Spontaneous reactivation of hepatitis B virus (HBV) infection in patients with resolved or occult HBV infection

Journal of Medical Virology

Volumn 87, Issue 4, 2015, Pages 589-600

  Kamitsukasa, Hiroshi ^a   Iri, Masanobu ^a   Tanaka, Akihisa ^a   Nagashima, Shigeo ^b   Takahashi, Masaharu ^b   Nishizawa, Tsutomu ^b   Okamoto, Hiroaki ^b  

^a TOKYO NATIONAL HOSPITAL   (Japan)

^b JICHI MEDICAL UNIVERSITY   (Japan)

Author keywords

Entire genome; Hepatitis viruses; Phylogenetic analysis; Precore mutant

Indexed keywords

ALANINE AMINOTRANSFERASE; ALBUMIN; ASPARTATE AMINOTRANSFERASE; BILIRUBIN; CHOLESTEROL; CISPLATIN; CREATININE; ENTECAVIR; FLUOROURACIL; GAMMA GLUTAMYLTRANSFERASE; HEMOGLOBIN; HEPATITIS B SURFACE ANTIBODY; HEPATITIS B SURFACE ANTIGEN; HEPATITIS B(E) ANTIGEN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; PROTEIN; UREA; VIRUS DNA; HEPATITIS B ANTIBODY;

AGED; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ALBUMIN BLOOD LEVEL; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BILIRUBIN BLOOD LEVEL; CASE REPORT; CHOLECYSTECTOMY; CHOLELITHIASIS; CHOLESTEROL BLOOD LEVEL; CORONARY ARTERY BYPASS GRAFT; CREATININE BLOOD LEVEL; DEATH; DIABETES MELLITUS; DRUG MISUSE; ENDOSCOPIC MUCOSAL RESECTION; ERYTHROCYTE COUNT; ESOPHAGUS CANCER; GAMMA GLUTAMYL TRANSFERASE BLOOD LEVEL; GENERAL CONDITION DETERIORATION; GENOTYPE; GERIATRIC PATIENT; HEMATOCRIT; HEMOGLOBIN BLOOD LEVEL; HEPATITIS B VIRUS; HOSPITAL ADMISSION; HUMAN; LABORATORY TEST; LEUKOCYTE COUNT; MALE; NUCLEOTIDE SEQUENCE; OUTPATIENT CARE; PATIENT HISTORY OF SURGERY; PHYLOGENY; PROMOTER REGION; PROTEIN BLOOD LEVEL; SEQUENCE ANALYSIS; UREA NITROGEN BLOOD LEVEL; VIRUS REACTIVATION; VIRUS REPLICATION; ADVERSE EFFECTS; BLOOD; CHEMISTRY; COMPLICATION; DNA SEQUENCE; ENDOSCOPY; ESOPHAGUS TUMOR; GENETICS; HEPATITIS B; IMMUNOCOMPROMISED PATIENT; MOLECULAR GENETICS; PHYSIOLOGY; VIROLOGY; VIRUS ACTIVATION;

HEPATITIS B VIRUS;

AGED; CORONARY ARTERY BYPASS; DNA, VIRAL; ENDOSCOPY; ESOPHAGEAL NEOPLASMS; GENOTYPE; HEPATITIS B; HEPATITIS B ANTIBODIES; HEPATITIS B SURFACE ANTIGENS; HEPATITIS B VIRUS; HUMANS; IMMUNOCOMPROMISED HOST; MALE; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; VIRUS ACTIVATION;

EID: 84922947341     PISSN: 01466615     EISSN: 10969071     Source Type: Journal    
DOI: 10.1002/jmv.24115     Document Type: Article

References (61)

1. Akahane Y, Okada S, Sakamoto M, Wakamiya M, Kitamura T, Tawara A, Naitoh S, Tsuda F, Okamoto H. 2002. Persistence of hepatitis B viremia after recovery from acute hepatitis B: Correlation between anti-HBc titer and HBV DNA in serum. Hepatol Res 24:8-17.
2. Arauz-Ruiz P, Norder H, Robertson BH, Magnius LO. 2002. Genotype H: A new Amerindian genotype of hepatitis B virus revealed in Central America. J Gen Virol 83:2059-2073.
3. Blackberg J, Kidd-Ljunggren K. 2000. Occult hepatitis B virus after acute self-limited infection persisting for 30 years without sequence variation. J Hepatol 33:992-997.
4. Davis GL, Hoofnagle JH, Waggoner JG. 1984. Spontaneous reactivation of chronic hepatitis B virus infection. Gastroenterology 86:230-235.
5. Fattovich G, Brollo L, Alberti A, Realdi G, Pontisso P, Giustina G, Ruol A. 1990. Spontaneous reactivation of hepatitis B virus infection in patients with chronic type B hepatitis. Liver 10:141-146.
6. Goujon M, McWilliam H, Li W, Valentin F, Squizzato S, Paern J, Lopez R. 2010. A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res 38:W695-W699.
7. Gupta S, Govindarajan S, Fong TL, Redeker AG. 1990. Spontaneous reactivation in chronic hepatitis B: Patterns and natural history. J Clin Gastroenterol 12:562-568.
8. Hoofnagle JH. 2009. Reactivation of hepatitis B. Hepatology 49:S156-S165.
9. Hui CK, Cheung WW, Zhang HY, Au WY, Yueng YH, Leung AY, Leung N, Luk JM, Lie AK, Kwong YL, Liang R, Lau GK. 2006. Kinetics and risk of de novo hepatitis B infection in HBsAg-negative patients undergoing cytotoxic chemotherapy. Gastroenterology 131:59-68.
10. Inoue J, Takahashi M, Nishizawa T, Narantuya L, Sakuma M, Kagawa Y, Shimosegawa T, Okamoto H. 2005. High prevalence of hepatitis delta virus infection detectable by enzyme immunoassay among apparently healthy individuals in Mongolia. J Med Virol 76:333-340.
11. Inuzuka T, Ueda Y, Morimura H, Fujii Y, Umeda M, Kou T, Osaki Y, Uemoto S, Chiba T, Marusawa H. 2014. Reactivation from occult HBV carrier status is characterized by low genetic heterogeneity with the wild-type or G1896A variant prevalence. J Hepatol 61:492-501.
12. Kim JH, Park YK, Park ES, Kim KH. 2014. Molecular diagnosis and treatment of drug-resistant hepatitis B virus. World J Gastroenterol 20:5708-5720.
13. Kosaka Y, Takase K, Kojima M, Shimizu M, Inoue K, Yoshiba M, Tanaka S, Akahane Y, Okamoto H, Tsuda F, Miyakawa Y, Mayumi M. 1991. Fulminant hepatitis B: Induction by hepatitis B virus mutants defective in the precore region and incapable of encoding e antigen. Gastroenterology 100:1087-1094.
14. Kusumoto S, Tanaka Y, Mizokami M, Ueda R. 2009. Reactivation of hepatitis B virus following systemic chemotherapy for malignant lymphoma. Int J Hematol 90:13-23.
15. Laskus T, Rakela J, Tong MJ, Persing DH. 1994. Nucleotide sequence analysis of the precore region in patients with spontaneous reactivation of chronic hepatitis B. Dig Dis Sci 39:2000-2006.
16. Lavanchy D. 2004. Hepatitis B virus epidemiology, disease burden, treatment, and current and emerging prevention and control measures. J Viral Hepat 11:97-107.
17. Lennard TW, Shenton BK, Borzotta A, Donnelly PK, White M, Gerrie LM, Proud G, Taylor RM. 1985. The influence of surgical operations on components of the human immune system. Br J Surg 72:771-776.
18. Levrero M, Pollicino T, Petersen J, Belloni L, Raimondo G, Dandri M. 2009. Control of cccDNA function in hepatitis B virus infection. J Hepatol 51:581-592.
19. Liang TJ. 2009. Hepatitis B: The virus and disease. Hepatology 49:S13-S21.
20. Liang TJ, Hasegawa K, Rimon N, Wands JR, Ben-Porath E. 1991. A hepatitis B virus mutant associated with an epidemic of fulminant hepatitis. N Engl J Med 324:1705-1709.
21. Lok AS, Liang RH, Chiu EK, Wong KL, Chan TK, Todd D. 1991. Reactivation of hepatitis B virus replication in patients receiving cytotoxic therapy. Report of a prospective study. Gastroenterology 100:182-188.
22. Loomba R, Rowley A, Wesley R, Liang TJ, Hoofnagle JH, Pucino F, Csako G. 2008. Systematic review: The effect of preventive lamivudine on hepatitis B reactivation during chemotherapy. Ann Intern Med 148:519-528.
23. Marzano A, Angelucci E, Andreone P, Brunetto M, Bruno R, Burra P, Caraceni P, Daniele B, Di Marco V, Fabrizi F, Fagiuoli S, Grossi P, Lampertico P, Meliconi R, Mangia A, Puoti M, Raimondo G, Smedile A. 2007. Prophylaxis and treatment of hepatitis B in immunocompromised patients. Dig Liver Dis 39:397-408.
24. Mason WS, Gerlich WH, Taylor JM, Kann M, Mizokami M, Loeb D, Sureau C, Magnius L, Norder H. 2012. Hepadnaviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ, editors. Virus taxonomy. Ninth report of the International Committee on taxonomy of viruses. Oxford: Elsevier/Academic Press. pp 445-455.
25. Meyer RA, Duffy MC. 1993. Spontaneous reactivation of chronic hepatitis B infection leading to fulminant hepatic failure. Report of two cases and review of the literature. J Clin Gastroenterol 17:231-234.
26. Michalak TI, Pasquinelli C, Guilhot S, Chisari FV. 1994. Hepatitis B virus persistence after recovery from acute viral hepatitis. J Clin Invest 93:230-239.
27. Moriyama K, Okamoto H, Tsuda F, Mayumi M. 1996. Reduced precore transcription and enhanced core-pregenome transcription of hepatitis B virus DNA after replacement of the precore-core promoter with sequences associated with e antigen-seronegative persistent infections. Virology 226:269-280.
28. Mulyanto, Depamede SN, Surayah K, Tjahyono AA, Jirintai, Nagashima S, Takahashi M, Okamoto H. 2010. Identification and characterization of novel hepatitis B virus subgenotype C10 in Nusa Tenggara, Indonesia. Arch Virol 155:705-715.
29. Mulyanto, Pancawardani P, Depamede SN, Wahyono A, Jirintai S, Nagashima S, Takahashi M, Nishizawa T, Okamoto H. 2012. Identification of four novel subgenotypes (C13-C16) and two inter-genotypic recombinants (C12/G and C13/B3) of hepatitis B virus in Papua province, Indonesia. Virus Res 163:129-140.
30. Nakao R, Yatsuhashi H, Myoji M, Tsuchida T, Kusumoto K, Kamihira T, Nagaoka S, Ohata K, Yano K, Ahiru S, Komori A, Matsumoto T, Daikoku M, Ishibashi H. 2006. Discrimination between acute hepatitis B and acute exacerbation of chronic hepatitis B by measurement of IgM class antibody to hepatitis core antigen by CLIA method. Kanzo 47:279-282.
31. Norder H, Courouce AM, Magnius LO. 1994. Complete genomes, phylogenetic relatedness, and structural proteins of six strains of the hepatitis B virus, four of which represent two new genotypes. Virology 198:489-503.
32. Okamoto H, Tsuda F, Sakugawa H, Sastrosoewignjo RI, Imai M, Miyakawa Y, Mayumi M. 1988. Typing hepatitis B virus by homology in nucleotide sequence: Comparison of surface antigen subtypes. J Gen Virol 69:2575-2583.
33. Okamoto H, Yotsumoto S, Akahane Y, Yamanaka T, Miyazaki Y, Sugai Y, Tsuda F, Tanaka T, Miyakawa Y, Mayumi M. 1990. Hepatitis B viruses with precore region defects prevail in persistently infected hosts along with seroconversion to the antibody against e antigen. J Virol 64:1298-1303.
34. Okuno T, Takeda M, Matsumoto M, Shindo M, Arai K, Takino T. 1989. Spontaneous reactivation of hepatitis B virus replication in HBsAg carriers who seroconverted from HBeAg to anti-HBe. Jpn J Med 28:45-49.
35. Omata M, Ehata T, Yokosuka O, Hosoda K, Ohto M. 1991. Mutations in the precore region of hepatitis B virus DNA in patients with fulminant and severe hepatitis. N Engl J Med 324:1699-1704.
36. Pei R, Grund S, Verheyen J, Esser S, Chen X, Lu M. 2014. Spontaneous reactivation of hepatitis B virus replication in an HIV coinfected patient with isolated anti-Hepatitis B core antibodies. Virol J 11:9.
37. Perrillo RP. 2001. Acute flares in chronic hepatitis B: The natural and unnatural history of an immunologically mediated liver disease. Gastroenterology 120:1009-1022.
38. Raimondo G, Allain JP, Brunetto MR, Buendia MA, Chen DS, Colombo M, Craxi A, Donato F, Ferrari C, Gaeta GB, Gerlich WH, Levrero M, Locarnini S, Michalak T, Mondelli MU, Pawlotsky JM, Pollicino T, Prati D, Puoti M, Samuel D, Shouval D, Smedile A, Squadrito G, Trepo C, Villa E, Will H, Zanetti AR, Zoulim F. 2008. Statements from the Taormina expert meeting on occult hepatitis B virus infection. J Hepatol 49:652-657.
39. Raimondo G, Caccamo G, Filomia R, Pollicino T. 2013. Occult HBV infection. Semin Immunopathol 35:39-52.
40. Restrepo BI, Schlesinger LS. 2014. Impact of diabetes on the natural history of tuberculosis. Diabetes Res Clin Pract 106:191-199.
41. Rodella A, Galli C, Terlenghi L, Perandin F, Bonfanti C, Manca N. 2006. Quantitative analysis of HBsAg, IgM anti-HBc and anti-HBc avidity in acute and chronic hepatitis B. J Clin Virol 37:206-212.
42. Rodriguez C, Chevaliez S, Bensadoun P, Pawlotsky JM. 2013. Characterization of the dynamics of hepatitis B virus resistance to adefovir by ultra-deep pyrosequencing. Hepatology 58:890-901.
43. Saitou N, Nei M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425.
44. Sato S, Suzuki K, Akahane Y, Akamatsu K, Akiyama K, Yunomura K, Tsuda F, Tanaka T, Okamoto H, Miyakawa Y, Mayumi M. 1995. Hepatitis B virus strains with mutations in the core promoter in patients with fulminant hepatitis. Ann Intern Med 122:241-248.
45. Seth P, Alrajhi AA, Kagevi I, Chaudhary MA, Colcol E, Sahovic E, Aljurf M, Gyger M. 2002. Hepatitis B virus reactivation with clinical flare in allogeneic stem cell transplants with chronic graft-versus-host disease. Bone Marrow Transplant 30:189-194.
46. Shouval D, Shibolet O. 2013. Immunosuppression and HBV reactivation. Semin Liver Dis 33:167-177.
47. Steinberg JL, Yeo W, Zhong S, Chan JY, Tam JS, Chan PK, Leung NW, Johnson PJ. 2000. Hepatitis B virus reactivation in patients undergoing cytotoxic chemotherapy for solid tumours: Precore/core mutations may play an important role. J Med Virol 60:249-255.
48. Stramer SL, Wend U, Candotti D, Foster GA, Hollinger FB, Dodd RY, Allain JP, Gerlich W. 2011. Nucleic acid testing to detect HBV infection in blood donors. N Engl J Med 364:236-247.
49. Stuyver L, De Gendt S, Van Geyt C, Zoulim F, Fried M, Schinazi RF, Rossau R. 2000. A new genotype of hepatitis B virus: Complete genome and phylogenetic relatedness. J Gen Virol 81:67-74.
50. Szczesny T, Slotwinski R, Szczesny G. 2005. Changes in humoral and cellular immunity in patients operated on due to esophageal cancer. Pol Merkur Lekarski 18:478-482.
51. Takahashi M, Kusakai S, Mizuo H, Suzuki K, Fujimura K, Masuko K, Sugai Y, Aikawa T, Nishizawa T, Okamoto H. 2005. Simultaneous detection of immunoglobulin A (IgA) and IgM antibodies against hepatitis E virus (HEV) is highly specific for diagnosis of acute HEV infection. J Clin Microbiol 43:49-56.
52. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6. 0. Mol Biol Evol 30:2725-2729.
53. Tanaka Y, Orito E, Yuen MF, Mukaide M, Sugauchi F, Ito K, Ozasa A, Sakamoto T, Kurbanov F, Lai CL, Mizokami M. 2005. Two subtypes (subgenotypes) of hepatitis B virus genotype C: A novel subtyping assay based on restriction fragment length polymorphism. Hepatol Res 33:216-224.
54. Tatematsu K, Tanaka Y, Kurbanov F, Sugauchi F, Mano S, Maeshiro T, Nakayoshi T, Wakuta M, Miyakawa Y, Mizokami M. 2009. A genetic variant of hepatitis B virus divergent from known human and ape genotypes isolated from a Japanese patient and provisionally assigned to new genotype J. J Virol 83:10538-10547.
55. Tong MJ, Sampliner RE, Govindarajan S, Co RL. 1987. Spontaneous reactivation of hepatitis B in Chinese patients with HBsAg-positive chronic active hepatitis. Hepatology 7:713-718.
56. Tran TT, Trinh TN, Abe K. 2008. New complex recombinant genotype of hepatitis B virus identified in Vietnam. J Virol 82:5657-5663.
57. Umemura T, Tanaka E, Kiyosawa K, Kumada H. 2008. Mortality secondary to fulminant hepatic failure in patients with prior resolution of hepatitis B virus infection in Japan. Clin Infect Dis 47:e52-e56.
58. Usuda S, Okamoto H, Iwanari H, Baba K, Tsuda F, Miyakawa Y, Mayumi M. 1999. Serological detection of hepatitis B virus genotypes by ELISA with monoclonal antibodies to type-specific epitopes in the preS2-region product. J Virol Methods 80:97-112.
59. Yuki N, Nagaoka T, Yamashiro M, Mochizuki K, Kaneko A, Yamamoto K, Omura M, Hikiji K, Kato M. 2003. Long-term histologic and virologic outcomes of acute self-limited hepatitis B. Hepatology 37:1172-1179.
60. Zachou K, Sarantopoulos A, Gatselis NK, Vassiliadis T, Gabeta S, Stefos A, Saitis A, Boura P, Dalekos GN. 2013. Hepatitis B virus reactivation in hepatitis B virus surface antigen negative patients receiving immunosuppression: A hidden threat. World J Hepatol 5:387-392.
61. Zhang Y, Hu XY, Zhong S, Yang F, Zhou TY, Chen G, Wang YY, Luo JX. 2014. Entecavir vs lamivudine therapy for naive patients with spontaneous reactivation of hepatitis B presenting as acute-on-chronic liver failure. World J Gastroenterol 20:4745-4752.