Occult hepatitis B virus infection and hepatocellular carcinoma: A systematic review

Journal of Viral Hepatitis

Volumn 21, Issue 3, 2014, Pages 153-162

  Huang, Xiangyan ^a   Hollinger, F B ^b  

^a JINAN MILITARY GENERAL HOSPITAL   (China)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

hepatitis C; hepatocellular carcinoma; incidence; occult hepatitis B; systematic review

Indexed keywords

CANCER RISK; DISEASE ASSOCIATION; HEPATITIS B; HEPATITIS B VIRUS; HEPATITIS C; HUMAN; IMMUNOPATHOGENESIS; LIVER CELL CARCINOMA; MIXED INFECTION; OCCULT HEPATITIS B; PREVALENCE; PRIORITY JOURNAL; REVIEW; RISK FACTOR; SYSTEMATIC REVIEW;

HEPATITIS C; HEPATOCELLULAR CARCINOMA; INCIDENCE; OCCULT HEPATITIS B; SYSTEMATIC REVIEW;

ANIMALS; CARCINOMA, HEPATOCELLULAR; HEPATITIS B; HEPATITIS B VIRUS; HUMANS; INCIDENCE; LIVER NEOPLASMS; PREVALENCE; RISK FACTORS;

EID: 84892711842     PISSN: 13520504     EISSN: 13652893     Source Type: Journal    
DOI: 10.1111/jvh.12222     Document Type: Review

References (89)

1. Galy O, Chemin I, Le Roux E, et al,. Mutations in TP53 and CTNNB1 in relation to hepatitis B and C infections in hepatocellular carcinomas from Thailand. Hepat Res Treat 2011; 2011: 697162.
2. Lai CL, Ratziu V, Yuen MF, Poynard T,. Viral hepatitis B. Lancet 2003; 62: 2089-2094.
3. Okuda K,. Hepatocellular carcinoma. J Hepatol 2000; 32: 225-237.
4. Kew MC,. Epidemiology of hepatocellular carcinoma. Toxicology 2002; 181-182: 35-38.
5. Shi J, Zhu L, Liu S, Xie WF,. A meta-analysis of case-control studies on the combined effect of hepatitis B and C virus infections in causing hepatocellular carcinoma in China. Br J Cancer 2005; 92: 607-612.
6. Pollicino T, Saitta C, Raimondo G,. Hepatocellular carcinoma: the point of view of the hepatitis B virus. Carcinogenesis 2011; 32: 1122-1132.
7. Jeantet D, Chemin I, Mandrand B, et al,. Cloning and expression of surface antigens from occult chronic hepatitis B virus infections and their recognition by commercial detection assays. J Med Virol 2004; 73: 508-515.
8. Levicnik-Stezinar S,. Hepatitis B surface antigen escape mutant in a first time blood donor potentially missed by a routine screening assay. Clin Lab 2004; 50: 49-51.
9. Paparella C, De Rosa F, Longo R, et al,. Appearance of HBeAg in an occult persistent hepatitis B virus infection. Intervirology 2010; 53: 173-175.
10. Svicher V, Cento V, Bernassola M, et al,. Novel HBsAg markers tightly correlate with occult HBV infection and strongly affect HBsAg detection. Antiviral Res 2012; 93: 86-93.
11. Chamorro AJ, Casado JL, Bellido D, Moreno S,. Reactivation of hepatitis B in an HIV-infected patient with antibodies against hepatitis B core antigen as the only serological marker. Eur J Clin Microbiol Infect Dis 2005; 24: 492-494.
12. Hass M, Hannoun C, Kalinina T, Sommer G, Manegold C, Günther S,. Functional analysis of hepatitis B virus reactivating in hepatitis B surface antigen-negative individuals. Hepatology 2005; 42: 93-103.
13. Mrani S, Chemin I, Menouar K, et al,. Occult HBV infection may represent a major risk factor of non-response to antiviral therapy of chronic hepatitis C. J Med Virol 2007; 79: 1075-1081.
14. De Mitri MS, Cassini R, Bernardi M,. Hepatitis B virus-related hepatocarcinogenesis: molecular oncogenic potential of clear or occult infections. Eur J Cancer 2010; 46: 2178-2186.
15. Raimondo G, Caccamo G, Filomia R, Pollicino T,. Occult HBV infection. Semin Immunopathol 2013; 35: 39-52.
16. Chemin I, Zoulim F, Merle P, et al,. High incidence of hepatitis B infections among chronic hepatitis cases of unknown aetiology. J Hepatol 2001; 34: 447-454.
17. Liang TJ, Baruch Y, Ben-Porath E, et al,. Hepatitis B virus infection in patients with idiopathic liver disease. Hepatology 1991; 13: 1044-1051.
18. Chemin I, Trépo C,. Clinical impact of occult HBV infections. J Clin Virol 2005; 34: S15-21.
19. Sagnelli E, Imparato M, Coppola N, et al,. Diagnosis and clinical impact of occult hepatitis B infection in patients with biopsy proven chronic hepatitis C: a multicenter study. J Med Virol 2008; 80: 1547-1553.
20. Ohba K, Kubo S, Tamori A, et al,. Previous or occult hepatitis B virus infection in hepatitis B surface antigen-negative and anti-hepatitis C-negative patients with hepatocellular carcinoma. Surg Today 2004; 34: 842-848.
21. Ikeda K, Kobayashi M, Someya T, et al,. Occult hepatitis B virus infection increases hepatocellular carcinogenesis by eight times in patients with non-B, non-C liver cirrhosis: a cohort study. J Viral Hepat 2009; 16: 437-443.
22. Shire AM, Roberts LR,. Occult hepatitis B virus infection: bit player or role player? Hepatology 2011; 54: 760-763.
23. Raimondo G, Allain JP, Brunetto MR, et al,. Statements from the Taormina expert meeting on occult hepatitis B virus infection. J Hepatol 2008; 49: 652-657.
24. Hollinger FB, Sood G,. Occult hepatitis B virus infection: a covert operation. J Viral Hepat 2010; 17: 1-15.
25. Fierro NA, Roman S, Realpe M, Hernandez-Nazara Z, Zepeda-Carrillo EA, Panduro A,. Multiple cytokine expression profiles reveal immune-based differences in occult hepatitis B genotype H-infected Mexican Nahua patients. Mem Inst Oswaldo Cruz 2011; 106: 1007-1013.
26. Torbenson M, Thomas DL,. Occult hepatitis B. Lancet Infect Dis 2002; 2: 479-486.
27. Shi Y, Wu YH, Wu W, Zhang WJ, Yang J, Chen Z,. Association between occult hepatitis B infection and the risk of hepatocellular carcinoma: a meta-analysis. Liver Int 2012; 32: 231-240.
28. Allain JP, Candotti D,. Diagnostic algorithm for HBV safe transfusion. Blood Transfus 2009; 7: 174-182.
29. Stramer SL, Wend U, Candotti D, et al,. Nucleic acid testing to detect HBV infection in blood donors. N Engl J Med 2011; 364: 236-247.
30. Cacciola I, Pollicino T, Squadrito G, Cerenzia G, Orlando ME, Raimondo G,. Occult hepatitis B virus infection in patients with chronic hepatitis C liver disease. N Engl J Med 1999; 341: 22-26.
31. Brown SE, Howard CR, Steward MW, Ajdukiewicz AB, Whittle HC,. Hepatitis B surface antigen containing immune complexes occur in seronegative hepatocellular carcinoma patients. Clin Exp Immunol 1984; 55: 355-359.
32. Michalak TI, Mulrooney PM, Coffin CS,. Low doses of hepadnavirus induce infection of the lymphatic system that does not engage the liver. J Virol 2004; 78: 1730-1738.
33. Zerbini A, Pilli M, Boni C, et al,. The characteristics of the cell-mediated immune response identify different profiles of occult hepatitis B virus infection. Gastroenterology 2008; 134: 1470-1481.
34. Samal J, Kandpal M, Vivekanandan P,. Molecular mechanisms underlying occult hepatitis B virus infection. Clin Microbiol Rev 2012; 25: 142-163.
35. Shih CM, Lo SJ, Miyamura T, Chen SY, Lee YH,. Suppression of hepatitis B virus expression and replication by hepatitis C virus core protein in HuH-7 cells. J Virol 1993; 67: 5823-5832.
36. Chen SY, Kao CF, Chen CM, et al,. Mechanisms for inhibition of hepatitis B virus gene expression and treplication by hepatitis C virus core protein. J Biol Chem 2003; 278: 591-607.
37. Schüttler CG, Fiedler N, Schmidt K, Repp R, Gerlich WH, Schaefer S,. Suppression of hepatitis B virus enhancer 1 and 2 by hepatitis C virus core protein. J Hepatol 2002; 37: 855-862.
38. Zhu W, Wu C, Deng W, et al,. Inhibition of the HCV core protein on the immune response to HBV surface antigen and on HBV gene expression and replication in vivo. PLoS ONE 2012; 7: e45146.
39. Pollicino T, Raffa G, Costantino L, et al,. Molecular and functional analysis of occult hepatitis B virus isolates from patients with hepatocellular carcinoma. Hepatology 2007; 45: 277-285.
40. Bréchot C, Thiers V, Kremsdorf D, Nalpas B, Pol S, Paterlini-Bréchot P,. Persistent hepatitis B virus infection in subjects without hepatitis B surface antigen: clinically significant or purely "occult"? Hepatology 2001; 34: 194-203.
41. Castillo I, Rodríguez-Iñigo E, Lõpez-Alcorocho JM, Bartolomé J, Pardo M, Carreño V,. Comparative study on the clinical and virological characteristics among patients with single occult hepatitis B virus (HBV), single occult hepatitis C virus (HCV) and occult HBV and HCV dual infection. J Med Virol 2007; 79: 236-241.
42. Fang Y, Shang QL, Liu JY, et al,. Prevalence of occult hepatitis B virus infection among hepatopathy patients and healthy people in China. J Infect 2009; 58: 383-388.
43. Liedõ JL, Fernández C, Gutiérrez ML, Ocaña S,. Management of occult hepatitis B virus infection: an update for the clinician. World J Gastroenterol 2011; 17: 1563-1568.
44. Bréchot C,. Pathogenesis of hepatitis B virus-related hepatocellular carcinoma: old and new paradigms. Gastroenterology 2004; 127: S56-61.
45. Wong DK, Huang FY, Lai CL, et al,. Occult hepatitis B infection and HBV replicative activity in patients with cryptogenic cause of hepatocellular carcinoma. Hepatology 2011; 54: 829-836.
46. Shiota G, Oyama K, Udagawa A, et al,. Occult hepatitis B virus infection in HBs antigen-negative hepatocellular carcinoma in a Japanese population: involvement of HBx and p53. J Med Virol 2000; 62: 151-158.
47. Hassan ZK, Hafez MM, Mansor TM, Zekri AR,. Occult HBV infection among Egyptian hepatocellular carcinoma patients. Virol J 2011; 8: 90.
48. Momosaki S, Nakashima Y, Kojiro M, Tabor E,. HBsAg-negative hepatitis B virus infections in hepatitis C virus-associated hepatocellular carcinoma. J Viral Hepat 2005; 12: 325-329.
49. Yotsuyanagi H, Shintani Y, Moriya K, et al,. Virologic analysis of non-B, non-C hepatocellular carcinoma in Japan: frequent involvement of hepatitis B virus. J Infect Dis 2000; 181: 1920-1928.
50. Chen CH, Changchien CS, Lee CM, et al,. A study on sequence variations in pre-S/surface, X and enhancer II/core promoter/precore regions of occult hepatitis B virus in non-B, non-C hepatocellular carcinoma patients in Taiwan. Int J Cancer 2009; 125: 621-629.
51. Pollicino T, Squadrito G, Cerenzia G, et al,. Hepatitis B virus maintains its pro-oncogenic properties in the case of occult HBV infection. Gastroenterology 2004; 126: 102-110.
52. Kim SM, Lee KS, Park CJ, et al,. Prevalence of occult HBV infection among subjects with normal serum ALT levels in Korea. J Infect 2007; 54: 185-191.
53. Shih LN, Sheu JC, Wang JT, et al,. Serum hepatitis B virus DNA in healthy HBsAg-negative Chinese adults evaluated by polymerase chain reaction. J Med Virol 1990; 32: 257-260.
54. Fang ZL, Zhuang H, Wang XY, Ge XM, Harrison TJ,. Hepatitis B virus genotypes, phylogeny and occult infection in a region with a high incidence of hepatocellular carcinoma in China. World J Gastroenterol 2004; 10: 3264-3268.
55. Kew MC, Welschinger R, Viana R,. Occult hepatitis B virus infection in Southern African blacks with hepatocellular carcinoma. J Gastroenterol Hepatol 2008; 23: 1426-1430.
56. Tanaka T, Inoue K, Hayashi Y, et al,. Virological significance of low-level hepatitis B virus infection in patients with hepatitis C virus associated liver disease. J Med Virol 2004; 72: 223-229.
57. Branco F, Mattos AA, Coral GP, et al,. Occult hepatitis B virus infection in patients with chronic liver disease due to hepatitis C virus and hepatocellular carcinoma in Brazil. Arq Gastroenterol 2007; 44: 58-63.
58. Kao JH, Chen PJ, Lai MY, Chen DS,. Occult hepatitis B virus infection and clinical outcomes of patients with chronic hepatitis C. J Clin Microbiol 2002; 40: 4068-4071.
59. Alencar RS, Gomes MM, Sitnik R, et al,. Low occurrence of occult hepatitis B virus infection and high frequency of hepatitis C virus genotype 3 in hepatocellular carcinoma in Brazil. Braz J Med Biol Res 2008; 41: 235-240.
60. Tamori A, Hayashi T, Shinzaki M, et al,. Frequent detection of hepatitis B virus DNA in hepatocellular carcinoma of patients with sustained virologic response for hepatitis C virus. J Med Virol 2009; 81: 1009-1014.
61. Squadrito G, Pollicino T, Cacciola I, et al,. Occult hepatitis B virus infection is associated with the development of hepatocellular carcinoma in chronic hepatitis C patients. Cancer 2006; 106: 1326-1330.
62. Miura Y, Shibuya A, Adachi S, et al,. Occult hepatitis B virus infection as a risk factor for hepatocellular carcinoma in patients with chronic hepatitis C in whom viral eradication fails. Hepatol Res 2008; 38: 546-556.
63. Matsuoka S, Nirei K, Tamura A, et al,. Influence of occult hepatitis B virus coinfection on the incidence of fibrosis and hepatocellular carcinoma in chronic hepatitis C. Intervirology 2008; 51: 352-361.
64. Hasegawa I, Orito E, Tanaka Y, et al,. Impact of occult hepatitis B virus infection on efficacy and prognosis of interferon-alpha therapy for patients with chronic hepatitis C. Liver Int 2005; 25: 247-253.
65. Adachi S, Shibuya A, Miura Y, Takeuchi A, Nakazawa T, Saigenji K,. Impact of occult hepatitis B virus infection and prior hepatitis B virus infection on development of hepatocellular carcinoma in patients with liver cirrhosis due to hepatitis C virus. Scand J Gastroenterol 2008; 43: 849-856.
66. Obika M, Shinji T, Fujioka S,. Hepatitis B virus DNA in liver tissue and risk for hepatocarcinogenesis in patients with hepatitis C virus-related chronic liver disease. A prospective study. Intervirology 2008; 51: 59-68.
67. Shetty K, Hussain M, Nei L, Reddy KR, Lok AS,. Erratum: prevalence and significance of occult hepatitis B in a liver transplant population with chronic hepatitis C. Liver Transpl 2011; 17: 97.
68. Schirmacher P, Rogler CE, Dienes HP,. Current pathogenetic and molecular concepts in viral liver carcinogenesis. Virchows Arch B Cell Pathol Incl Mol Pathol 1993; 63: 71-89.
69. Murakami Y, Saigo K, Takashima H, et al,. Large scaled analysis of hepatitis B virus (HBV) DNA integration in HBV related hepatocellular carcinomas. Gut 2005; 54: 1162-1168.
70. Tamori A, Yamanishi Y, Kawashima S, et al,. Alteration of gene expression in human hepatocellular carcinoma with integrated hepatitis B virus DNA. Clin Cancer Res 2005; 11: 5821-5826.
71. Matsubara K, Tokino T,. Integration of hepatitis B virus DNA and its implications for hepatocarcinogenesis. Mol Biol Med 1990; 7: 243-260.
72. Chemin I, Zoulim F,. Hepatitis B virus induced hepatocellular carcinoma. Cancer Lett 2009; 286: 52-59.
73. Utsunomiya T, Shimada M,. Molecular characteristics of non-cancerous liver tissue in non-B non-C hepatocellular carcinoma. Hepatol Res 2011; 41: 711-721.
74. Keasler VV, Lerat H, Madden CR, et al,. Increased liver pathology in hepatitis C virus transgenic mice expressing the hepatitis B virus X protein. Virology 2006; 347: 466-475.
75. Said ZN,. An overview of occult hepatitis B virus infection. World J Gastroenterol 2011; 17: 1927-1938.
76. Matsuzaki Y, Chiba T, Hadama T, et al,. HBV genome integration and genetic instability in HBsAg-negative and anti-HCV-positive hepatocellular carcinoma in Japan. Cancer Lett 1997; 119: 53-61.
77. Tamori A, Nishiguchi S, Kubo S, et al,. HBV DNA integration and HBV-transcript expression in non-B, non-C hepatocellular carcinoma in Japan. J Med Virol 2003; 71: 492-498.
78. Gujar SA, Michalak TI,. Primary occult hepadnavirus infection induces virus-specific T-cell and aberrant cytokine responses in the absence of antiviral antibody reactivity in the woodchuck model of hepatitis B virus infection. J Virol 2009; 83: 3861-3876.
79. Weber B,. Diagnostic impact of the genetic variability of the hepatitis B virus surface antigen gene. J Med Virol 2006; 78: S59-65.
80. Osiowy C,. Detection of HBsAg mutants. J Med Virol 2006; 78: S48-51.
81. Huang X, Qin Y, Li W, et al,. Molecular analysis of the hepatitis B virus presurface and surface gene in patients from Eastern China with occult hepatitis B. J Med Virol 2013; 85: 979-986.
82. Zhang Q, Cao G,. Genotypes, mutations, and viral load of hepatitis B virus and the risk of hepatocellular carcinoma: HBV properties and hepatocarcinogenesis. Hepat Mon 2011; 11: 86-91.
83. Sinn DH, Choi MS, Gwak GY, et al,. Pre-S mutation is a significant risk factor for hepatocellular carcinoma development: a long-term retrospective cohort study. Dig Dis Sci 2013; 58: 751-758.
84. Yeung P, Wong DK, Lai CL, Fung J, Seto WK, Yuen MF,. Association of hepatitis B virus pre-S deletions with the development of hepatocellular carcinoma in chronic hepatitis B. J Infect Dis 2011; 203: 646-654.
85. Lee SA, Kim K, Kim H, Kim BJ,. Nucleotide change of codon 182 in the surface gene of hepatitis B virus genotype C leading to truncated surface protein is associated with progression of liver diseases. J Hepatol 2012; 56: 63-69.
86. Liu S, Xie J, Yin J, et al,. A matched case-control study of hepatitis B virus mutations in the preS and core promoter regions associated independently with hepatocellular carcinoma. J Med Virol 2011; 83: 45-53.
87. Kao JH, Liu CJ, Jow GM, Chen PJ, Chen DS, Chen BF,. Fine mapping of hepatitis B virus pre-S deletion and its association with hepatocellular carcinoma. Liver Int 2012; 32: 1373-1381.
88. Kaur P, Paliwal A, Durantel D, et al,. DNA methylation of hepatitis B virus (HBV) genome associated with the development of hepatocellular carcinoma and occult HBV infection. J Infect Dis 2010; 202: 700-704.
89. Levrero M, Pollicino T, Petersen J, Belloni L, Raimondo G, Dandri M,. Control of cccDNA function in hepatitis B virus infection. J Hepatol 2009; 51: 581-592.