Resolved Hepatitis B: Achieved or Imaginary Wellbeing?
https://doi.org/10.22416/1382-4376-2021-31-1-7-19
Abstract
Aim. Assessment of the clinical impact of previous hepatitis B infection (PHB).
Key points. PHB is characterized by the presence of viral DNA in the organism (including intrahepatic cccDNA and integrated DNA). Possible virus persistence in the PHB patient's hepatocytes potentiates the agent transmission risk via haemotransfusion, organ transplantation and haemodialysis. Occult HBV infection in PHB individuals can reactivate at background immunosuppressive or chemotherapies. PHB with chronic liver diseases of various aetiology significantly rises the risk of cirrhosis and hepatic cancer. The PHB association with autoimmune liver diseases and extrahepatic gastrointestinal cancer needs a careful research to confirm the possible involvement of hepatitis B virus in morbid genesis.
Conclusion. No clinical signs of acute or chronic disease, HBsAg clearance and negative viral DNA load in blood of PHB individuals do not necessarily imply a complete disease eradication.
PHB elicitation improves accuracy of the overall prognosis, reduces the virus transmission risk and prevents the reactivation of HBV infection.
About the Author
S. N. BatskikhRussian Federation
Sergey N. Batskikh — Cand. Sci. (Med.), Senior Researcher, Department of Hepatology, Loginov Moscow Clinical Scientific Center.
111123, Moscow, Entuziastov highway, 86.
References
1. World Health Organization. Global Hepatitis Report, 2017. WHO: Geneve, Switzerland, 2017.
2. World Health Organization. Prevention and Control of Viral Hepatitis Infection: Framework for Global Action. WHO: Geneve, Switzerland, 2012. Available https://www.who.int/hepatitis/publications/Framework/en/ (accessed on 06 June 2020).
3. Terrault N.A., Lok A.S.F., McMahon B.J., Chang K.M., Hwang J.P., Jonas M.M., et al. Update on prevention, diagnosis, and treatment of chronic hepatitis B: AASLD 2018 hepatitis B guidance. Hepatology. 2018;67(4):1560— 99. DOI:10.1002/hep.29800
4. Hollinger F.B. Hepatitis B virus infection and transfusion medicine: science and the occult. Transfusion 2008;48(5):1001-26. DOI:10.1111/j.1537-2995.2008.01701.x
5. Trepo C., Chan H., Lok A. Hepatitis B virus infection. Lancet. 2014;384(9959):2053-63. DOI: 10.1016/S0140-6736(14)60220-8
6. Bertoletti A., Ferrari C. Adaptive immunity in HBV infection. J Hepatol; 2016;64:S71-83. DOI: 10.1016/j. jhep.2016.01.026
7. Seeger C., Mason W.S. Molecular biology of hepatitis B virus infection. Virology 2015;479-80:672-86. DOI: 10.1016/j.virol.2015.02.031
8. Tong S., Revill P. Overview of hepatitis B viral replication and genetic variability. J Hepatol. 2016;64:S4—16. DOI: 10.1016/j.jhep.2016.01.027
9. Tu T., Budzinska M.A., Vondran F.W.R., Shackel N.A., Urban S. Hepatitis B Virus DNA Integration Occurs Early in the Viral Life Cycle in an In Vitro Infection Model via Sodium Taurocholate Cotransporting PolypeptideDependent Uptake of Enveloped Virus Particles. J Virol. 2018;92(11):e02007-17. Published 2018 May 14. DOI: 10.1128/JVI.02007-1
10. Brechot C., Kremsdorf D., Soussan P., Dejean A., Paterlini-Brechot P., Tiollais P. Hepatitis B virus (HBV)-related hepatocellular carcinoma (HCC): molecular mechanisms and novel paradigms. Pathol Biol (Paris). 2010;58(4):278-87. DOI: 10.1016/j.patbio.2010.05.001
11. Mason W.S., Gill U.S., Litwin S., Zhou Y., Peri S., Pop O., et al. HBV DNA integration and clonal hepatocyte expansion in chronic hepatitis B patients considered immune tolerant. Gastroenterology 2016;151:986-98 e4. DOI: 10.1053/j.gastro.2016.07.012
12. Pollicino T., Squadrito G., Cerenzia G., Cacciola I., Raffa G., Craxi A., et al. Hepatitis B virus maintains its pro-oncogenic properties in the case of occult HBV infection. Gastroenterology. 2004;126(1):102-10. DOI: 10.1053/j.gastro.2003.10.048
13. Wong D.K., Huang F.Y., Lai C.L., Poon R.T., Seto W.K., Fung J., et al. Occult hepatitis B infection and HBV replicative activity in patients with cryptogenic cause of hepatocellular carcinoma. Hepatology. 2011;54:829-36.
14. Raimondo G., Locarnini S., Pollicino T., Levrero M., Zoulim F., Lok A.S., et al. Update of the statements on biology and clinical impact of occult hepatitis B virus infection. J Hepatol. 2019;71(2):397-408. DOI: 10.1016/j.jhep.2019.03.034
15. Villar L.M., Medina-Cruz H., Ribeiro-Barbosa J., Souz-Bezerra C., Machado-Portilho M., Scalioni L. Update on hepatitis B and C virus diagnosis. World J Virol. 2015;4(4):323-42. DOI: 10.5501/wjv.v4.i4.323
16. European Association for the Study of the Liver. Electronic address: easloffice@easloffice.eu; European Association for the Study of the Liver.EASL 2017 Clinical Practice Guidelines on the management of hepatitis B virus infection. J. Hepatol. 2017;67(2):370-98. DOI: 10.1016/j.jhep.2017.03.021
17. Song L.-W., Liu P.-G., Liu C.-J., Zhang T.-Y., Cheng X.-D., Wu H.-L., et al. Quantitative hepatitis B core antibody levels in the natural history of hepatitis B virus infection. Clin. Microbiol. Infect. 2015;21:197-203. DOI: 10.1016/j.cmi.2014.10.002
18. Yang H.-C., Tsou H.-H., Pei S.-N., Chang C.-S., Chen J.-H., Yao M., et al. Quantification of HBV core antibodies may help predict HBV reactivation in patients with lymphoma and resolved HBV infection. J Hepatol. 2018;69(2):286-292. DOI: 10.1016/j.jhep.2018.02.033
19. Moretto F., Catherine F.-X., Esteve C., Blot M., Piroth L. Isolated Anti-HBc: Significance and Management. J Clin Med. 2020;9(1):202. Published 2020 Jan 11. DOI: 10.3390/jcm9010202
20. Coppola N., Onorato L., Sagnelli C., Sagnelli E., Angelillo I.F. Association between anti-HBc positivity and hepatocellular carcinoma in HBsAg-negative subjects with chronic liver disease: A meta-analysis. Medicine (Baltimore). 2016;95(30):e4311. DOI: 10.1097/MD.0000000000004311
21. Paul S., Dickstein A., Saxena A., Terrin N., Viveiros K., Balk E.M., et al. Role of surface antibody in hepatitis B reactivation in patients with resolved infection and hematologic malignancy: A meta-analysis. Hepatology. 2017;66(2):379-388. DOI: 10.1002/hep.29082
22. Kuo M.H., Tseng C.-W., Lee C.-H., Tung C.-H., Tseng K.-C., Lai N.-S. Moderate Risk of Hepatitis B Virus Reactivation in HBsAg-/HBcAb+ Carriers Receiving Rituximab for Rheumatoid Arthritis. Sci Rep. 2020;10(1):2456. Published 2020 Feb 12. DOI: 10.1038/s41598-020-59406-4
23. Onozawa M., Hashino S., Izumiyama K., Kahata K., Chuma M., Mori A., et al. Progressive disappearance of anti-hepatitis B surface antigen antibody and reverse seroconversion after allogeneic hematopoietic stem cell transplantation in patients with previous hepatitis B virus infection. Transplantation. 2005;79(5):616-9. DOI: 10.1097/01.tp.0000151661.52601.fb
24. Hammond S.P., Borchelt A.M., Ukomadu C., Ho V.T., Baden L.R., Marty F.M. Hepatitis B virus reactivation following allogeneic hematopoietic stem cell transplantation. Biol Blood Marrow Transplant. 2009;15(9):1049-59. DOI: 10.1016/j.bbmt.2009.05.001
25. Kanaan N., Kabamba B., Marechal C., Pirson Y., Beguin C., Goffin E., et al. Significant rate of hepatitis B reactivation following kidney transplantation in patients with resolved infection. J Clin Virol. 2012;55(3):233-8. DOI: 10.1016/j.jcv.2012.07.015
26. Meng C., Belino C., Pereira L., Pinho A., Sampaio S., Tavares I., et al. Reactivation of Hepatitis B virus in kidney transplant recipients with previous clinically resolved infection: A single-center experience. Nefrologia. 2018;38(5):545-50. DOI: 10.1016/j.nefro.2018.02.004
27. Cornberg M., Lok A.S., Terrault N.A., Zoulim F.; 2019 EASL-AASLD HBV Treatment Endpoints Conference Faculty. Guidance for design and endpoints of clinical trials in chronic hepatitis B - Report from the 2019 EASL-AASLD HBV Treatment Endpoints Conference. J Hepatol. 2020;72(3):539-557. doi:10.1016/j.jhep.2019.11.003
28. Allain J.P., Hewitt P.E., Tedder R.S., Williamson L.M. Evidence that anti-HBc but not HBV DNA testing may prevent some HBV transmission by transfusion. Br J Haematol. 1999;107(1):186-95. DOI: 10.1046/j.1365-2141.1999.01665.x
29. Houareau C., Offergeld R. Anti-HBc screening — is it worth the effort? Results of a 10-year surveillance programme covering more than 30 million donations in Germany. Vox Sang. 2019;114(5):459-66. DOI: 10.1111/vox.12781
30. Zervou E.K., Dalekos G.N., Boumba D.S., Tsianos E.V. Value of anti-HBc screening of blood donors for prevention of HBV infection: results of a 3-year prospective study in Northwestern Greece. Transfusion. 2001;41(5):652-8. DOI: 10.1046/j.1537-2995.2001.41050652.x
31. Manzini P., Girotto M., Borsotti R., Giachino O., Guaschino R., Lanteri M., et al. Italian blood donors with anti-HBc and occult hepatitis B virus infection. Haematologica. 2007;92(12):1664-70. DOI: 10.3324/haematol.11224
32. Batskikh S.N., Teplinskaya N.P., Isakov V.A., Samokhvalov E.I., Kaganov B.S. Seropositive occult HBV infection in blood donors. Infectious Diseases. 2007;4:12-4 (In Russ.).
33. Makroo R.N., Chowdhry M., Bhatia A., Arora B., Rosamma N.L. Hepatitis B core antibody testing in Indian blood donors: A double-edged sword! Asian J Transfus Sci. 2012;6:10-3. PMID: 22623835. DOI: 10.4103/09736247.95043
34. Bhatti F.A., Ullah Z., Salamat N., Ayub M., Ghani E. Antihepatits B core antigen testing, viral markers, and occult hepatitis B virus infection in Pakistani blood donors: implications for transfusion practice. Transfusion. 2007;47(1):74-9. DOI: 10.1111/j.1537-2995.2007.01066.x
35. Findik D., Arslan U., Baykan M. Determination of hepatitis B virus DNA incidence, viral load, and mutations in blood donors with HBsAg and anti-HBs-negative serology and antibodies to hepatitis B core antigen. Eur J Intern Med 2007;18:571-5. PMID: 18054706. DOI: 10.1016/j.ejim.2007.07.001
36. Alizadeh Z., Milani S., Sharifi Z. Occult hepatitis B virus infection among Iranian blood donors: a preliminary study. Arch Iran Med. 2014;17(2):106-7.
37. Alshayea A.I., Eid G.E., El-Hazmi M.M., Alhetheel A.F. Prevalence and characterization of occult hepatitis B infection among blood donors in central Saudi Arabia. Saudi Med J. 2016;37(10):1114-9. DOI: 10.15537/smj.2016.10.14708
38. Seo D.H., Whang D.H., Song E.Y., Kim H.S., Park Q. Prevalence of antibodies to hepatitis B core antigen and occult hepatitis B virus infections in Korean blood donors. Transfusion. 2011;51(8):1840-6. DOI: 10.1111/j.1537-2995.2010.03056.x
39. Ye X., Li T., Xu X., Du P., Zeng J., Zhu W., et al. Characterisation and follow-up study of occult hepatitis B virus infection in anti-HBc-positive qualified blood donors in southern China. Blood Transfus. 2017;15(1):6-12. DOI: 10.2450/2016.0268-15
40. Shambesh M.K., Franka E.A., Agila A.R., Ismail F.F. Frequency of Hepatitis B core antibody and Hepatitis B Virus DNA among apparently healthy male blood donors in Eastern Libya. Libyan J Med Sci. 2018;2:12-5. DOI: 10.4103/LJMS.LJMS_47_17
41. Said Z.N., Sayed M.H., Salama I.I., Aboel-Magd E.K., Mahmoud M.H., Setouhy M.E., et al. Occult hepatitis B virus infection among Egyptian blood donors. World J Hepatol. 2013;5(2):64-73. DOI: 10.4254/wjh.v5.i2.64
42. Fopa D., Candotti D., Tagny C.T., Doux C., Mbanya D., Murphy E.L., et al. Occult hepatitis B infection among blood donors from Yaounde, Cameroon. Blood Transfus. 2019;17(6):403-8. DOI: 10.2450/2019.0182-19
43. Olotu A.A., Oyelese A.O., Salawu L., Audu R.A., Okwuraiwe A.P., Aboderin AO. Occult Hepatitis B virus infection in previously screened, blood donors in Ile-Ife, Nigeria: implications for blood transfusion and stem cell transplantation. Virol J. 2016;13:76. Published 2016 May 5. DOI: 10.1186/s12985-016-0533-3
44. Rios-Ocampo W.A., Cortes-Mancera F., Olarte J.C., Soto A., Navas M.C. Occult hepatitis B virus infection among blood donors in Colombia. Virol J. 2014;11:206. Published 2014 Nov 29. DOI: 10.1186/s12985-014-0206-z
45. Moresco M.N., Virgolino Hde A., de Morais M.P, da Motta-Passos I., Gomes-Gouvea M.S., de Assis L.M.S., et al. Occult hepatitis B virus infection among blood donors from the Brazilian Amazon: implications for transfusion policy. Vox Sang. 2014;107(1):19-25. DOI: 10.1111/vox.12125
46. Stramer S.L., Zou S., Notari E.P., Foster G.A., Krysztof D.E., Musavi F., Dodd R.Y. Blood donation screening for hepatitis B virus markers in the era of nucleic acid testing: are all tests of value? Transfusion 2012;52:440-6.
47. O'Brien S.F., Fearon M.A., Yi Q.L., Fan W., Scalia V., Muntz I.R., et al. Hepatitis B virus DNA-positive, hepatitis B surface antigen-negative blood donations intercepted by anti-hepatitis B core antigen testing: the Canadian Blood Services experience. Transfusion. 2007;47(10):1809-15. DOI: 10.1111/j.1537-2995.2007.01396.x
48. Seo D.H., Whang D.H., Song E.Y., Han K.S. Occult hepatitis B virus infection and blood transfusion. World J Hepatol. 2015;7(3):600-6. DOI: 10.4254/wjh.v7.i3.600
49. Candotti D., Laperche S. Hepatitis B Virus Blood Screening: Need for Reappraisal of Blood Safety Measures? Front Med (Lausanne). 2018;5:29. Published 2018 Feb 21. DOI: 10.3389/fmed.2018.00029
50. Prieto M., Gomez M.D., Berenguer M., Cordoba J., Rayon J.M., Pastoret M., et al. De novo hepatitis B after liver transplantation from hepatitis B core antibodypositive donors in an area with high prevalence of anti-HBc positivity in the donor population. Liver Transpl. 2001;7(1):51-8. DOI: 10.1053/jlts.2001.20786
51. Raimondo G., Pollicino T., Cacciola I., Squadrito G. Occult hepatitis B virus infection. J Hepatol. 2007;46(1):160-70. DOI: 10.1016/j.jhep.2006.10.007
52. Pin M., Compte M.T., Angelet P., Gallego C., Gutierrez C., Martinez Vea A. Evaluacion a largo plazo de la respuesta inmunologica a la vacuna de la hepatitis B en 136 pacientes en hemodialisis [Long-term evaluation of immune response to hepatitis B vaccine in 136 patients undergoing hemodialysis]. Nefrologia. 2009;29(5):415-20. DOI: 10.3265/Nefrologia.2009.29.5.5349.en.full
53. Cabrerizo M., Bartolome J., De Sequera P., Caramelo C., Carreno V. Hepatitis B virus DNA in serum and blood cells of hepatitis B surface antigen-negative hemodialysis patients and staff. J Am Soc Nephrol. 1997;8:1443-7. PMID: 9294837
54. Yoo J.H., Hwang S.G., Yang D.H., Son M.S., Kwon C.-I., Ko K.H., et al. Prevalence of occult hepatitis B virus infection in hemodialysis patients. Korean J Gastroenterol. 2013;61(4):209-14. DOI: 10.4166/kjg.2013.61.4.209
55. Weinstein T., Chagnac A., Boaz M., Ori Y., Herman M., Zevin D., Schmilovitz-Weiss H., Gafter U. Improved Immunogenicity of a Novel Third-Generation Recombinant Hepatitis B Vaccine in Patients with End-Stage Renal Disease. Nephron Clin Pract 2004;97:c67-72. DOI: 10.1159/000078403
56. Aksoy S., Harputluoglu H., Kilickap S., Dede D.S., Dizdar O., Altundag K., et al. Rituximab-related viral infections in lymphoma patients. Leuk Lymphoma. 2007;48(7):1307-12. DOI: 10.1080/10428190701411441
57. Wands J.R., Chura C.M., Roll F.J., Maddrey W.C. Serial studies of hepatitis-associated antigen and antibody in patients receiving antitumor chemotherapy for myeloproliferative and lymphoproliferative disorders. Gastroenterology. 1975;68(1):105-12.
58. Loomba R., Liang T.J. Hepatitis B Reactivation Associated With Immune Suppressive and Biological Modifier Therapies: Current Concepts, Management Strategies, and Future Directions. Gastroenterology. 2017; 152(6): 1297— 309. DOI: 10.1053/j.gastro.2017.02.009
59. Zhang Y., Shi Y., Wu R., Wang X, Gao X., Niu J. Primary biliary cholangitis is more severe in previous hepatitis B virus infection patients. Eur J Gastroenterol Hepatol. 2018;30(6):682-6. DOI: 10.1097/MEG.0000000000001100
60. Wang H., Swann R., Thomas E., Innes H.A., Valerio H., Hayes P.C., et al. Impact of previous hepatitis B infection on the clinical outcomes from chronic hepatitis C? A population-level analysis. J Viral Hepat. 2018;25(8):930-8. DOI: 10.1111/jvh.12897
61. Chan T.T., Chan W.K., Wong G.L., Chan A.W.-H., Mustapha N.R.N., Chan S.L., et al. Positive Hepatitis B Core Antibody Is Associated With Cirrhosis and Hepatocellular Carcinoma in Nonalcoholic Fatty Liver Disease. Am J Gastroenterol. 2020;115(6):867-75. DOI: 10.14309/ajg.0000000000000588
62. Batskikh S.N., Vinnitskaya E.V., Sbikina E.S., Borunova Z.V., Dorofeev A.S., Sandler Yu.G. Risk of Cirrhosis in Patients with Non-alcoholic Fatty Liver Disease and Previous Viral Hepatitis B. Russ J Gastroenterol Hepatol Coloproctol. 2020;30(4):28—34 (In Russ.). DOI: 10.22416/1382-4376-2020-30-4-28-34
63. Georgiadou S.P., Zachou K., Liaskos C., Gabeta S., Rigopoulou E.I., Dalekos G.N. Occult hepatitis B virus infection in patients with autoimmune liver diseases. Liver Int. 2009;29(3):434-42. DOI: 10.1111/j.1478-3231.2008.01851.x
64. Chen X.X., Xiang K.H., Zhang H.P., Kong X.-S., Huang C.-Y., Liu Y.-M., et al. Occult HBV infection in patients with autoimmune hepatitis: A virological and clinical study [published online ahead of print, 2019 May 18]. J Microbiol Immunol Infect. 2019;S1684-1182(19)30046-5. DOI: 10.1016/j.jmii.2019.04.009
65. Maya R., Gershwin M.E., Shoenfeld Y. Hepatitis B virus (HBV) and autoimmune disease. Clin Rev Allergy Immunol. 2008;34(1):85-102. DOI: 10.1007/s12016-007-8013-6
66. Christen U., Hintermann E. Autoantibodies in Autoimmune Hepatitis: Can Epitopes Tell Us about the Etiology of the Disease? Front Immunol. 2018;9:163. Published 2018 Feb 16. DOI: 10.3389/fimmu.2018.00163
67. Shi Y., Wu Y.H., Wu W., Zhang W.J., Yang J., Chen Z. Association between occult hepatitis B infection and the risk of hepatocellular carcinoma: a meta-analysis. Liver Int. 2012;32(2):231-40. DOI: 10.1111/j.1478-3231.2011.02481.x
68. Yip T.C.-F., Chan H.L.-Y., Wong V.W.-S., Tse Y.-K., Lam K.L.-Y., Wong G.L.-H. Impact of age and gender on risk of hepatocellular carcinoma after hepatitis B surface antigen seroclearance. J Hepatol. 2017;67(5):902—8. DOI: 10.1016/j.jhep.2017.06.019
69. Fang Y., Shang Q.L., Liu J.Y., Li D., Xu W.-Z., Teng X., et al. Prevalence of occult hepatitis B virus infection among hepatopathy patients and healthy people in China. J Infect. 2009;58(5):383-8. DOI: 10.1016/j.jinf.2009.02.013
70. Wong D.K., Cheng S.C.Y., Mak L.L., To E.W.-P., Lo R.C.-L., Cheung T.-T., et al. Among Patients with Undetectable Hepatitis B Surface Antigen and Hepatocellular Carcinoma, a High Proportion Has Integration of HBV DNA into Hepatocyte DNA and No Cirrhosis. Clin Gastroenterol Hepatol. 2020;18(2):449-56. DOI: 10.1016/j.cgh.2019.06.029
71. Saitta C., Tripodi G., Barbera A., Bertuccio A., Smedile A., Ciancio A., et al. Hepatitis B virus (HBV) DNA integration in patients with occult HBV infection and hepatocellular carcinoma. Liver Int. 2015;35(10):2311—7. DOI: 10.1111/liv.12807
72. Sung W.K., Zheng H., Li S., Chen R., Liu X., Li Y., et al. Genome-wide survey of recurrent HBV integration in hepatocellular carcinoma. Nat Genet. 2012;44(7):765-9. Published 2012 May 27. DOI: 10.1038/ng.2295
73. Yang L., Ye S., Zhao X., Ji L., Zhang Y., Zhou P., et al. Molecular Characterization of HBV DNA Integration in Patients with Hepatitis and Hepatocellular Carcinoma. J Cancer. 2018;9(18):3225-35. Published 2018 Sep 7. DOI: 10.7150/jca.26052
74. Tu T., Budzinska M.A., Shackel N.A., Urban S. HBV DNA Integration: Molecular Mechanisms and Clinical Implications. Viruses. 2017;9(4):75. Published 2017 Apr 10. DOI: 10.3390/v9040075
75. Budzinska M.A., Shackel N.A., Urban S., Tu T. Cellular Genomic Sites of Hepatitis B Virus DNA Integration. Genes (Basel). 2018;9(7):365. Published 2018 Jul 20. DOI: 10.3390/genes9070365
76. Wang D., Cai H., Yu W.B., Yu L. Identification of hepatitis B virus X gene variants between hepatocellular carcinoma tissues and pericarcinoma liver tissues in Eastern China. Int J Clin Exp Pathol. 2014;7(9):5988—96. Published 2014 Aug 15.
77. Wang Y., Zeng L.I., Chen W. HBV X gene point mutations are associated with the risk of hepatocellular carcinoma: A systematic review and meta-analysis. Mol Clin Oncol. 2016;4(6):1045-51. DOI: 10.3892/mco.2016.847
78. Tu H., Bonura C., Giannini C., Mouly H., Soussan P., Kew M., et al. Biological impact of natural COOH-terminal deletions of hepatitis B virus X protein in hepatocellular carcinoma tissues. Cancer Res. 2001;61(21):7803-10.
79. Ng K.Y., Chai S., Tong M., Guan X.-Y., Lin C.-H., Ching Y.-P., et al. C-terminal truncated hepatitis B virus X protein promotes hepatocellular carcinogenesis through induction of cancer and stem cell-like properties. Oncotarget. 2016;7(17):24005-17. DOI: 10.18632/oncotarget.8209
80. 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(3):581-92. DOI: 10.1016/j.jhep.2009.05.022
81. Pollicino T., Vegetti A., Saitta C., Ferrara F., Corradini E., Raffa G., et al. Hepatitis B virus DNA integration in tumour tissue of a non-cirrhotic HFE-haemochromatosis patient with hepatocellular carcinoma. J Hepatol. 2013;58(1):190-3. DOI: 10.1016/j.jhep.2012.09.005
82. Hwang G.Y., Lin C.Y., Huang L.M., Wang Y.-H., Wang J.-C., Hsu C.-T., et al. Detection of the hepatitis B virus X protein (HBx) antigen and anti-HBx antibodies in cases of human hepatocellular carcinoma. J Clin Microbiol. 2003;41(12):5598-603. DOI: 10.1128/jcm.41.12.5598-5603.2003
83. Peng Z., Zhang Y., Gu W., Li D., Zhang F., Qiu G., et al. Integration of the hepatitis B virus X fragment in hepatocellular carcinoma and its effects on the expression of multiple molecules: a key to the cell cycle and apoptosis. Int J Oncol. 2005;26(2):467-73.
84. Tarocchi M., Polvani S., Marroncini G., Galli A. Molecular mechanism of hepatitis B virus-induced hepatocarcino-genesis. World J Gastroenterol. 2014;20(33):11630-40. DOI: 10.3748/wjg.v20.i33.11630
85. Dejean A., Lugassy C., Zafrani S., Tiollais P., Brechot C. Detection of hepatitis B virus DNA in pancreas, kidney and skin of two human carriers of the virus. J Gen Virol. 1984;65( Pt 3):651-5. DOI: 10.1099/0022-1317-653-651
86. Mason A., Wick M., White H., Perrillo R. Hepatitis B virus replication in diverse cell types during chronic hepatitis B virus infection. Hepatology. 1993;18(4):781-9. DOI: 10.1002/hep.1840180406
87. Umeda M., Marusawa H., Seno H., Katsurada A., Nabeshima M., Egawa H., et al. Hepatitis B virus infection in lymphatic tissues in inactive hepatitis B carriers. J Hepatol. 2005;42(6):806-12. DOI: 10.1016/j.jhep.2005.01.016
88. Mason A., Theal J., Bain V., Adams E., Perrillo R. Hepatitis B virus replication in damaged endothelial tissues of patients with extrahepatic disease. Am J Gastroenterol. 2005;100(4):972-6. DOI: 10.1111/j.1572-0241.2005.41308.x
89. Iloeje U.H., Yang H.I., Jen C.L., Su J., Wang L.-Y., You S.-L., et al. Risk of pancreatic cancer in chronic hepatitis B virus infection: data from the REVEAL-HBV cohort study. Liver Int. 2010;30(3):423-9. DOI: 10.1111/j.1478-3231.2009.02147.x
90. Desai R., Patel U., Sharma S., Singh S., Doshi S., Shaheen S., et al. Association Between Hepatitis B Infection and Pancreatic Cancer: A Population-Based Analysis in the United States. Pancreas. 2018;47(7):849-55. DOI: 10.1097/MPA.0000000000001095
91. Jung Y.S., Kim N.H., Park J.H., Park D.I., Sohn C.I. Correlation between Hepatitis B Virus Infection and Colorectal Neoplasia. J Clin Med. 2019;8(12):2085. DOI: 10.3390/jcm8122085
92. Su F.H., Le T.N., Muo C.H., Te S.A., Sung F.C., Yeh C.C. Chronic Hepatitis B Virus Infection Associated with Increased Colorectal Cancer Risk in Taiwanese Population. Viruses. 2020;12(1):97. Published 2020 Jan 14. DOI: 10.3390/v12010097
93. Song C., Lv J., Liu Y., Chen J.G., Ge Z., Zhu J., et al. Associations Between Hepatitis B Virus Infection and Risk of All Cancer Types. JAMA Netw Open. 2019;2(6):e195718. Published 2019 Jun 5. DOI: 10.1001/jamanetworkopen.2019.5718
94. Wang Y., Yang S., Song F., Cao S., Yin X., Xie J., et al. Hepatitis B virus status and the risk of pancreatic cancer: a meta-analysis. Eur J Cancer Prev. 2013;22(4):328-34. DOI: 10.1097/CEJ.0b013e32835b6a21
95. Jin Y., Gao H., Chen H., Wang J., Chen M., Li G., et al. Identification and impact of hepatitis B virus DNA and antigens in pancreatic cancer tissues and adjacent non-cancerous tissues. Cancer Lett. 2013;335(2):447-54. DOI: 10.1016/j.canlet.2013.03.001
96. zur Hausen H., de Villiers E.M. Cancer “causation” by infections-individual contributions and synergistic networks. Semin Oncol. 2014;41(6):860-75. DOI: 10.1053/j.seminoncol.2014.10.003
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Review
For citations:
Batskikh S.N. Resolved Hepatitis B: Achieved or Imaginary Wellbeing? Russian Journal of Gastroenterology, Hepatology, Coloproctology. 2021;31(1):7-19. (In Russ.) https://doi.org/10.22416/1382-4376-2021-31-1-7-19