Large variations in risk of hepatocellular carcinoma and mortality in treatment Naïve hepatitis B patients: Systematic review with meta-analyses

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Thiele, Maja ^a   Gluud, Lise Lotte ^b   Fialla, Annette Dam ^a   Dahl, Emilie Kirstine ^a   Krag, Aleksander ^a  

^a ODENSE UNIVERSITY HOSPITAL   (Denmark)

^b Mental Health Services CPH   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER RISK; FOLLOW UP; HEPATITIS B; HEPATITIS C; HIGH RISK PATIENT; HUMAN; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; MIXED INFECTION; MORTALITY; OBSERVATIONAL STUDY; PROGNOSIS; REVIEW; RISK ASSESSMENT; RISK FACTOR; SYSTEMATIC REVIEW; TREATMENT PLANNING; ASIAN CONTINENTAL ANCESTRY GROUP; CARCINOMA, HEPATOCELLULAR; CAUCASIAN; COMPLICATION; INCIDENCE; LIVER NEOPLASMS; META ANALYSIS; RISK;

ASIAN CONTINENTAL ANCESTRY GROUP; CARCINOMA, HEPATOCELLULAR; COINFECTION; EUROPEAN CONTINENTAL ANCESTRY GROUP; HEPATITIS B, CHRONIC; HEPATITIS C; HUMANS; INCIDENCE; LIVER CIRRHOSIS; LIVER NEOPLASMS; RISK;

EID: 84907259430     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0107177     Document Type: Review

References (86)

1. WHO (2009) Position Paper on Hepatitis B Vaccines. WHO Weekly Epidemiological Report 84: 405-420.
2. Wong CR, Garcia RT, Trinh HN, Lam KD, Ha NB, et al. (2009) Adherence to screening for hepatocellular carcinoma among patients with cirrhosis or chronic hepatitis B in a community setting. Dig Dis Sci 54: 2712-2721.
3. Bruix J, Sherman M (2010) AASLD Practice Guideline. Management of Hepatocellular Carcinoma. Hepatology: 1-35.
4. Beasley RP, Lin CC, Hwang LY, Chien CS (1981) Hepatocellular Carcinoma and Hepatitis B Virus: A Prospective Study of 22 707 Men in Taiwan. The Lancet 318: 1129-1133.
5. Manno M, Cammà C, Schepis F, Bassi F, Gelmini R, et al. (2004) Natural history of chronic HBV carriers in northern Italy: Morbidity and mortality after 30 years. Gastroenterology 127: 756-763.
6. McMahon BJ, Holck P, Bulkow L, Snowball M (2001) Serologic and Clinical Outcomes of 1536 Alaska Natives Chronically Infected with Hepatitis B Virus. Annals of Internal Medicine 135: 759-768.
7. Fattovich G, Giustina G, Schalm SW, Hadziyannis S, Sanchez-Tapias J, et al. (1995) Occurrence of hepatocellular carcinoma and decompensation in western European patients with cirrhosis type B. The EUROHEP Study Group on Hepatitis B Virus and Cirrhosis. Hepatology 21: 77-82.
8. Chen CJ, Yang HI (2011) Natural history of chronic hepatitis B REVEALed. Journal of Gastroenterology and Hepatology 26: 628-638.
9. Fattovich G, Bortolotti F, Donato F (2008) Natural history of chronic hepatitis B: Special emphasis on disease progression and prognostic factors. Journal of Hepatology 48: 335-352.
10. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, et al. (2000) Metaanalysis of observational studies in epidemiology: a proposal for reporting. Metaanalysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 283: 2008-2012.
11. Higgins JP, Green S, editors (2011) Cochrane Handbook for Systematic Reviews of Interventions. Version 5.1.0 [updated March 2011]: The Cochrane Collaboration
12. Center for Evidence Based Medicine (2013) Critical Appraisal Tools. Available: http://www.cebm.net/index.aspx?o=1157.
13. Trinchet JC, Chaffaut C, Bourcier V, Degos F, Henrion J, et al. (2011) Ultrasonographic surveillance of hepatocellular carcinoma in cirrhosis: A randomized trial comparing 3- and 6-month periodicities. Hepatology 54: 1987-1997.
14. Wang JH, Chang KC, Kee KM, Chen PF, Yen YH, et al. (2013) Hepatocellular carcinoma surveillance at 4- vs. 12-month intervals for patients with chronic viral hepatitis: a randomized study in community. American Journal of Gastroenterology 108: 416-424.
15. Farci P, Roskams T, Chessa L, Peddis G, Mazzoleni AP, et al. (2004) Long-term benefit of interferon α therapy of chronic hepatitis D: regression of advanced hepatic fibrosis. Gastroenterology 126: 1740-1749.
16. Liaw YF, Sung JJY, Chow WC, Farrell G, Lee CZ, et al. (2004) Lamivudine for Patients with Chronic Hepatitis B and Advanced Liver Disease. New England Journal of Medicine 351: 1521-1531.
17. Mazzella G, Saracco G, Festi D, Rosina F, Marchetto S, et al. (1999) Long-term results with interferon therapy in chronic type B hepatitis: a prospective randomized trial. Am J Gastroenterol 94: 2246-2250.
18. EASL ATGo (1986) Steroids in chronic B-hepatitis. A randomized, doubleblind, multinational trial on the effect of low-dose, long-term treatment on survival. A trial group of the European Association for the Study of the Liver. Liver 6: 227-232.
19. Zavaglia C, Severini R, Tinelli C, Franzone JS, Airoldi A, et al. (2000) A randomized, controlled study of thymosin-alpha1 therapy in patients with anti- HBe, HBV-DNA-positive chronic hepatitis B. Dig Dis Sci 45: 690-696.
20. Benvegnù L, Chemello L, Noventa F, Fattovich G, Pontisso P, et al. (1998) Retrospective analysis of the effect of interferon therapy on the clinical outcome of patients with viral cirrhosis. Cancer 83: 901-909.
21. Benvegnù L, Gios M, Boccato S, Alberti A (2004) Natural history of compensated viral cirrhosis: a prospective study on the incidence and hierarchy of major complications. Gut 53: 744-749.
22. Borzio M, Bruno S, Roncalli M, Colloredo Mels G, Ramella G, et al. (1995) Liver cell dysplasia is a major risk factor for hepatocellular carcinoma in cirrhosis: A prospective study. Gastroenterology 108: 812-817.
23. Brunetto MR, Oliveri F, Coco B, Leandro G, Colombatto P, et al. (2002) Outcome of anti-HBe positive chronic hepatitis B in alpha-interferon treated and untreated patients: a long term cohort study. Journal of Hepatology 36: 263-270.
24. Chen YC, Chu CM, Yeh CT, Liaw YF (2007) Natural course following the onset of cirrhosis in patients with chronic hepatitis B: a long-term follow-up study. Hepatol Int 1: 267-273.
25. Colombo M, de Franchis R, Del Ninno E, Sangiovanni A, De Fazio C, et al. (1991) Hepatocellular Carcinoma in Italian Patients with Cirrhosis. New England Journal of Medicine 325: 675-680.
26. Cottone M, Turri M, Caltagirone M, Parisi P, Orlando A, et al. (1994) Screening for hepatocellular carcinoma in patients with Child's A cirrhosis: an 8- year prospective study by ultrasound and alphafetoprotein. Journal of Hepatology 21: 1029-1034.
27. de Franchis R, Meucci G, Vecchi M, Tatarella M, Colombo M, et al. (1993) The Natural History of Asymptomatic Hepatitis B Surface Antigen Carriers. Annals of Internal Medicine 118: 191.
28. Di Marco V, Iacono OL, Cammà C, Vaccaro A, Giunta M, et al. (1999) The long-term course of chronic hepatitis B. Hepatology 30: 257-264.
29. Dragosics B, Ferenci P, Hitchman E, Denk H (1987) Long-term follow-up study of asymptomatic HBsAg-positive voluntary blood donors in Austria: a clinical and histologic evaluation of 242 cases. Hepatology 7: 302-306.
30. Guptan RC, Thakur V, Sarin SK, Banerjee K, Khandekar P (1996) Frequency and clinical profile of precore and surface hepatitis B mutants in Asian-Indian patients with chronic liver disease. Am J Gastroenterol 91: 1312-1317.
31. Kim JH, Lee JH, Park SJ, Bae MH, Kim JH, et al. (2008) Factors associated with natural seroclearance of hepatitis B surface antigen and prognosis after seroclearance: a prospective follow-up study. Hepatogastroenterology 55: 578-581.
32. Liaw YF, Lin DY, Chen TJ, Chu CM (1989) Natural course after the development of cirrhosis in patients with chronic type B hepatitis: a prospective study. Liver 9: 235-241.
33. Lo KJ, Tong MJ, Chien MC, Tsai YT, Liaw YF, et al. (1982) The natural course of hepatitis B surface antigen-positive chronic active hepatitis in Taiwan. J Infect Dis 146: 205-210.
34. Lok AS, Lai CL (1989) alpha-Fetoprotein monitoring in Chinese patients with chronic hepatitis B virus infection: role in the early detection of hepatocellular carcinoma. Hepatology 9: 110-115.
35. Ma H, Wei L, Guo F, Zhu S, Sun Y, et al. (2008) Clinical features and survival in Chinese patients with hepatitis B e antigen-negative hepatitis B virus-related cirrhosis. Journal of Gastroenterology and Hepatology 23: 1250-1258.
36. Manzillo G, Piccinino F, Sagnelli E, Izzo CM, Pasquale G, et al. (1983) Treatment of HBsAg-positive chronic active hepatitis with corticosteroids and/ or azathioprine. A prospective study. Ric Clin Lab 13: 261-268.
37. Mazzella G, Accogli E, Sottili S, Festi D, Orsini M, et al. (1996) Alpha interferon treatment may prevent hepatocellular carcinoma in HCV-related liver cirrhosis. J Hepatol 24: 141-147.
38. Nakazawa T, Shibuya A, Takeuchi A, Shibata Y, Hidaka H, et al. (2011) Viral level is an indicator of long-term outcome of hepatitis B virus e antigen-negative carriers with persistently normal serum alanine aminotransferase levels. J Viral Hepat 18: e191-e199.
39. Oka H, Kurioka N, Kim K, Kanno T, Kuroki T, et al. (1990) Prospective study of early detection of hepatocellular carcinoma in patients with cirrhosis. Hepatology 12: 680-687.
40. Papatheodoridis GV, Manesis E, Hadziyannis SJ (2001) The long-term outcome of interferon-alpha treated and untreated patients with HBeAg-negative chronic hepatitis B. J Hepatol 34: 306-313.
41. Paul SB, Sreenivas V, Gulati MS, Madan K, Gupta AK, et al. (2007) Incidence of hepatocellular carcinoma among Indian patients with cirrhosis of liver: an experience from a tertiary care center in northern India. Indian J Gastroenterol 26: 274-278.
42. Sherman M, Peltekian KM, Lee C (1995) Screening for hepatocellular carcinoma in chronic carriers of hepatitis B virus: Incidence and prevalence of hepatocellular carcinoma in a North American urban population. Hepatology 22: 432-438.
43. Solmi L, Primerano AM, Gandolfi L (1996) Ultrasound follow-up of patients at risk for hepatocellular carcinoma: results of a prospective study on 360 cases. Am J Gastroenterol 91: 1189-1194.
44. Sulaiman HA (1989) The development of hepatocellular carcinoma from liver cirrhosis during a follow-up study. Gastroenterol Jpn 24: 567-572.
45. Tong MJ, Blatt LM, Kao VWC (2001) Surveillance for hepatocellular carcinoma in patients with chronic viral hepatitis in the United States of America. J Gastroenterol Hepatol 16: 553-559.
46. Tong MJ, Blatt LM, Tyson KB, Kao VWC (2006) Death from liver disease and development of hepatocellular carcinoma in patients with chronic hepatitis B virus infection: a prospective study. Gastroenterol Hepatol 2: 41-47.
47. Tsubota A, Arase Y, Ren F, Tanaka H, Ikeda K, et al. (2001) Genotype may correlate with liver carcinogenesis and tumor characteristics in cirrhotic patients infected with hepatitis B virus subtype adw. J Med Virol 65: 257-265.
48. Yu MW, Hsu FC, Sheen IS, Chu CM, Lin DY, et al. (1997) Prospective Study of Hepatocellular Carcinoma and Liver Cirrhosis in Asymptomatic Chronic Hepatitis B Virus Carriers. Am J Epidemiol 145: 1039-1047.
49. Yu MW, Shih WL, Lin CL, Liu CJ, Jian JW, et al. (2008) Body-mass index and progression of hepatitis B: a population-based cohort study in men. J Clin Oncol 26: 5576-5582.
50. Zacharakis GH, Koskinas J, Kotsiou S, Papoutselis M, Tzara F, et al. (2005) Natural history of chronic HBV infection: A cohort study with up to 12 years follow-up in North Greece (part of the Interreg I-II/EC-project). J Med Virol 77: 173-179.
51. Loomba R, Yang HI, Su J, Brenner D, Barrett-Connor E, et al. (2013) Synergism between obesity and alcohol in increasing the risk of hepatocellular carcinoma: a prospective cohort study. American Journal of Epidemiology 177: 333-342.
52. Chen CH, Hung CH, Lee CM, Hu TH, Wang JH, et al. (2007) Pre-S Deletion and Complex Mutations of Hepatitis B Virus Related to Advanced Liver Disease in HBeAg-Negative Patients. Gastroenterology 133: 1466-1474.
53. Chiaramonte M, Stroffolini T, Vian A, Stazi MA, Floreani A, et al. (1999) Rate of incidence of hepatocellular carcinoma in patients with compensated viral cirrhosis. Cancer 85: 2132-2137.
54. Chu CM, Liaw YF (2007) HBsAg seroclearance in asymptomatic carriers of high endemic areas: Appreciably high rates during a long-term follow-up. Hepatology 45: 1187-1192.
55. Fattovich G, Giustina G, Realdi G, Corrocher R, Schalm SW (1997) Long-term outcome of hepatitis B e antigen-positive patients with compensated cirrhosis treated with interferon alfa. Hepatology 26: 1338-1342.
56. Gheorghe L, Iacob S, Simionov I, Vadan R, Gheorghe C, et al. (2005) Natural history of compensated viral B and D cirrhosis. Rom J Gastroenterol 14: 329-335.
57. Ikeda K, Arase Y, Kobayashi M, Someya T, Saitoh S, et al. (2003) Consistently Low Hepatitis B Virus DNA Saves Patients from Hepatocellular Carcinogenesis in HBV-Related Cirrhosis. Intervirology 46: 96-104.
58. Ikeda K, Saitoh S, Suzuki Y, Kobayashi M, Tsubota A, et al. (1998) Interferon decreases hepatocellular carcinogenesis in patients with cirrhosis caused by the hepatitis B virus. Cancer 82: 827-835.
59. Ishikawa T, Ichida T, Yamagiwa S, Sugahara S, Uehara K, et al. (2001) High viral loads, serum alanine aminotransferase and gender are predictive factors for the development of hepatocellular carcinoma from viral compensated liver cirrhosis. Journal of Gastroenterology and Hepatology 16: 1274-1281.
60. Macias Rodriguez MA, Rendon Unceta P, Tejada Cabrera M, Infante Hernandez JM, Correro Aguilar F, et al. (2000) Risk factors for hepatocellular carcinoma in patients with liver cirrhosis. Rev Esp Enferm Dig 92: 458-469.
61. Maeshiro T, Arakaki S, Watanabe T, Aoyama H, Shiroma J, et al. (2007) Different natural courses of chronic hepatitis B with genotypes B and C after the fourth decade of life. World J Gastroenterol 13: 4560-4565.
62. Romeo R, Del Ninno E, Rumi M, Russo A, Sangiovanni A, et al. (2009) A 28- Year Study of the Course of Hepatitis Δ Infection: A Risk Factor for Cirrhosis and Hepatocellular Carcinoma. Gastroenterology 136: 1629-1638.
63. Sato A, Kato Y, Nakata K, Nakao K, Daikoku M, et al. (1996) Relationship between sustained elevation of serum alanine aminotransferase and progression from cirrhosis to hepatocellular carcinoma: comparison in patients with hepatitis B virus- and hepatitis C virus-associated cirrhosis. J Gastroenterol Hepatol 11: 944-948.
64. Tai DI, Lin SM, Sheen IS, Chu CM, Lin DY, et al. (2009) Long-term outcome of hepatitis B e antigen-negative hepatitis B surface antigen carriers in relation to changes of alanine aminotransferase levels over time. Hepatology 49: 1859-1867.
65. Tong MJ, Hsien C, Song JJ, Kao JH, Sun HE, et al. (2009) Factors associated with progression to hepatocellular carcinoma and to death from liver complications in patients with HBsAg-positive cirrhosis. Dig Dis Sci 54: 1337-1346.
66. Trerè D, Borzio M, Morabito A, Borzio F, Roncalli M, et al. (2003) Nucleolar hypertrophy correlates with hepatocellular carcinoma development in cirrhosis due to HBV infection. Hepatology 37: 72-78.
67. Yuen MF, Wong DKH, Sablon E, Tse E, Ng IOL, et al. (2004) HBsAg seroclearance in chronic hepatitis B in the Chinese: Virological, histological, and clinical aspects. Hepatology 39: 1694-1701.
68. Yuen MF, Yuan HJ, Wong DK, Yuen JC, Wong WM, et al. (2005) Prognostic determinants for chronic hepatitis B in Asians: therapeutic implications. Gut 54: 1610-1614.
69. Bolukbas C, Bolukbas FF, Kendir T, Akbayir N, Ince AT, et al. (2006) The effectiveness of lamivudine treatment in cirrhotic patients with HBV precore mutations: a prospective, open-label study. Dig Dis Sci 51: 1196-1202.
70. Das K, Das K, Datta S, Pal S, Hembram JR, et al. (2010) Course of disease and survival after onset of decompensation in hepatitis B virus-related cirrhosis. Liver International 30: 1033-1042.
71. IIHCSG (1998) Effect of interferon-α on progression of cirrhosis to hepatocellular carcinoma: a retrospective cohort study. The Lancet 351: 1535-1539.
72. Lin CC, Wu JC, Chang TT, Huang YH, Wang YJ, et al. (2001) Long-term evaluation of recombinant interferon α2b in the treatment of patients with hepatitis B e antigen-negative chronic hepatitis B in Taiwan. J Viral Hepat 8: 438-446.
73. Lin SM, Yu ML, Lee CM, Chien RN, Sheen IS, et al. (2007) Interferon therapy in HBeAg positive chronic hepatitis reduces progression to cirrhosis and hepatocellular carcinoma. J Hepatol 46: 45-52.
74. Manolakopoulos S, Karatapanis S, Elefsiniotis J, Mathou N, Vlachogiannakos J, et al. (2004) Clinical course of lamivudine monotherapy in patients with decompensated cirrhosis due to HBeAg negative chronic HBV infection. Am J Gastroenterol 99: 57-63.
75. Matsumoto A, Tanaka E, Rokuhara A, Kiyosawa K, Kumada H, et al. (2005) Efficacy of lamivudine for preventing hepatocellular carcinoma in chronic hepatitis B: A multicenter retrospective study of 2795 patients. Hepatology Research 32: 173-184.
76. Niederau C, Heintges T, Lange S, Goldmann G, Niederau CM, et al. (1996) Long-Term Follow-up of HBeAg-Positive Patients Treated with Interferon Alfa for Chronic Hepatitis B. New England Journal of Medicine 334: 1422-1427.
77. Sinn DH, Choi MS, Gwak GY, Paik YH, Lee JH, et al. (2013) Pre-s mutation is a significant risk factor for hepatocellular carcinoma development: a long-term retrospective cohort study. Digestive Diseases & Sciences 58: 751-758.
78. Tangkijvanich P, Thong-ngam D, Mahachai V, Kladchareon N, Suwangool P, et al. (2001) Long-term effect of interferon therapy on incidence of cirrhosis and hepatocellular carcinoma in Thai patients with chronic hepatitis B. Southeast Asian J Trop Med Public Health 32: 452-458.
79. Tseng TC, Liu CJ, Yang HC, Su TH, Wang CC, et al. (2012) High levels of hepatitis B surface antigen increase risk of hepatocellular carcinoma in patients with low HBV load. Gastroenterology 142: 1140-1149.e1143; quiz e1113-1144.
80. Yuen MF, Seto WK, Chow DH, Tsui K, Wong DK, et al. (2007) Long-term lamivudine therapy reduces the risk of long-term complications of chronic hepatitis B infection even in patients without advanced disease. Antivir Ther 12: 1295-1303.
81. Heleno B, Thomsen MF, Rodrigues DS, Jørgensen KJ, Brodersen J (2013) Quantification of harms in cancer screening trials: literature review. BMJ 347.
82. Aggestrup LM, Hestbech MS, Siersma V, Pedersen JH, Brodersen J (2012) Psychosocial consequences of allocation to lung cancer screening: a randomised controlled trial. BMJ Open 2.
83. Iloeje UH, Yang HI, Jen CL, Su J, Wang LY, et al. (2007) Risk and predictors of mortality associated with chronic hepatitis B infection. Clin Gastroenterol Hepatol 5: 921-931.
84. Ioannou GN, Splan MF, Weiss NS, McDonald GB, Beretta L, et al. (2007) Incidence and predictors of hepatocellular carcinoma in patients with cirrhosis. Clin Gastroenterol Hepatol 5: 938-945, 945 e931-934.
85. Bedogni G, Miglioli L, Masutti F, Ferri S, Castiglione A, et al. (2008) Natural Course of Chronic HCV and HBV Infection and Role of Alcohol in the General Population: The Dionysos Study. Am J Gastroenterol 103: 2248-2253.
86. Chao LT, Wu CF, Sung FY, Lin CL, Liu CJ, et al. (2011) Insulin, glucose and hepatocellular carcinoma risk in male hepatitis B carriers: results from 17-year follow-up of a population-based cohort. Carcinogenesis 32: 876-881.