Yuen, Man Fung ^a   Ahn, Sang Hoon ^b   Chen, Ding Shinn ^c   Chen, Pei Jer ^c   Dusheiko, Geoffrey M ^d   Hou, Jin Lin ^e   Maddrey, Willis C ^f   Mizokami, Masashi ^g   Seto, Wai Kay ^a   Zoulim, Fabien ^h   Lai, Ching Lung ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b Yonsei University   (South Korea)

^c NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^d ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^e SOUTHERN MEDICAL UNIVERSITY   (China)

^f UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^g NATIONAL CENTER FOR GLOBAL HEALTH AND MEDICINE   (Japan)

^h CENTRE DE RECHERCHE EN CANCÉROLOGIE DE LYON   (France)

Author keywords

chronic hepatitis B; natural history; treatment

Indexed keywords

ALANINE AMINOTRANSFERASE; CIRCULAR DNA; ENTECAVIR; HEPATITIS B SURFACE ANTIGEN; HEPATITIS B(E) ANTIGEN; HLA DP ANTIGEN; HOST FACTOR; LAMIVUDINE; PEGINTERFERON ALPHA; TENOFOVIR DISOPROXIL; VIRUS DNA; ANTIVIRUS AGENT; BIOLOGICAL MARKER;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ALCOHOL CONSUMPTION; ANTIVIRAL RESISTANCE; CANCER DIAGNOSIS; CANCER SCREENING; CHRONIC HEPATITIS B; CROSS RESISTANCE; FAMILY HISTORY; GROUPS BY AGE; HEPATITIS B VIRUS; HUMAN; IMMUNOLOGICAL TOLERANCE; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LIVER HISTOLOGY; LONG TERM CARE; MONOTHERAPY; MULTICENTER STUDY (TOPIC); MULTIDRUG RESISTANCE; NONHUMAN; PATIENT MONITORING; PERSISTENT INFECTION; PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; REVIEW; RISK FACTOR; SEROCONVERSION; SEX DIFFERENCE; TREATMENT DURATION; VIRUS LOAD; VIRUS REACTIVATION; VIRUS REPLICATION; BLOOD; DRUG EFFECTS; GENETICS; GENOTYPE; HEPATITIS B, CHRONIC; HOST PATHOGEN INTERACTION; IMMUNOLOGY; TREATMENT OUTCOME;

ANTIVIRAL AGENTS; BIOMARKERS; DNA, VIRAL; DRUG RESISTANCE, VIRAL; GENOTYPE; HEPATITIS B SURFACE ANTIGENS; HEPATITIS B VIRUS; HEPATITIS B, CHRONIC; HOST-PATHOGEN INTERACTIONS; HUMANS; TREATMENT OUTCOME; VIRAL LOAD;

EID: 84984550324     PISSN: 01920790     EISSN: 15392031     Source Type: Journal    
DOI: 10.1097/MCG.0000000000000478     Document Type: Review

References (96)

1. Paraskevis D, Magiorkinis G, Magiorkinis E, et al. Dating the origin and dispersal of hepatitis B virus infection in humans and primates. Hepatology. 2013; 57: 908-916.
2. Tedder RS, Rodger AJ, Fries L, et al. The diversity and management of chronic hepatitis B virus infections in the United Kingdom: a wake-up call. Clin Infect Dis. 2013; 56: 951-960.
3. Kowdley KV, Wang CC, Welch S, et al. Prevalence of chronic hepatitis B among foreign-born persons living in the United States by country of origin. Hepatology. 2012; 56: 422-433.
4. Steven CE, Neurath RA, Beasley RP, et al. HBeAg and anti-HBe detection by radiommunoassay: correlation with vertical transmission of hepatitis B in Taiwan. J Med Virol. 1979; 3: 237-241.
5. Zoulim F, Mason WS. Reasons to consider earlier treatment of chronic HBV infections. Gut. 2012; 61: 333-336.
6. Tsai SL, Chen PJ, Lai MY, et al. Acute exacerbation of chronic type B hepatitis are accompanied by increased T cell responses to hepatitis B core and e antigens. Implications for hepatitis B e antigen seroconversion. J Clin Invest. 1992; 89: 87-96.
7. Chen DS. From hepatitis to hepatoma: lessons from type B viral hepatitis. Science. 1993; 262: 369-370.
8. Chen CJ, Yang HI, Su J, et al. Risk of hepatocellular carcinoma across a biological gradient of serum hepatitis B virus DNA level. JAMA. 2006; 295: 65-73.
9. Iloeje UH, Yang HI, Su J, et al. Predicting cirrhosis risk based on the level of circulating hepatitis B viral load. Gastroenterology. 2006; 130: 678-686.
10. Yang HI, Lu SN, Liaw YF, et al. Hepatitis B e antigen and the risk of hepatocellular carcinoma. N Engl J Med. 2002; 347: 168-174.
11. Blumberg BS, Sutnick AI, London WT, et al. Sex distribution of Australia antigen. Arch Intern Med. 1972; 130: 227-231.
12. Chu CM, Liaw YF, Sheen IS, et al. Sex difference in chronic hepatitis B virus infection: an appraisal based on the status of hepatitis B e antigen and antibody. Hepatology. 1983; 3: 947-950.
13. Huang YT, Jen CL, Yang HI, et al. Lifetime risk and sex difference of hepatocellular carcinoma among patients with chronic hepatitis B and C. J Clin Oncol. 2011; 29: 3643-3650.
14. Alexandrov LB, Nik-Zainal S, Wedge DC, et al. Signatures of mutational processes in human cancer. Nature. 2013; 500: 415-421.
15. Yu MW, Chang HC, Chen PJ, et al. Increased risk for hepatitis B-related liver cirrhosis in relatives of patients with hepatocellular carcinoma in northern Taiwan. Int J Epidemiol. 2002; 31: 1008-1015.
16. Nishida N, Tokunaga K, Mizokami M, et al. Genome-wide association study confirming association of HLA-DP with protection against chronic hepatitis B and viral clearance in Japanese and Korean. PLoS One. 2012; 7: e39175.
17. Kumar M, Sarin SK, Hissar S, et al. Virologic and histologic features of chronic hepatitis B virus-infected asymptomatic patients with persistently normal ALT. Gastroenterology. 2008; 134: 1376-1384.
18. Zacharakis G, Koskinas J, Kotsiou S, et al. The role of serial measurement of serum HBV DNA levels in patients with chronic HBeAg(-) hepatitis B infection: association with liver disease progression A prospective cohort study. J Hepatol. 2008; 49: 884-891.
19. Tsang PS, Trinh H, Garcia RT, et al. Significant prevalence of histologic disease in patients with chronic hepatitis B and mildly elevated serum alanine aminotransferase levels. Clin Gastroenterol Hepatol. 2008; 6: 569-574.
20. Nguyen MH, Garcia RT, Trinh HN, et al. Histological disease in Asian-Americans with chronic hepatitis B, high hepatitis B virus DNA, and normal alanine aminotransferase levels. Am J Gastroenterol. 2009; 104: 2206-2213.
21. Yuen MF, Tanaka Y, Fong DY, et al. Independent risk factors and predictive score for the development of hepatocellular carcinoma in chronic hepatitis B. J Hepatol. 2009; 50: 80-88.
22. Yuen MF, Yuan HJ, Wong DK, et al. Prognostic determinants for chronic hepatitis B in Asians: therapeutic implications. Gut. 2005; 54: 1610-1614.
23. Yuan HJ, Yuen MF, Wong DKH, et al. The relationship between HBV-DNA levels and cirrhosis-related complications in Chinese with chronic hepatitis B. J Viral Hepatitis. 2005; 12: 373-379.
24. Fung J, Yuen MF, Yuen JC, et al. Low serum HBV DNA levels and development of hepatocellular carcinoma in patients with chronic hepatitis B: a case-control study. Aliment Pharmacol Ther. 2007; 26: 377-382.
25. Orito E, Mizokami M, Ina Y, et al. Host-independent evolution and a genetic classification of the hepadnavirus family based on nucleotide sequences. Proc Natl Acad Sci USA. 1989; 86: 7059-7062.
26. Liu S, Zhang H, Gu C, et al. Associations between hepatitis B virus mutations and the risk of hepatocellular carcinoma: a meta-Analysis. J Natl Cancer Inst. 2009; 101: 1066-1082.
27. Cho EY, Kim HJ, Park C, et al. Impact of nucleotide mutations at the HNF3- And HNF4-binding sites in enhancer 1 on viral replication in patients with chronic hepatitis B virus infection. Gut Liver. 2013; 7: 569-575.
28. Milich DR, Thornton GB, Neurath AR, et al. Enhanced immunogenicity of the pre-S region of hepatitis B surface antigen. Science. 1985; 228: 1195-1199.
29. Tseng TC, Liu CJ, Yang HC, et al. High levels of hepatitis B surface antigen increase risk of hepatocellular carcinoma in patients with low HBV load. Gastroenterology. 2012; 142: 1140-1149.
30. Yang HI, Sherman M, Su J, et al. Nomograms for risk of hepatocellular carcinoma in patients with chronic hepatitis B virus infection. J Clin Oncol. 2010; 28: 2437-2444.
31. Yang HI, Yuen MF, Chan HL, et al. Risk estimation for hepatocellular carcinoma in chronic hepatitis B (REACH-B): development and validation of a predictive score. Lancet Oncol. 2011; 12: 568-574.
32. Wong VW, Chan SL, Mo F, et al. Clinical scoring system to predict hepatocellular carcinoma in chronic hepatitis B carriers. J Clin Oncol. 2010; 28: 1660-1665.
33. Abu-Amara M, Cerocchi O, Malhi G, et al. The applicability of hepatocellular carcinoma risk prediction scores in a North American patient population with chronic hepatitis B infection. Gut. 2016. (In press).
34. Jung KS, Kim SU, Ahn SH, et al. Risk assessment of hepatitis B virus-related hepatocellular carcinoma development using liver stiffness measurement (FibroScan). Hepatology. 2011; 53: 885-894.
35. Prati D, Taioli E, Zanella A, et al. Updated definitions of healthy ranges for serum alanine aminotransferase levels. Ann Intern Med. 2002; 137: 1-10.
36. Chan HL, Chan CK, Hui AJ, et al. Effects of tenofovir disoproxil fumarate in hepatitis B e antigen-positive patients with normal levels of alanine aminotransferase and high levels of hepatitis B virus DNA. Gastroenterology. 2014; 146: 1240-1248.
37. Fung J, Seto WK, Lai CL, et al. Profiles of HBV DNA in a large population of Chinese patients with chronic hepatitis B: implications for antiviral therapy. J Hepatol. 2011; 54: 195-200.
38. Yuen MF, Ng IO, Fan ST, et al. Significance of HBV DNA levels in liver histology of HBeAg and Anti-HBe positive patients with chronic hepatitis B. Am J Gastroenterol. 2004; 99: 2032-2037.
39. Chao DT, Lim JK, Ayoub WS, et al. Systemic review with meta-Analysis: the proportion of chronic hepatitis B patients with normal alanine transaminase r40 IU/L and significant fibrosis. Aliment Pharmacol Ther. 2014; 39: 349-358.
40. Nguyen LH, Chao D, Lim JK, et al. Histologic changes in liver tissue from patients with chronic hepatitis B and minimal increases in levels of alanine aminotransferase: a meta-Analysis and systematic review. Clin Gastroenterol Hepatol. 2014; 12: 1262-1266.
41. Tong MJ, Hsien C, Hsu L, et al. Treatment recommendations for chronic hepatitis B: an evaluation of current guidelines based on a natural history study in the United States. Hepatology. 2008; 48: 1070-1078.
42. Yuen MF, Tanaka Y, Shinkai N, et al. Risk for hepatocellular carcinoma with respect to hepatitis B virus genotypes B/C, specific mutations of enhancer II/core promoter/precore regions and HBV DNA levels. Gut. 2008; 57: 98-102.
43. Lau GKK, Piratvisuth T, Luo KX, et al. Peginterferon alfa-2a, lamivudine, and the combination for HBeAg-positive chronic hepatitis B. N Engl J Med. 2005; 352: 2682-2695.
44. Buster EHCJ, Flink HJ, Cakaloglu Y, et al. Sustained HBeAg and HBsAg loss after long-Term follow-up of HBeAg-positive patients treated with peginterferon a-2b. Gastroenterology. 2008; 135: 459-467.
45. Wong VW, Wong GL, Yan KK, et al. Durability of peginterferon alfa-2b treatment at 5 years in patients with hepatitis B e antigen-positive chronic hepatitis B. Hepatology. 2010; 51: 1945-1953.
46. Marcellin P, Lau GKK, Bonino F, et al. Peginterferon alfa-2a alone, lamivudine alone, and the two in combination in patients with HBeAg-negative chronic hepatitis B. N Engl J Med. 2004; 351: 1206-1217.
47. Marcellin P, Bonino F, Yurdaydin C, et al. Hepatitis B surface antigen levels: association with 5-year response to peginterferon alfa-2a in hepatitis B e-Antigen-negative patients. Hepatol Int. 2013; 7: 88-97.
48. Janssen HL, van Zonneveld M, Senturk H, et al. Pegylated interferon alfa-2b alone or in combination with lamivudine for HBeAg-positive chronic hepatitis B: a randomised trial. Lancet. 2005; 365: 123-129.
49. Flink HJ, van Zonneveld M, Hansen BE, et al. Treatment with peg-interferon a-2b for HBeAg-positive chronic hepatitis B: HBsAg loss is associated with HBV genotype. Am J Gastroenterol. 2006; 101: 297-303.
50. Buster EHCJ, Hansen BE, Lau GK, et al. Factors that predict response of patients with hepatitis B e antigen-positive chronic hepatitis B to peginterferon-Alfa. Gastroenterology. 2009; 137: 2002-2009.
51. Piratvisuth T, Marcellin P, Popescu M, et al. Hepatitis B surface antigen: association with sustained response to peginterferon alfa-2a in hepatitis B e antigen-positive patients. Hepatol Int. 2013; 7: 429-436.
52. Sonneveld MJ, Rijckborst V, Boucher CAB, et al. Prediction of sustained response to peginterferon alfa-2b for hepatitis B e antigen-positive chronic hepatitis B using on-Treatment hepatitis B surface antigen decline. Hepatology. 2010; 52: 1251-1257.
53. Fried MW, Piratvisuth T, Lau GK, et al. HBeAg and hepatitis B virus DNA as outcome predictors during therapy with peginterferon alfa-2a for HBeAg-positive chronic hepatitis B. Hepatology. 2008; 47: 428-434.
54. Brunetto MR, Moriconi F, Bonino F, et al. Hepatitis B virus surface antigen levels: a guide to sustained response to peginterferon alfa-2a in HBeAg-negative chronic hepatitis B. Hepatology. 2009; 49: 1141-1150.
55. Liaw YF, Kao JH, Piratvisuth T, et al. Asian-Pacific consensus statement on the management of chronic hepatitis B: a 2012 update. Hepatol Int. 2012; 6: 531-561.
56. European Association For The Study Of The Liver. EASL clinical practice guidelines: management of chronic hepatitis B virus infection. J Hepatol. 2012; 57: 167-185.
57. Lok AS, McMahon BJ. Chronic hepatitis B: update 2009. Hepatology. 2009; 50: 661-662.
58. Chang TT, Lai CL, Kew Yoon S, et al. Entecavir treatment for up to 5 years in patients with hepatitis B e antigen-positive chronic hepatitis B. Hepatology. 2010; 51: 422-430.
59. Gordon SC, Krastev Z, Horban A, et al. Efficacy of tenofovir disoproxil fumarate at 240 weeks in patients with chronic hepatitis B with high baseline viral load. Hepatology. 2013; 58: 505-513.
60. Marcellin P, Gane EJ, Tsai N, et al. Seven years of treatment with tenofovir DF for chronic hepatitis B virus infection is safe and well tolerated and associated with sustained virological, biochemical and serological responses with no detectable resistance. Hepatology. 2013; 58(suppl 1): 649A.
61. Lam YF, Seto WK, Fung J, et al. Continuous entecavir for treatment naïve Chinese chronic hepatitis B patients in the real world setting the seven year results. Hepatol Int. 2015; 9 (suppl 1): S204.
62. Gish RG, Chang TT, Lai CL, et al. Loss of HBsAg antigen during treatment with entecavir or lamivudine in nucleosidenaive HBeAg-positive patients with chronic hepatitis B. J Viral Hepat. 2010; 17: 16-22.
63. Schiff ER, Lee SS, Chao YC, et al. Long-Term treatment with entecavir induces reversal of advanced fibrosis or cirrhosis in patients with chronic hepatitis B. Clin Gastroenterol Hepatol. 2011; 9: 274-276.
64. Marcellin P, Gane E, Buti M, et al. Regression of cirrhosis during treatment with tenofovir disoproxil fumarate for chronic hepatitis B: a 5-year open-label follow-up study. Lancet. 2013; 381: 468-475.
65. Liaw YF, Sung JJ, Chow WC, et al. Lamivudine for patients with chronic hepatitis B and advanced liver disease. N Engl J Med. 2004; 351: 1521-1531.
66. Yuen MF, Seto WK, Chow DH, et al. Long-Term lamivudine therapy reduces the risk of long-Term complications of chronic hepatitis B infection even in patients without advanced disease. Antivir Ther. 2007; 12: 1295-1303.
67. Hosaka T, Suzuki F, Kobayashi M, et al. Long-Term entecavir treatment reduces hepatocellular carcinoma incidence in patients with hepatitis B virus infection. Hepatology. 2013; 58: 98-107.
68. Wong GL, Chan HL, Mak CW, et al. Entecavir treatment reduces hepatic events and deaths in chronic hepatitis B patients with liver cirrhosis. Hepatology. 2013; 58: 1537-1547.
69. Kim WR, Loomba R, Berg T, et al. HCC risk scores: application of the CU-HCC, GAG-HCC and PAGE-B scores to chronic hepatitis B (CHB) patients treated with tenofovir disoproxil fumarate (TDF). J Hepatol. 2015; 62: S561.
70. Lai CL, Shouval D, Lok AS, et al. Entecavir versus lamivudine for patients with HBeAg-negative chronic hepatitis B. N Engl J Med. 2006; 354: 1011-1020.
71. Chang TT, Gish RG, de Man R, et al A comparison of entecavir and lamivudine for HBeAg-positive chronic hepatitis B. N Engl J Med. 2006; 354: 1001-1010.
72. Pan CQ, Lee HM. Antiviral therapy for chronic hepatitis B in pregnancy. Semin Liver Dis. 2013; 33: 138-146.
73. Lee JM, Ahn SH, Kim HS, et al. Quantitative hepatitis B surface antigen and hepatitis B e antigen titers in prediction of treatment response to entecavir. Hepatology. 2011; 53: 1486-1493.
74. Zoulim F, Locarnini S. Hepatitis B virus resistance to nucleos(t)ide analogues. Gastroenterology. 2009; 137: 1593-1608.
75. Gish R, Jia JD, Locarnini S, et al. Selection of chronic hepatitis B therapy with high barrier to resistance. Lancet Infect Dis. 2012; 12: 341-353.
76. Lavocat F, Deny P, Pichoud C, et al. Similar evolution of hepatitis B virus quasispecies in patients with incomplete adefovir response receiving tenofovir/emtricitabine combination or tenofovir monotherapy. J Hepatol. 2013; 59: 684-695.
77. Reijnder JG, Deterding K, Petersen J, et al. Antiviral effect of entecavir in chronic hepatitis B: influence of prior exposure to nucleos(t)ide analogues. J Hepatol. 2010; 52: 493-500.
78. Ville S, Pichoud C, Billioud G, et al. Impact of hepatitis B virus rtA181V/T mutants on hepatitis B treatment failure. J Hepatol. 2008; 48: 747-755.
79. Si-Ahmed SN, Pradat P, Zoutendijk R, et al. Efficacy and tolerance of a combination of tenofovir disoproxil fumarate plus emtricitabine in patients with chronic hepatitis B: a European multicenter study. Antiviral Res. 2011; 92: 90-95.
80. Petersen J, Ratziu V, Buti M, et al. Entecavir plus tenofovir combination as rescue therapy in pre-Treated chronic hepatitis B patients: an international multicenter cohort study. J Hepatol. 2012; 56: 520-526.
81. Zoulim F, Locarnini S. Optimal management of chronic hepatitis B patients with treatment failure and antiviral drug resistance. Liver Int. 2013; 33(suppl 1): 116-124.
82. Yuan HJ, Wong DKH, Doutreloigne J, et al. Precore and core promoter mutations at the time of HBeAg seroclearance in Chinese patients with chronic hepatitis B. J Infection. 2007; 54: 497-503.
83. Lai CL, Yuen MF. The natural history and treatment of chronic hepatitis B: a critical evaluation of standard treatment criteria and end points. Ann Int Med. 2007; 147: 58-61.
84. Mitka M. FDA: increased HBV reactivation risk with ofatumumab or rituximab. JAMA. 2013; 310: 1664.
85. Yuen MF, Wong DK, Fung J, et al. HBsAg seroclearance in chronic hepatitis B in Asian patients: replicative level and risk of hepatocellular carcinoma. Gastroenterology. 2008; 135: 1192-1199.
86. Seto WK, Wong DK, Fung J, et al. Reduction of hepatitis B surface antigen levels and hepatitis B surface antigen seroclearance in chronic hepatitis B patients receiving 10 years of nucleoside analogue therapy. Hepatology. 2013; 58: 923-931.
87. Chang TT, Liaw YF, Wu SS, et al. Long-Term entecavir therapy results in the reversal of fibrosis/cirrhosis and continued histological improvement in patients with chronic hepatitis B. Hepatology. 2010; 52: 886-893.
88. Fung J, Lai CL, Tanaka Y, et al. The duration of lamivudine therapy for chronic hepatitis B: cessation versus continuation of treatment after HBeAg seroconversion. Am J Gastroenterol. 2009; 104: 1940-1946.
89. Seto WK, Hui AJ, Wong VW, et al. Treatment cessation of entecavir in Asian patients with hepatitis B e antigen negative chronic hepatitis B: a multicentre prospective study. Gut. 2015; 64: 667-672.
90. Lai CL, Yuen MF. Chronic hepatitis B-new goals, new treatment. N Engl J Med. 2008; 359: 2488-2491.
91. Wooddell CI, Rozema DB, Hossbach M, et al. Hepatocytetargeted RNAi therapeutics for the treatment of chronic hepatitis B virus infection. Mol Ther. 2013; 21: 973-985.
92. Yuen MF, Chan HLY, Given G, et al. Phase II, dose ranging study of ARC-520, a siRNA-based therapeutic, in patients with chronic hepatitis B virus infection. Hepatology. 2014; 60(suppl 1): 1280A.
93. Klumpp K, Crépin T. Capsid proteins of enveloped viruses as antiviral drug targets. Curr Opin Virol. 2014; 5: 63-71.
94. Nilsson J, Moss S, Coates N, et al. P1044 NVP018, a cyclophilin inhibitor for treatment of chronic HBV infection. J Hepatol. 2014; 60(suppl 1): S423.
95. Yuen MF, Lai CL. HBV research moves forward-receptors and reactivation. Nat Rev Gastroenterol Hepatol. 2015; 12: 70-72.
96. Lai CL, Wong DKH, Ip P, et al. Profound reduction of HBV covalently closed circular DNA with long-Term nucleoside/tide analogue therapy. Hepatology. 2014; 60(suppl 1): 1090A.