Natural history of chronic hepatitis B virus infection: What we knew in 1981 and what we know in 2005

Hepatology

Volumn 43, Issue 2 SUPPL. 1, 2006, Pages

  Yim, Hyung Joon ^a   Lok, Anna Suk Fong ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADEFOVIR; ANTIVIRUS AGENT; ENTECAVIR; HEPATITIS B(E) ANTIGEN; INTERFERON; LAMIVUDINE; PLACEBO;

CHRONIC HEPATITIS; CLINICAL TRIAL; DISEASE COURSE; DNA DETERMINATION; GENOME ANALYSIS; GENOTYPE; HEPATITIS B VIRUS; HETEROZYGOTE; HUMAN; IMMUNOLOGICAL TOLERANCE; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LIVER DISEASE; PRIORITY JOURNAL; REVIEW; SEROCONVERSION; UNSPECIFIED SIDE EFFECT; VIRUS CARRIER; VIRUS REPLICATION;

HEPATITIS B; HEPATITIS B E ANTIGENS; HEPATITIS B, CHRONIC; HUMANS; LIVER CIRRHOSIS;

EID: 33644506166     PISSN: 02709139     EISSN: None     Source Type: Journal    
DOI: 10.1002/hep.20956     Document Type: Review

References (97)

1. Redeker AG. Viral hepatitis: clinical aspects. Am J Med Sci 1975;270:9-16.
2. Hoofnagle JH. Type B hepatitis: virology, serology and clinical course. Semin Liver Dis 1981;1:7-14.
3. Okada K, Kamiyama I, Inomata M, Imai M, Miyakawa Y. e antigen and anti-e in the serum of asymptomatic carrier mothers as indicators of positive and negative transmission of hepatitis B virus to their infants. N Engl J Med 1976;294:746-749.
4. Alberti A, Pontisso P, Realdi G. Changes in hepatitis B virus DNA-polymerase activity in patients with chronic infection. J Med Virol 1981;8:223-229.
5. Bonino F, Hoyer B, Nelson J, Engle R, Verme G, Gerin J. Hepatitis B virus DNA in the sera of HBsAg carriers: a marker of active hepatitis B virus replication in the liver. HEPATOLOGY 1981;1:386-391.
6. Brechot C, Hadchouel M, Scotto J, Degos F, Charnay P, Trepo C, et al. Detection of hepatitis B virus DNA in liver and serum: a direct appraisal of the chronic carrier state. Lancet 1981;318:765-768.
7. Andres LL, Sawhney VK, Scullard GH, Smith JL, Merigan TC, Robinson WS, et al. Dane particle DNA polymerase and HBeAg: impact on clinical, laboratory, and histologic findings in hepatitis B-associated chronic liver disease. HEPATOLOGY 1981;1:583-585.
8. Hoofnagle JH, Dusheiko GM, Seeff LB, Jones EA, Waggoner JG, Bales ZB. Seroconversion from hepatitis B e antigen to antibody in chronic type B hepatitis. Ann Intern Med 1981;94:744-748.
9. Realdi G, Alberti A, Rugge M, Bortolotti F, Rigoli AM, Tremolada F, et al. Seroconversion from hepatitis B e antigen to anti-HBe in chronic hepatitis B virus infection. Gastroenterology 1980;79:195-199.
10. Sampliner RE, Hamilton FA, Iseri OA, Tabor E, Boitnott J. The liver histology and frequency of clearance of the hepatitis B surface antigen (HBsAg) in chronic carriers. Am J Med Sci 1979;277:17-22.
11. Chen DS, Sung JL. Hepatitis B virus infection and chronic liver disease in Taiwan. Acta Hepatogastroenterol 1978;25:423-430.
12. Obata H, Hayashi N, Motoike Y, Hisamitsu T, Okuda H, Kobayashi S, et al. A prospective study on the development of hepatocellular carcinoma from liver cirrhosis with persistent hepatitis B virus infection. Int J Cancer 1980;25:741-747.
13. Rizzetto M, Shih JW, Gocke DJ, Purcell RH, Verme G, Gerin JL. Incidence and significance of antibodies to delta antigen in hepatitis B virus infection. Lancet 1979;314:986-990.
14. Sherlock S, Fox RA, Niazi SP, Scheuer PJ. Chronic liver disease and primary liver-cell cancer with hepatitis-associated (Australia) antigen in serum. Lancet 1970;295:1243-1247.
15. Beasley RP, Hwang LY, Lin CC, Chien CS. Hepatocellular carcinoma and hepatitis B virus. A prospective study of 22 707 men in Taiwan. Lancet 1981;318:1129-1133.
16. Heyward WL, Lanier AP, Bender TR, Hardison HH, Dohan PH, McMahon BJ, et al. Primary hepatocellular carcinoma in Alaskan natives, 1969-1979. Int J Cancer 1981;28:47-50.
17. Brechot C, Pourcel C, Louise A, Rain B, Tiollais P. Presence of integrated hepatitis B virus DNA sequences in cellular DNA of human hepatocellular carcinoma. Nature 1980;286:533-535.
18. Shafritz DA, Shouval D, Sherman HI, Hadziyannis SJ, Kew MC. Integration of hepatitis B virus DNA into the genome of liver cells in chronic liver disease and hepatocellular carcinoma. Studies in percutaneous liver biopsies and post-mortem tissue specimens. N Engl J Med 1981;305:1067-1073.
19. Lutwick LI. Relation between aflatoxin, hepatitis-B virus, and hepatocellular carcinoma. Lancet 1979;313:755-757.
20. Pawlotsky JM. Hepatitis B virus (HBV) DNA assays (methods and practical use) and viral kinetics. J Hepatol 2003;39(Suppl. 1):S31-35.
21. Locarnini S. Molecular virology of hepatitis B virus. Semin Liver Dis 2004;24 (Suppl. 1):3-10.
22. Rehermann B. Immune responses in hepatitis B virus infection. Semin Liver Dis 2003;23:21-38.
23. Summers J, Mason WS. Replication of the genome of a hepatitis B-like virus by reverse transcription of an RNA intermediate. Cell 1982;29:403-415.
24. Fung SK, Lok AS. Hepatitis B virus genotypes: do they play a role in the outcome of HBV infection? HEPATOLOGY 2004;40:790-792.
25. Stoop JN, van der Molen RG, Baan CC, van der Laan LJ, Kuipers EJ, Kusters JG, et al. Regulatory T cells contribute to the impaired immune response in patients with chronic hepatitis B virus infection. HEPATOLOGY 2005;41:771-778.
26. Penna A, Chisari FV, Bertoletti A, Missale G, Fowler P, Giuberti T, et al. Cytotoxic T lymphocytes recognize an HLA-A2-restricted epitope within the hepatitis B virus nucleocapsid antigen. J Exp Med 1991;174:1565-1570.
27. Liaw YF, Yang SS, Chen TJ, Chu CM. Acute exacerbation in hepatitis B e antigen positive chronic type B hepatitis. A clinicopathological study. J Hepatol 1985;1:227-233.
28. Davis GL, Hoofnagle JH. Reactivation of chronic type B hepatitis presenting as acute viral hepatitis. Ann Intern Med 1985;102:762-765.
29. Lok AS, Lai CL. Acute exacerbations in Chinese patients with chronic hepatitis B virus (HBV) infection. Incidence, predisposing factors and etiology. J Hepatol 1990;10:29-34.
30. Tassopoulos NC, Papaevangelou GJ, Sjogren MH, Roumeliotou-Karayannis A, Gerin JL, Purcell RH. Natural history of acute hepatitis B surface antigen-positive hepatitis in Greek adults. Gastroenterology 1987;92:1844-1850.
31. Beasley RP, Trepo C, Stevens CE, Szmuness W. The e antigen and vertical transmission of hepatitis B surface antigen. Am J Epidemiol 1977;105:94-98.
32. Beasley RP, Hwang LY, Lin CC, Leu ML, Stevens CE, Szmuness W, et al. Incidence of hepatitis B virus infections in preschool children in Taiwan. J Infect Dis 1982;146:198-204.
33. Blackberg J, Kidd-Ljunggren K. Occult hepatitis B virus after acute self-limited infection persisting for 30 years without sequence variation. J Hepatol 2000;33:992-997.
34. Rehermann B, Ferrari C, Pasquinelli C, Chisari FV. The hepatitis B virus persists for decades after patients' recovery from acute viral hepatitis despite active maintenance of a cytotoxic T-lymphocyte response. Nat Med 1996;2:1104-1108.
35. Shimizu D, Nomura K, Matsumoto Y, Ueda K, Yamaguchi K, Minami M, et al. Hepatitis B virus reactivation in a patient undergoing steroid-free chemotherapy. World J Gastroenterol 2004;10:2301-2302.
36. Lok AS, Liang RH, Chiu EK, Wong KL, Chan TK, Todd D. Reactivation of hepatitis B virus replication in patients receiving cytotoxic therapy: report of a prospective study. Gastroenterology 1991;100:182-188.
37. Yuki N, Nagaoka T, Yamashiro M, Mochizuki K, Kaneko A, Yamamoto K, et al. Long-term histologic and virologic outcomes of acute self-limited hepatitis B. HEPATOLOGY 2003;37:1172-1179.
38. Brunetto MR, Stemler M, Schodel F, Will H, Orrobrelli A, Rizzetto M, et al. Identification of HBV variants which cannot produce precore derived HBeAg and may be responsible for severe hepatitis. Ital J Gastroenterol 1989;21:151-154.
39. Carman WF, Jacyna MR, Hadziyannis S, Karayiannis P, McGarvey MJ, Makris A, et al. Mutation preventing formation of hepatitis B e antigen in patients with chronic hepatitis B infection. Lancet 1989;334:588-591.
40. Okamoto H, Tsuda F, Akahane Y, Sugai Y, Yoshiba M, Moriyama K, et al. Hepatitis B virus with mutations in the core promoter for an e antigen-negative phenotype in carriers with antibody to e antigen. J Virol 1994;68:8102-8110.
41. Chu CM, Karayiannis P, Fowler MJ, Monjardino J, Liaw YF, Thomas HC. Natural history of chronic hepatitis B virus infection in Taiwan: studies of hepatitis B virus DNA in serum. HEPATOLOGY 1985;5:431-434.
42. Chu CM, Hung SJ, Lin J, Tai DI, Liaw YF. Natural history of hepatitis B c antigen to antibody seroconversion in patients with normal serum aminotransferase levels. Am J Med 2004;116:829-834.
43. Tsai SL, Chen PJ, Lai MY, Yang PM, Sung JL, Huang JH, et al. Acute exacerbations 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.
44. Chu CM, Liaw YF. Intrahepatic distribution of hepatitis B surface and core antigens in chronic hepatitis B virus infection. Hepatocyte with cytoplasmic/membranous hepatitis B core antigen as a possible target for immune hepatocytolysis. Gastroenterology 1987;92:220-225.
45. Liaw YF, Chu CM, Su IJ, Huang MJ, Lin DY, Chang-Chien CS. Clinical and histological events preceding hepatitis B e antigen seroconversion in chronic type B hepatitis. Gastroenterology 1983;84:216-219.
46. Sheen IS, Liaw YF, Tai DI, Chu CM. Hepatic decompensation associated with hepatitis B e antigen clearance in chronic type B hepatitis. Gastroenterology 1985;89:732-735.
47. McMahon BJ, Holck P, Bulkow L, Snowball M. Serologic and clinical outcomes of 1536 Alaska Natives chronically infected with hepatitis B virus. Ann Intern Med 2001;135:759-768.
48. Liaw YF, Tai DI, Chu CM, Chen TJ. The developmenr of cirrhosis in patients with chronic type B hepatitis: a prospective study. HEPATOLOGY 1988;8:493-496.
49. Yuen MF, Yuan HJ, Hui CK, Wong DK, Wong WM, Chan AO, et al. A large population study of spontaneous HBeAg seroconversion and acute exacerbation of chronic hepatitis B infection: implications for antiviral therapy. Gut 2003;52:416-419.
50. Liaw YF. Hepatitis flares and hepatitis B e antigen seroconversion: implication in anti-hepatitis B virus therapy. J Gastroenterol Hepatol 2003;18:246-252.
51. Kao JH, Chen PJ, Lai MY, Chen DS. Hepatitis B virus genotypes and spontaneous hepatitis B e antigen seroconversion in Taiwanese hepatitis B carriers. J Med Virol 2004;72:363-369.
52. Chu CJ, Hussain M, Lok AS. Hepatitis B virus genotype B is associated with earlier HBeAg seroconversion compared with hepatitis B virus genotype C. Gastroenterology 2002;122:1756-1762.
53. Manno M, Camma C, Schepis F, Bassi F, Gelmini R, Giannini F, et al. Natural history of chronic HBV carriers in northern Italy: morbidity and mortality after 30 years. Gastroenterology 2004;127:756-763.
54. Lok AS, Lai CL, Wu PC, Leung EK, Lam TS. Spontaneous hepatitis B e antigen to antibody seroconversion and reversion in Chinese patients with chronic hepatitis B virus infection. Gastroenterology 1987;92:1839-1843.
55. Hsu YS, Chien RN, Yeh CT, Sheen IS, Chiou HY, Chu CM, et al. Long-term outcome after spontaneous HBeAg seroconversion in patients with chronic hepatitis B. HEPATOLOGY 2002;35:1522-1527.
56. Hadziyannis SJ, Vassilopoulos D. Hepatitis B e antigen-negative chronic hepatitis B. HEPATOLOGY 2001;34:617-624.
57. Brunetto MR, Oliveri F, Coco B, Leandro G, Colombatto P, Gorin JM, et al. Outcome of anti-HBe positive chronic hepatitis B in alpha-interferon treated and untreated patients: a long term cohort study. J Hepatol 2002;36:263-270.
58. Chu CJ, Hussain M, Lok AS. Quantitative serum HBV DNA levels during different stages of chronic hepatitis B infection. HEPATOLOGY 2002;36:1408-1415.
59. Funk ML, Rosenberg DM, Lok AS. World-wide epidemiology of HBeAg-negative chronic hepatitis B and associated precore and core promoter variants. J Viral Hepatol 2002;9:52-61.
60. Chu CJ, Keeffe EB, Han SH, Perrillo RP, Min AD, Soldevila-Pico C, et al. U.S. HBV Epidemiology Study Group. Prevalence of HBV precore/core promoter variants in the United States. HEPATOLOGY 2003;38:619-628.
61. Chen YC, Sheen IS, Chu CM, Liaw YF. Prognosis following spontaneous HBsAg seroclearance in chronic hepatitis B patients with or without concurrent infection. Gastroenterology 2002;123:1084-1089.
62. Huo TI, Wu JC, Lee PC, Chau GY, Lui WY, Tsay SH, et al. Seroclearance of hepatitis B surface antigen in chronic carriers does not necessarily imply a good prognosis. HEPATOLOGY 1998;28:231-236.
63. Fattovich G, Brollo L, Alberti A, Pontisso P, Giustina G, Realdi G. Long-term follow-up of anti-HBe-positive chronic active hepatitis B. HEPATOLOGY 1988;8:1651-1654.
64. Brunetto MR, Oliveri F, Rocca G, Criscuolo D, Chiaberge E, Capalbo M, et al. Natural course and response to interferon of chronic hepatitis B accompanied by antibody to hepatitis B e antigen. HEPATOLOGY 1989;10:198-202.
65. Fattovich G. Natural history and prognosis of hepatitis B. Semin Liver Dis 2003;23:47-58.
66. Ohnishi K, Iida S, Iwama S, Goto N, Nomura F, Takashi M, et al. The effect of chronic habitual alcohol intake on the development of liver cirrhosis and hepatocellular carcinoma: relation to hepatitis B surface antigen carriage. Cancer 1982;49:672-677.
67. Liaw YF, Chen YC, Sheen IS, Chien RN, Yeh CT, Chu CM. Impact of acute hepatitis C virus superinfection in patients with chronic hepatitis B virus infection. Gastroenterology 2004;126:1024-1029.
68. Thio CL, Seaberg EC, Skolasky R Jr, Phair J, Visscher B, Munoz A, et al. Multicenter AIDS Cohort Study. HIV-1, hepatitis B virus, and risk of liver-related mortality in the Multicenter Cohort Study (MACS). Lancet 2002;360:1921-1926.
69. Iloeje UH, Yang HI, Su J, Jen CL, Kuo E, You SL, et al. Viral load not serum ALT is the primary predictor of progression to cirrhosis in persons chronically infected with HBV: results from a long-term prospective study. J Hepatol 2005;42 Suppl:S180.
70. Kao JH, Chen PJ, Lai MY, Chen DS. Hepatitis B genotypes correlate with clinical outcomes in patients with chronic hepatitis B. Gastroenterology 2000;118:554-559.
71. Sumi H, Yokosuka O, Seki N, Arai M, Imazeki F, Kurihara T, et al. Influence of hepatitis B virus genotypes on the progression of chronic type B liver disease. HEPATOLOGY 2003;37:19-26.
72. Orito E, Mizokami M, Sakugawa H, Michitaka K, Ishikawa K, Ichida T, et al. A case-control study for clinical and molecular biological differences between hepatitis B viruses of genotypes B and C. Japan HBV Genotype Research Group. HEPATOLOGY 2001;33:218-223.
73. de Jongh FE, Janssen HL, de Man RA, Hop WC, Schalm SW, van Blankenstein M. Survival and prognostic indicators in hepatitis B surface antigen-positive cirrhosis of the liver. Gastroenterology 1992;103:1630-1635.
74. Fattovich G, Pantalena M, Zagni I, Realdi G, Schalm SW, Christensen E. European Concerted Action on Viral Hepatitis (EUROHEP). Effect of hepatitis B and C virus infections on the natural history of compensated cirrhosis: a cohort study of 297 patients. Am J Gastroenterol 2002;97:2886-2895.
75. Tsubota A, Arase Y, Ren F, Tanaka H, Ikeda K, Kumada H. Genotype may correlate with liver carcinogenesis and tumor characteristics in cirrhotic patients infected with hepatitis B virus subtype adw. J Med Virol 2001;65:257-265.
76. Kato Y, Nakata K, Omagari K, Furukawa R, Kusumoto Y, Mori I, et al. Risk of hepatocellular carcinoma in patients with cirrhosis in Japan: analysis of infectious hepatitis viruses. Cancer 1994;74:2234-2238.
77. Benvegnu L, Gios M, Boccato S, Alberti A. Natural history of compensated viral cirrhosis: a prospective study on the incidence and hierarchy of major complications. Gut 2004;53:744-749.
78. Fattovich G, Stroffolini T, Zagni I, Donato F. Hepatocellular carcinoma in cirrhosis: incidence and risk factors. Gastroenterology 2004;127 (Suppl 1):S35-S50.
79. Yu MW, Chang HC, Liaw YF, Lin SM, Lee SD, Liu CJ, et al. Familial risk of hepatocellular carcinoma among chronic hepatitis B carriers and their relatives. J Natl Cancer Inst 2000;92:1159-1164.
80. Donato F, Tagger A, Gelatti U, Parrinello G, Boffetta P, Albertini A, et al. Alcohol and hepatocellular carcinoma: the effect of lifetime intake and hepatitis virus infections in men and women. Am J Epidemiol 2002;155:323-331.
81. Yang HI, Lu SN, Liaw YF, You SL, Sun CA, Wang LY, et al. Taiwan Community-Based Cancer Screening Project Group. Hepatitis B e antigen and the risk of hepatocellular carcinoma. N Engl J Med 2002;347:168-174.
82. Yu MW, Yeh SH, Chen PJ, Liaw YF, Lin CL, Liu CJ, et al. Hepatitis B virus genotype and DNA level and hepatocellular carcinoma: a prospective study in men. J Natl Cancer Inst 2005;97:265-272.
83. Tang B, Kruger WD, Chen G, Shen F, Lin WY, Mboup S, et al. Hepatitis B viremia is associated with increased risk of hepatocellular carcinoma in chronic carriers. J Med Virol 2004;72:35-40.
84. Baptista M, Kramvis A, Kew MC. High prevalence of 1762(T) 1764(A) mutations in the basic core promoter of hepatitis B virus isolated from black Africans with hepatocellular carcinoma compared with asymptomatic carriers. HEPATOLOGY 1999;29:946-953.
85. Kao JH, Chen PJ, Lai MY, Chen DS. Basal core promoter mutations of hepatitis B virus increase the risk of hepatocellular carcinoma in hepatitis B carriers. Gastroenterology 2003;124:327-334.
86. Yuan JM, Govindarajan S, Arakawa K, Yu MC. Synergism of alcohol, diabetes, and viral hepatitis on the risk of hepatocellular carcinoma in blacks and whites in the U.S. Cancer 2004;101:1009-1017.
87. Zheng Y, Li J, Ou JH. Regulation of hepatitis B virus core promoter by transcription factors HNF1 and HNF4 and the viral X protein. J Virol 2004;78:6908-6914.
88. Caselmann WH. Transactivation of cellular gene expression by hepatitis B viral proteins: a possible molecular mechanism of hepatocarcinogenesis. J Hepatol 1995;22(Suppl 1):S34-S37.
89. Yuen MF, Hui CK, Cheng CC, Wu CH, Lai YP, Lai CL. Long-term follow-up of interferon alfa treatment in Chinese patients with chronic hepatitis B infection: the effect on hepatitis B e antigen seroconversion and the development of cirrhosis-related complications. HEPATOLOGY 2001;34:139-145.
90. Craxi A, Di Bona D, Camma C. Interferon-alpha for HBeAg-positive chronic hepatitis B. J Hepatol 2003;39(Suppl 1):S99-S105.
91. Lin SM, Sheen IS, Chien RN, Chu CM, Liaw YF. Long-term beneficial effect of interferon therapy in patients with chronic hepatitis B virus infection. HEPATOLOGY 1999;29:971-975.
92. Dienstag JL, Goldin RD, Heathcote EJ, Hann HW, Woessner M, Stephenson SL, et al. Histological outcome during long-term lamivudine therapy. Gastroenterology 2003;124:105-117.
93. Papatheodoridis GV, Dimou E, Dimakopoulos K, Manolakopoulos S, Rapti I, Kitis G, et al. Outcome of hepatitis B e antigen-negative chronic hepatitis B on long-term nucleos(t)ide analog therapy starting with lamivudine. HEPATOLOGY 2005;42:121-129.
94. Rizzetto M, Tassopoulos NC, Goldin RD, Esteban R, Santantonio T, Heathcote EJ, et al. Extended lamivudine treatment in patients with HBeAg-negative chronic hepatitis B. J Hepatol 2005;42:173-179.
95. Liaw YF, Sung JJ, Chow WC, Farrell G, Lee CZ, Yuen H, et al. Cirrhosis Asian Lamivudine Multicentre Study Group. Lamivudine for patients with chronic hepatitis B and advanced liver disease. N Engl J Med 2004;351:1521-1531.
96. Marcellin P, Chang TT, Lim SG, Tong MJ, Sievert W, Shiffman ML, et al. Adefovir Dipivoxil 437 Study Group. Adefovir dipivoxil for the treatment of hepatitis B e antigen-positive chronic hepatitis B. N Engl J Med 2003;348:808-816.
97. Lai CL, Rosmawati M, Lao J, Van Vlierberghe H, Anderson FH, Thomas N, et al. Entecavir is superior to lamivudine in reducing hepatitis B virus DNA in patients with chronic hepatitis B infection. Gastroenterology 2002;123:1831-1838.