Infection

, Volume 44, Issue 5, pp 575–582 | Cite as

Occult HBV infection in the oncohematological setting

  • C. Sagnelli
  • M. Macera
  • M. Pisaturo
  • R. Zampino
  • M. Coppola
  • E. Sagnelli
Review

Abstract

Introduction

Occult hepatitis B infection (OBI), a virological condition characterized by a low release of Hepatitis B Virus (HBV) from liver cells and low HBV-DNA levels in serum and/or liver tissue of HBsAg-negative subjects, may reactivate in oncohematological patients undergoing immunosuppression by aggressive chemotherapy or hematopoietic stem cell transplantation. The entity of OBI reactivation varies from an increase in HBV replication without liver damage to an active HBV replication followed by liver cell necrosis, frequently severe and in some cases life threatening. Because of a possible severe outcome associated with OBI reactivation (hepatic failure or death due to the discontinuation of chemotherapy), prophylaxis with anti-HBV nucleot(s)ide analogues is recommended in relation to the foreseeable degree of immunosuppression.

Materials and methods

This review article focuses on the clinical impact of OBI in the oncohematological setting and is addressed to all health care workers having in care oncohematological patients or involved in the treatment of HBV infection and OBI prophylaxis.

Conclusion

International guidelines have indicated lamivudine prophylaxis in hematopoietic stem cell transplantation and when high-dose corticosteroids or anti-CD20 or anti-CD52 monoclonal antibodies are used. Entecavir or tenofovir should replace lamivudine for patients with advanced liver diseases for whom reactivation of OBI may be life threatening. When anti-CD20 or anti-CD52 sparing schedules or other non-aggressive chemotherapies are used, monitoring may be indicated, but very early treatment with highly effective antiviral drugs (entecavir or tenofovir) should be administered once a reactivation of OBI has occurred.

Keywords

Occult HBV infection Silent HBV infection Oncohematological setting Immunosuppression HBV prophylactic measures HBV infection 

References

  1. 1.
    Torbenson M, Thomas DL. Occult hepatitis B. Lancet Infect Dis. 2002;2:479–86. doi:10.1016/S14733099(02)00345-6.CrossRefPubMedGoogle Scholar
  2. 2.
    Izmirli S, Celik DG, Yuksel P, Saribas S, Aslan M, Ergin S, et al. The detection of occult HBV infection in patients with HBsAg negative pattern by real-time PCR method. Transfus Apher Sci. 2012;47:283–7. doi:10.1016/j.transci.2012.07.009.CrossRefPubMedGoogle Scholar
  3. 3.
    Coppola N, Loquercio G, Tonziello G, Azzaro R, Pisaturo M, Di Costanzo G, et al. HBV transmission from an occult carrier with five mutations in the major hydrophilic region of HBsAg to an immunosuppressed plasma recipient. J Clin Virol. 2013;58:315–7. doi:10.1016/j.jcv.2013.06.020.CrossRefPubMedGoogle Scholar
  4. 4.
    Raimondo G, Allain JP, Brunetto MR, Buendia MA, Chen DS, Colombo M, et al. Statements from the Taormina expert meeting on occult hepatitis B virus infection. J Hepatol. 2008;49:652–7. doi:10.1016/j.jhep.2008.07.014.CrossRefPubMedGoogle Scholar
  5. 5.
    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.CrossRefPubMedGoogle Scholar
  6. 6.
    Grob P, Jilg W, Bornhak H, Gerken G, Gerlich W, Günther S, et al. Serological pattern “anti-HBc alone”: report on a workshop. J Med Virol. 2000;62:450–5.CrossRefPubMedGoogle Scholar
  7. 7.
    Jilg W, Hottenträger B, Weinberger K, Schlottmann K, Frick E, Holstege A, et al. Prevalence of markers of hepatitis B in the adult German population. J Med Virol. 2001;63:96–102.CrossRefPubMedGoogle Scholar
  8. 8.
    Weber B, Melchior W, Gehrke R, Doerr HW, Berger A, Rabenau H. Hepatitis B virus markers in anti-HBc only positive individuals. J Med Virol. 2001;64:312–9.CrossRefPubMedGoogle Scholar
  9. 9.
    Hu KQ. Occult hepatitis B virus infection and its clinical implications. J Viral Hepat. 2002;9:243–57.CrossRefPubMedGoogle Scholar
  10. 10.
    Urbani S, Fagnoni F, Missale G, Franchini M. The role of anti-core antibody response in the detection of occult hepatitis B virus infection. Clin Chem Lab Med. 2010;48:23–9. doi:10.1515/CCLM.2010.002.CrossRefPubMedGoogle Scholar
  11. 11.
    Schmeltzer P, Sherman KE. Occult hepatitis B: clinical implications and treatment decisions. Dig Dis Sci. 2010;55:3328–35. doi:10.1007/s10620-010-1413-0.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Samal J, Kandpal M, Vivekanandan P. Molecular mechanisms underlying occult hepatitis B virus infection. Clin Microbiol Rev. 2012;25:142–142. doi:10.1128/CMR.00018-11.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    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;341:22–6. doi:10.1056/NEJM199907013410104.CrossRefPubMedGoogle Scholar
  14. 14.
    Raimondo G, Caccamo G, Filomia R, Pollicino T. Occult HBV infection. Semin Immunopathol. 2013;35:39–52. doi:10.1007/s00281-012-0327-7.CrossRefPubMedGoogle Scholar
  15. 15.
    Marusawa H, Osaki Y, Kimura T, Ito K, Yamashita Y, Eguchi T, et al. High prevalence of anti-hepatitis B virus serological markers in patients with hepatitis C virus related chronic liver disease in Japan. Gut. 1999;45:284–8.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Fukuda R, Ishimura N, Niigaki M, Hamamoto S, Satoh S, Tanaka S, et al. Serologically silent hepatitis B virus coinfection in patients with hepatitis C virus-associated chronic liver disease: clinical and virological significance. J Med Virol. 1999;58:201–7.CrossRefPubMedGoogle Scholar
  17. 17.
    Filippini P, Coppola N, Pisapia R, Scolastico C, Marrocco C, Zaccariello A, et al. Impact of occult hepatitis B virus infection in HIV patients naive for antiretroviral therapy. AIDS. 2006;20:1253–60. doi:10.1097/01.aids.0000232232.41877.2a.CrossRefPubMedGoogle Scholar
  18. 18.
    Neau D, Winnock M, Jouvencel AC, Faure M, Castéra L, Legrand E, et al. Occult hepatitis B virus infection in HIV-infected patients with isolated antibodies to hepatitis B core antigen: aquitaine cohort, 2002-2003. Clin Infect Dis. 2005;40:750–3. doi:10.1128/CMR.00018-11.CrossRefPubMedGoogle Scholar
  19. 19.
    Paterlini P, Driss F, Nalpas B, Pisi E, Franco D, Berthelot P, et al. Persistence of hepatitis B and hepatitis C viral genomes in primary liver cancers from HBsAg-negative patients: a study of a low-endemic area. Hepatology. 1993;17:20–9.CrossRefPubMedGoogle Scholar
  20. 20.
    Kubo S, Kim YJ, Ohba K, Shuto T, Yamamoto T, Tanaka H, et al. Previous or occult hepatitis B virus infection in hepatitis C virus-associated hepatocellular carcinoma without hepatic fibrosis. Dig Dis Sci. 2001;46:2408–14.CrossRefPubMedGoogle Scholar
  21. 21.
    Sheu JC, Huang GT, Shih LN, Lee WC, Chou HC, Wang JT, et al. Hepatitis C and B viruses in hepatitis B surface antigen-negative hepatocellular carcinoma. Gastroenterology. 1992;103:1322–7.CrossRefPubMedGoogle Scholar
  22. 22.
    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;126:102–10.CrossRefPubMedGoogle Scholar
  23. 23.
    Squadrito G, Pollicino T, Cacciola I, Caccamo G, Villari D, La Masa T, et al. Occult hepatitis B virus infection is associated with the development of hepatocellular carcinoma in chronic hepatitis C patients. Cancer. 2006;106:1326–30.CrossRefPubMedGoogle Scholar
  24. 24.
    Coppola N, Pisapia R, Tonziello G, Martini S, Imparato M, Piai G, et al. Virological pattern in plasma, peripheral blood mononuclear cells and liver tissue and clinical outcome in chronic hepatitis B and C virus coinfection. Antivir Ther. 2008;13:307–18.PubMedGoogle Scholar
  25. 25.
    Sagnelli E, Imparato M, Coppola N, Pisapia R, Sagnelli C, Messina V, 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;80:15471553. doi:10.1002/jmv.21239.Google Scholar
  26. 26.
    Koo YX, Tay M, Teh YE, Teng D, Tan DS, Tan IB, et al. Risk of hepatitis B virus (HBV) reactivation in hepatitis B surface antigen negative/hepatitis B core antibody positive patients receiving rituximab-containing combination chemotherapy without routine antiviral prophylaxis. Ann Hematol. 2011;90:1219–23. doi:10.1007/s00277-011-1241-0.CrossRefPubMedGoogle Scholar
  27. 27.
    Liang R. How I treat and monitor viral hepatitis B infection in patients receiving intensive immunosuppressive therapies or undergoing hematopoietic stem cell transplantation. Blood. 2009;113:3147–53. doi:10.1182/blood2008-10-163493.CrossRefPubMedGoogle Scholar
  28. 28.
    Lalazar G, Rund D, Shouval D. Screening, prevention and treatment of viral hepatitis B reactivation in patients with haematological malignancies. Br J Haematol. 2007;136:699–712. doi:10.1111/j.1365-2141.2006.06465.x.CrossRefPubMedGoogle Scholar
  29. 29.
    Kusumoto S, Tanaka Y, Mizokami M, Ueda R. Reactivation of hepatitis B virus following systemic chemotherapy for malignant lymphoma. Int J Hematol. 2009;90:13–23. doi:10.1007/s12185-009-0359-5.CrossRefPubMedGoogle Scholar
  30. 30.
    Montineri A, Nigro L, La Rosa R, Iacobello C, Larocca L, Cappello E, et al. Treatment induced seroconversion to HBsAb following HBV reactivation in the immunosuppressed haematology and oncology patient: a clinical survey of 5 cases in Catania, Italy. J Clin Virol. 2011;52:284–7. doi:10.1016/j.jcv.2011.08.007.CrossRefPubMedGoogle Scholar
  31. 31.
    Marzano A, Angelucci E, Andreone P, Brunetto M, Bruno R, Burra P, et al. Prophylaxis and treatment of hepatitis B in immunocompromised patients. Dig Liver Dis. 2007;39:397–408. doi:10.1016/j.dld.2006.12.017.CrossRefPubMedGoogle Scholar
  32. 32.
    Coppola N, Tonziello G, Pisaturo M, Messina V, Guastafierro S, Fiore M, et al. Reactivation of overt and occult hepatitis B infection in various immunosuppressive settings. J Med Virol. 2011;83:1909–16. doi:10.1002/jmv.22199.CrossRefPubMedGoogle Scholar
  33. 33.
    Yeo W, Johnson PJ. Diagnosis, prevention and management of hepatitis B virus reactivation during anticancer therapy. Hepatology. 2006;43:209–20.CrossRefPubMedGoogle Scholar
  34. 34.
    Ustün C, Koç H, Karayalcin S, Akyol G, Gürman G, Ilhan O, et al. Hepatitis B virus infection in allogeneic bone marrow transplantation. Bone Marrow Transplant. 1997;20:289–96. doi:10.1038/sj.bmt.1700885.CrossRefPubMedGoogle Scholar
  35. 35.
    Lau GK, Leung YH, Fong DY, Au WY, Kwong YL, Lie A, et al. High hepatitis B virus (HBV) DNA viral load as the most important risk factor for HBV reactivation in patients positive for HBV surface antigen undergoing autologous hematopoietic cell transplantation. Blood. 2002;99:2324–30. doi:10.1182/blood.V99.7.2324.CrossRefPubMedGoogle Scholar
  36. 36.
    Ma SY, Lau GK, Cheng VC, Liang R. Hepatitis B reactivation in patients positive for hepatitis B surface antigen undergoing autologous hematopoietic cell transplantation. Leuk Lymphoma. 2003;44:1281–5. doi:10.1080/1042819031000083343.CrossRefPubMedGoogle Scholar
  37. 37.
    Knöll A, Boehm S, Hahn J, Holler E, Jilg W. Reactivation of resolved hepatitis B virus infection after allogeneic haematopoietic stem cell transplantation. Bone Marrow Transplant. 2004;33:925–9. doi:10.1038/sj.bmt.1704457.CrossRefPubMedGoogle Scholar
  38. 38.
    Hui CK, Sun J, Au WY, Lie AK, Yueng YH, Zhang HY, et al. Occult hepatitis B virus infection in hematopoietic stem cell donors in a hepatitis B virus endemic area. J Hepatol. 2005;42:813–9. doi:10.1016/j.jhep.2005.01.018.CrossRefPubMedGoogle Scholar
  39. 39.
    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;79:616–9. doi:10.1097/01.TP.0000151661.52601.FB.CrossRefPubMedGoogle Scholar
  40. 40.
    Aksoy S, Harputluoglu H, Kilickap S, Dede DS, Dizdar O, Altundag K, et al. Rituximab related viral infections in lymphoma patients. Leuk Lymphoma. 2007;48:1307–12. doi:10.1080/10428190701411441.CrossRefPubMedGoogle Scholar
  41. 41.
    Francisci D, Falcinelli F, Schiaroli E, Capponi M, Belfiori B, Flenghi L, et al. Management of hepatitis B virus reactivation in patients with hematological malignancies treated with chemotherapy. Infection. 2010;38:58–61. doi:10.1007/s15010-009-9019-1.CrossRefPubMedGoogle Scholar
  42. 42.
    Coppola N, Gentile I, Pasquale G, Buonomo AR, Capoluongo N, D’Armiento M, et al. Anti-HBc positivity was associated with histological cirrhosis in patients with chronic hepatitis C. Ann Hepatol. 2014;13:20–6.Google Scholar
  43. 43.
    Jang JY, Park EJ. Occult hepatitis B virus infection in chronic hepatitis C. Korean J Gastroenterol. 2013;62:154159.CrossRefGoogle Scholar
  44. 44.
    Mastroianni CM, Lichtner M, Citton R, Del Borgo C, Rago A, Martini H, et al. Current trends in management of hepatitis B virus reactivation in the biologic therapy era. World J Gastroenterol. 2011;17:3881–7. doi:10.3748/wjg.v17.i34.3881.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Borentain P, Colson P, Coso D, Bories E, Charbonnier A, Stoppa AM, et al. Clinical and virological factors associated with hepatitis B virus reactivation in HBsAg-negative and anti-HBc antibodies-positive patients undergoing chemotherapy and/or autologous stem cell transplantation for cancer. J Viral Hepat. 2010;17:807–15.CrossRefPubMedGoogle Scholar
  46. 46.
    Sagnelli E, Pisaturo M, Martini S, Filippini P, Sagnelli C, Coppola N. Clinical impact of occult hepatitis B virus infection in immunosuppressed patients. World J Hepatol. 2014;6:384–93. doi:10.4254/wjh.v6.i6.384.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Sagnelli E, Sagnelli C, Pisaturo M, Coppola N. Hepatic flares in chronic hepatitis C: spontaneous exacerbation vs hepatotropic viruses superinfection. World J Gastroenterol. 2014;20:6707–15. doi:10.3748/wjg.v20.i22.6707.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Harris HE, Eldridge KP, Harbour S, Alexander G, Teo CG, Ramsay ME, et al. Does the clinical outcome of hepatitis C infection vary with the infecting hepatitis C virus type? J Viral Hepat. 2007;14:213–20.CrossRefPubMedGoogle Scholar
  49. 49.
    Mason AL, Xu L, Guo L, Kuhns M, Perrillo RP. Molecular basis for persistent hepatitis B virus infection in the liver after clearance of serum hepatitis B surface antigen. Hepatology. 1998;27:1736–42.CrossRefPubMedGoogle Scholar
  50. 50.
    Pei SN, Chen CH, Lee CM, Wang MC, Ma MC, Hu TH, et al. Reactivation of hepatitis B virus following rituximab-based regimens: a serious complication in both HBsAg-positive and HBsAg-negative patients. Ann Hematol. 2010;89:255–62. doi:10.1007/s00277-009-0806-7.CrossRefPubMedGoogle Scholar
  51. 51.
    Yeo W, Chan TC, Leung NW, Lam WY, Mo FK, Chu MT, et al. Hepatitis B virus reactivation in lymphoma patients with prior resolved hepatitis B undergoing anticancer therapy with or without rituximab. J Clin Oncol. 2009;27:605611. doi:10.1200/JCO.2008.18.0182.CrossRefGoogle Scholar
  52. 52.
    Shelburne SA, Hamill RJ, Rodriguez-Barradas MC, Greenberg SB, Atmar RL, Musher DM, et al. Immune reconstitution inflammatory syndrome: emergence of a unique syndrome during highly active antiretroviral therapy. Medicine. 2002;81:213–27.CrossRefPubMedGoogle Scholar
  53. 53.
    Zerbini A, Pilli M, Boni C, Fisicaro P, Penna A, Di Vincenzo P, et al. The characteristics of the cell-mediated immune response identify different profiles of occult hepatitis B virus infection. Gastroenterology. 2008;134:1470–81. doi:10.1053/j.gastro.2008.02.017.CrossRefPubMedGoogle Scholar
  54. 54.
    Said ZN. An overview of occult hepatitis B virus infection. World J Gastroenterol. 2011;17:1927–38. doi:10.3748/wjg.v17.i15.1927.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Hollinger FB, Sood G. Occult hepatitis B virus infection: a covert operation. J Viral Hepat. 2010;17:1–15. doi:10.1111/j.1365-2893.2009.01245.x.CrossRefPubMedGoogle Scholar
  56. 56.
    Pollicino T, Raffa G, Costantino L, Lisa A, Campello C, Squadrito G, et al. Molecular and functional analysis of occult hepatitis B virus isolates from patients with hepato-cellular carcinoma. Hepatology. 2007;45:277–85.CrossRefPubMedGoogle Scholar
  57. 57.
    Huang H, Li X, Zhu J, Ye S, Zhang H, Wang W, Wu X, Peng J, Xu B, Lin Y, Cao Y, Li H, Lin S, Liu Q, Lin T. Entecavir vs lamivudine for prevention of hepatitis B virus reactivation among patients with untreated diffuse large B-cell lymphoma receiving R-CHOP chemotherapy: a randomized clinical trial. JAMA. 2014;312:2521–30. doi:10.1001/jama.2014.15704.CrossRefPubMedGoogle Scholar
  58. 58.
    Squadrito G, Spinella R, Raimondo G. The clinical significance of occult HBV infection. Ann Gastroenterol. 2014;27:15–9.PubMedPubMedCentralGoogle Scholar
  59. 59.
    European Association For The Study Of The Liver. EASL Clinical Practice Guidelines: management of chronic hepatitis B. J Hepatol. 2009;50:227–42. doi:10.1016/j.jhep.2009.02.017.CrossRefGoogle Scholar
  60. 60.
    Barclay S, Pol S, Mutimer D, Benhamou Y, Mills PR, Hayes PC, et al. The management of chronic hepatitis B in the immunocompromised patient: recommendations from a single topic meeting. J Clin Virol. 2008;41:243–54. doi:10.1016/j.jcv.2007.11.017.CrossRefPubMedGoogle Scholar
  61. 61.
    Hui CK, Cheung WW, Zhang HY, Au WY, Yueng YH, Leung AY, et al. Kinetics and risk of de novo hepatitis B infection in HBsAg-negative patients undergoing cytotoxic chemotherapy. Gastroenterology. 2006;131:59–68.CrossRefPubMedGoogle Scholar
  62. 62.
    Matsue K, Kimura S, Takanashi Y, Iwama K, Fujiwara H, Yamakura M, et al. Reactivation of hepatitis B virus after rituximab-containing treatment in patients with CD20-positive B cell lymphoma. Cancer. 2010;116:4769–76. doi:10.1002/cncr.25253.CrossRefPubMedGoogle Scholar
  63. 63.
    Cheung WI, Lin SY, Leung VKS, Fung KSC, Lam YK, Lo FH, et al. Prospective evaluation of seropositive occult hepatitis B viral infection in lymphoma patients receiving chemotherapy. Hong Kong Med J. 2011;17:376–80.PubMedGoogle Scholar
  64. 64.
    Francisci D, Falcinelli F, Schiaroli E, Capponi M, Belfiori B, Cecchini E, et al. Reactivation of hepatitis B virus replication due to cytotoxic therapy: a five-year prospective study. Tumor. 2012;98:220–4. doi:10.1700/1088.11933.Google Scholar
  65. 65.
    Masarone M, De Renzo A, La Mura V, Sasso FC, Romano M, Signoriello G, et al. Management of the HBV reactivation in isolated HBcAb positive patients affected with non Hodgkin lymphoma. BMC Gastroenterol. 2014;14:31–40. doi:10.1186/1471-230X-14-31.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Elkady GA, Aboulfotuh S, Ali EM, Sayed D, Abdel-Aziz NM, Ali AM, et al. Incidence and characteristics of HBV reactivation in hematological malignant patients in south Egypt. World J Gastroenterol. 2013;19:6214–20. doi:10.3748/wjg.v19.i37.6214.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Zachou K, Sarantopoulos A, Gatselis NK, Vassiliadis T, Gabeta S, Stefos A, et al. Hepatitis B virus reactivation in hepatitis B virus surface antigen negative patients receiving immunosuppression: a hidden threat. World J Hepatol. 2013;5:387–92. doi:10.4254/wjh.v5.i7.387.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Hsu C, Tsou HH, Lin SJ, Wang MC, Yao M, Hwang WL, et al. Chemotherapy-induced hepatitis B reactivation in lymphoma patients with resolved HBV infection: a prospective study. Hepatology. 2014;59:2092–100.CrossRefPubMedGoogle Scholar
  69. 69.
    Lok AS, McMahon BJ. Chronic hepatitis B. Hepatology. 2007;45:507–39.CrossRefPubMedGoogle Scholar
  70. 70.
    Dong HJ, Ni LN, Sheng GF, Song HL, Xu JZ, Ling Y. Risk of hepatitis B virus (HBV) reactivation in non-Hodgkin lymphoma patients receiving rituximab-chemotherapy: a meta analysis. J ClinVirol. 2013;57:209–14. doi:10.1016/j.jcv.2013.03.010.Google Scholar
  71. 71.
    Baginski I, Chemin I, Hantz O, Pichoud C, Jullien AM, Chevre JC, et al. Transmission of serologically silent hepatitis B virus along with hepatitis C virus in two cases of post transfusion hepatitis. Transfusion. 1992;32:215–20. doi:10.1046/j.1537-2995.1992.32392213803.x.CrossRefPubMedGoogle Scholar
  72. 72.
    Liu WP, Zheng W, Song YQ, Ping LY, Wang GQ, Zhu J. Hepatitis B surface antigen seroconversion after HBV reactivation in non-Hodgkin’s lymphoma. World J Gastroenterol. 2014;20:5165–70. doi:10.3748/wjg.v20.i17.5165.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Tonziello G, Pisaturo M, Sica A, Ferrara MG, Sagnelli C, Pasquale G, et al. Transient reactivation of occult hepatitis B virus infection despite lamivudine prophylaxis in a patient treated for non-Hodgkin lymphoma. Infection. 2013;41(1):225–9. doi:10.1007/s15010-012-0305-y.CrossRefPubMedGoogle Scholar
  74. 74.
    Garcia-Rodriguez MJ, Canales MA, Hernandez-Maraver D, Hernandez-Navarro F. Late reactivation of resolved hepatitis B virus infection: an increasing complication post rituximab based regimens treatment? Am J Hematol. 2008;83:673–5. doi:10.1002/ajh.21214.CrossRefPubMedGoogle Scholar
  75. 75.
    Zingarelli S, Frassi M, Bazzani C, Scarsi M, Puoti M, Airò P. Use of tumor necrosis factor-alpha-blocking agents in hepatitis B virus-positive patients: reports of 3 cases and review of the literature. J Rheumatol. 2009;36:1188–94. doi:10.3899/jrheum.081246.CrossRefPubMedGoogle Scholar
  76. 76.
    Tamori A, Koike T, Goto H, Wakitani S, Tada M, Morikawa H, Enomoto M, Inaba M, Nakatani T, Hino M, Kawada N. Prospective study of reactivation of hepatitis B virus in patients with rheumatoid arthritis who received immunosuppressive therapy: evaluation of both HBsAg-positive and HBsAg-negative cohorts. J Gastroenterol. 2011;46:556–64.CrossRefPubMedGoogle Scholar
  77. 77.
    Kim YJ, Bae SC, Sung YK, Kim TH, Jun JB, Yoo DH, Kim TY, Sohn JH, Lee HS. Possible reactivation of potential hepatitis B virus occult infection by tumor necrosis factor-alpha blocker in the treatment of rheumatic diseases. J Rheumatol. 2010;37:346–50. doi:10.3899/jrheum.090436.CrossRefPubMedGoogle Scholar
  78. 78.
    Lee YH, Bae SC, Song GG. Hepatitis B virus (HBV) reactivation in rheumatic patients with hepatitis core antigen (HBV occult carriers) undergoing anti-tumor necrosis factor therapy. Clin Exp Rheumatol. 2013;31:118–21.PubMedGoogle Scholar
  79. 79.
    Nathan DM, Angus PW, Gibson PR. Hepatitis B and C virus infections and anti-tumor necrosis factor-alpha therapy: guidelines for clinical approach. J Gastroenterol Hepatol. 2006;21:1366–71. doi:10.1111/j.1440-1746.2006.04559.x.CrossRefPubMedGoogle Scholar
  80. 80.
    Biondo MI, Germano V, Pietrosanti M, Canzoni M, Marignani M, Stroffolini T, Salemi S, D’Amelio R. Lack of hepatitis B virus reactivation after anti-tumour necrosis factor treatment in potential occult carriers with chronic inflammatory arthropathies. Eur J Intern Med. 2014;25:482–4. doi:10.1016/j.ejim.2013.11.014.CrossRefPubMedGoogle Scholar
  81. 81.
    Morisco F, Guarino M, La Bella S, Di Costanzo L, Caporaso N, Ayala F, Balato N. Lack of evidence of viral reactivation in HBsAg-negative HBcAb-positive and HCV patients undergoing immunosuppressive therapy for psoriasis. BMC Gastroenterol. 2014;14:214. doi:10.1186/s12876-014-0214-x.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Lampertico P, Maini M, Papatheodoridis G. Optimal management of hepatitis B virus infection—EASL Special Conference. J Hepatol. 2015;63:1238–53. doi:10.1016/j.jhep.2015.06.026.CrossRefPubMedGoogle Scholar
  83. 83.
    Coppola N, Sagnelli C, Pisaturo M, Minichini C, Messina V, Alessio L, et al. Clinical and virological characteristics associated with severe acute hepatitis B. Clin Microbiol Infect. 2014;20:O991–7. doi:10.1111/1469-0691.12720.CrossRefPubMedGoogle Scholar
  84. 84.
    Sagnelli C, Ciccozzi M, Pisaturo M, Zehender G, Lo Presti A, Alessio L, et al. Molecular epidemiology of hepatitis B virus genotypes circulating in acute hepatitis B patients in the Campania region. J Med Virol. 2014;86:1683–93. doi:10.1002/jmv.24005.CrossRefPubMedGoogle Scholar
  85. 85.
    Coppola N, Masiello A, Tonziello G, Pisapia R, Pisaturo M, Sagnelli C, et al. Factors affecting the changes in molecular epidemiology of acute hepatitis B in a Southern Italian area. J Viral Hepat. 2010;17:493–500. doi:10.1111/j.1365-2893.2009.01201.x.PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • C. Sagnelli
    • 1
  • M. Macera
    • 2
  • M. Pisaturo
    • 3
  • R. Zampino
    • 4
  • M. Coppola
    • 5
  • E. Sagnelli
    • 5
  1. 1.Department of Clinical and Experimental Medicine and Surgery “F. Magrassi e A. Lanzara”Second University of NaplesNaplesItaly
  2. 2.Azienda Ospedaliera Universitaria-Second University of NaplesNaplesItaly
  3. 3.Division of Infectious DiseasesAORN Sant’Anna e San Sebastiano di CasertaCasertaItaly
  4. 4.Department of Medical, Surgical, Neurological, Metabolic and Geriatric SciencesSecond University of NaplesNaplesItaly
  5. 5.Section of Infectious Diseases, Department of Mental Health and Public MedicineSecond University of NaplesNaplesItaly

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