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Japanese Journal of Cancer Research : Gann logoLink to Japanese Journal of Cancer Research : Gann
. 2002 May;93(5):471–477. doi: 10.1111/j.1349-7006.2002.tb01280.x

Hepatitis B Virus Infection and B‐Cell Non‐Hodgkin's Lymphoma in a Hepatitis B Endemic Area: A Case‐control Study

Jee Hyun Kim 1, Yung‐Jue Bang 1,2,, Byung Joo Park 3, Taiwoo Yoo 4, Chul Woo Kim 2,5, Tae‐You Kim 1,2, Dae Seog Heo 1,2, Hyo‐Suk Lee 1,6, Noe Kyeong Kim 1
PMCID: PMC5927034  PMID: 12036441

Abstract

Several studies have reported a higher prevalence of chronic hepatitis C virus (HCV) infection in patients with B‐cell non‐Hodgkin's lymphoma and suggested a pathogenic role for HCV, but studies on hepatitis B virus (HBV) infection and non‐Hodgkin's lymphoma are limited. To determine the association between HBV infection and non‐Hodgkin's lymphoma, we performed a case‐control study in Korea, a hepatitis B endemic area. We recruited 222 patients newly diagnosed with non‐Hodgkin's lymphoma at Seoul National University Hospital between January 1997 and December 1998 as cases. Four age‐ and sex‐matched controls were selected for each case, and the control groups comprised of 439 patients with non‐hematological malignancy (control group 1) and 444 subjects with non‐malignant conditions (control group 2). Relative risk of developing non‐Hodgkin's lymphoma among individuals tested positive for hepatitis B surface antigen was calculated after controlling for other potential risk factors of lymphoma, such as smoking, alcohol drinking, transfusion history and HCV infection. Hepatitis B surface antigen was positive in 28 of 222 patients (12.6%) with non‐Hodgkin's lymphoma compared with 32 of 439 (7.3%) in control group 1, and 21 of 444 (4.7%) in control group 2 (P=0.001). The crude odds ratio for B‐cell non‐Hodgkin's lymphoma among the HBV carriers was 2.54 (1.46–4.45) and the adjusted odds ratio was 3.30 (1.69–6.45) by multivariate analysis. The present study suggests that the risk of B‐cell non‐Hodgkin's lymphoma is increased in HBV carriers and warrants further investigation of the possible role of hepatitis B virus in the pathogenesis of B‐cell non‐Hodgkin's lymphoma.

Keywords: Case‐control study, Non‐Hodgkin's lymphoma, Hepatitis B, Risk factor

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REFERENCES

  • 1. ) Devesa , S. S. and Fears , T.Non‐Hodgkin's lymphoma time trends: United States and international data . Cancer Res. , 52 ( Suppl ), 5432s – 5440s ( 1992. ). [PubMed] [Google Scholar]
  • 2. ) Ferri , C. , Caracciolo , F. , Zignego , A. L. , La Civita , L. , Monti , M. , Longombardo , G. , Greco , F. and Capochiani , E.Hepatitis C virus infection in patients with non‐Hodgkin's lymphoma . Br. J. Haematol. , 88 , 392 – 394 ( 1994. ). [DOI] [PubMed] [Google Scholar]
  • 3. ) Silvestri , F. , Pipan , C. , Barillari , G. , Zaja , F. , Fanin , R. , Infanti , L. , Russo , D. , Falasca , E. , Botta , G. A. and Baccarani , M.Prevalence of hepatitis C virus infection in patients with lymphoproliferative disorders . Blood , 87 , 4296 – 4301 ( 1996. ). [PubMed] [Google Scholar]
  • 4. ) Zuckerman , E. , Zuckerman , T. , Levine , A. M. , Douer , D. , Gutekunst , K. , Mizokami , M. , Qian , D. G. , Velankar , M. , Nathwani , B. N. and Fong , T.‐L.Hepatitis C virus infection in patients with B‐cell non‐Hodgkin's lymphoma . Ann. Intern. Med , 127 , 423 – 428 ( 1997. ). [DOI] [PubMed] [Google Scholar]
  • 5. ) Ferri , C. , Monti , M. , La Civita , L. , Longombardo , G. , Greco , F. , Pasero , G. , Gentilini , P. , Bombardieri , S. and Zignego , A. L.Infection of peripheral blood mononuclear cells by hepatitis C virus in mixed cryoglobulinemia . Blood , 82 , 3701 – 3704 ( 1993. ). [PubMed] [Google Scholar]
  • 6. ) Yoffe , B. , Burns , D. K. , Bhatt , H. S. and Combes , B.Extrahepatic hepatitis B virus DNA sequences in patients with acute hepatitis B infection . Hepatology , 12 , 187 – 192 ( 1990. ). [DOI] [PubMed] [Google Scholar]
  • 7. ) Mason , A. , Wick , M. , White , H. and Perrillo , R.Hepatitis B virus replication in diverse cell types during chronic hepatitis B virus infection . Hepatology , 18 , 781 – 789 ( 1993. ). [DOI] [PubMed] [Google Scholar]
  • 8. ) Stoll‐Becker , S. , Repp , R. , Glebe , D. , Schaefer , S. , Kreuder , J. , Kann , M. , Lampert , F. and Gerlich , W. H.Transcription of hepatitis B virus in peripheral blood mononuclear cells from persistently infected patients . J. Virol. , 71 , 5399 – 5407 ( 1997. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9. ) Liang , R. H. S. , Lok , A. S. F. , Lai , C. L. , Chan , T. K. , Todd , D. and Chiu , E. K. W.Hepatitis B infection in patients with lymphomas . Hematol. Oncol. , 8 , 261 – 270 ( 1990. ). [DOI] [PubMed] [Google Scholar]
  • 10. ) Lok , A. S. F. , Liang , R. H. S. , Chiu , E. K. W. , Wong , K. L. , Chan , T. K. and Todd , D.Reactivation of hepatitis B virus replication in patients receiving cytotoxic therapy. Report of a prospective study . Gastroenterology , 100 , 182 – 188 ( 1991. ). [DOI] [PubMed] [Google Scholar]
  • 11. ) Kumagai , K. , Takagi , T. , Nakamura , S. , Sawada , U. , Kura , Y. , Kodama , F. , Shimano , S. , Kudoh , I. , Nakamura , H. , Sawada , K. and Ohnoshi , T.Hepatitis B virus carriers in the treatment of malignant lymphoma: an epidemiological study in Japan . Ann. Oncol. , 8 ( Suppl. 1 ), S107 – S109 ( 1997. ). [PubMed] [Google Scholar]
  • 12. ) Markovic , S. , Drozina , G. , Vovk , M. and Fidler‐Jenko , M.Reactivation of hepatitis B but not hepatitis C in patients with malignant lymphoma and immunosuppressive therapy. A prospective study in 305 patients . Hepatogastroenterology , 46 , 2925 – 2930 ( 1999. ). [PubMed] [Google Scholar]
  • 13. ) Cucuianu , A. , Patiu , M. , Duma , M. , Basarab , C. , Soritau , O. , Bojan , A. , Vasilache , A. , Mates , M. and Petrov , L.Hepatitis B and C virus infection in Romanian non‐Hodgkin's lymphoma patients . Br. J. Haematol. , 107 , 353 – 356 ( 1999. ). [DOI] [PubMed] [Google Scholar]
  • 14. ) Kuniyoshi , M. , Nakamuta , M. , Sakai , H. , Enjoji , M. , Kinukawa , N. , Kotoh , K. , Fukutomi , M. , Yokota , M. , Nishi , H. , Iwamoto , H. , Uike , N. , Nishimura , J. , Inaba , S. , Maeda , Y. , Nawata , H. and Muta , K.Hepatitis B or C virus infections and non‐Hodgkin's lymphoma . J. Gastroenterol. Hepatol. , 16 , 215 – 219 ( 2001. ). [DOI] [PubMed] [Google Scholar]
  • 15. ) Ann , Y. O. , Kim , Y. S. , Lee , M. S. and Shin , M. H.Hepatitis B virus infection rate among Koreans . Seoul J. Med. , 33 , 105 – 114 ( 1992. ). [Google Scholar]
  • 16. ) Kim , Y. S. , Pai , C. H. , Chi , H. S. , Kim , D. W. , Min , Y. I. and Ann , Y. O.Prevalence of hepatitis C virus antibody among Korean adults . J. Kor. Med. Sci. , 7 , 333 – 336 ( 1992. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17. ) The Non‐Hodgkin's Lymphoma Pathologic Classification Project . National Cancer Institute sponsored study of classifications of non‐Hodgkin's lymphomas: summary and description of a working formulation for clinical usage . Cancer , 49 , 2112 – 2135 ( 1992. ). [DOI] [PubMed] [Google Scholar]
  • 18. ) Pontisso , P. , Poon , M. C. , Tiollais , P. and Brechot , C.Detection of hepatitis B virus DNA in mononuclear blood cells . Br. Med. J. , 288 , 1563 – 1566 ( 1984. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19. ) Yoffe , B. , Noonan , C. A. , Melnick , J. L. and Hollinger , F. B.Hepatitis B virus DNA in mononuclear cells and analysis of cell subsets for the presence of replicative intermediates of viral DNA . J. Infect. Dis. , 153 , 471 – 477 ( 1986. ). [DOI] [PubMed] [Google Scholar]
  • 20. ) Galun , E. , Ilan , Y. , Livni , N. , Ketzinel , M. , Nahor , O. , Pizov , G. , Nagler , A. , Fid , A. , Rivkind , A. , Laster , M. , Ron , N. , Blum , H. E. and Shouval , D.Hepatitis B virus infection associated with hematopoietic tumors . Am. J. Pathol. , 145 , 1001 – 1007 ( 1994. ). [PMC free article] [PubMed] [Google Scholar]
  • 21. ) Hausen , H. Z.Viruses in human cancers . Science , 254 , 1167 – 1173 ( 1991. ). [DOI] [PubMed] [Google Scholar]
  • 22. ) Nagington , J. , Cossart , Y. E. and Cohen , B. J.Reactivation of hepatitis B after transplantation operations . Lancet , i , 558 – 560 ( 1977. ). [DOI] [PubMed] [Google Scholar]
  • 23. ) Blanpain , C. , Knoop , C. , Delforge , M. L. , Antoine , M. , Peny , M. O. , Liesnard , C. , Vereerstraeten , P. , Cogan , E. , Adler , M. and Abramowicz , D.Reactivation of hepatitis B after transplantation in patients with pre‐existing anti‐hepatitis B surface antigen antibodies: report on three cases and review of the literature . Transplantation , 66 , 883 – 886 ( 1998. ). [DOI] [PubMed] [Google Scholar]
  • 24. ) Kane , M.Global programme for control of hepatitis B infection . Vaccine , 13 ( Suppl. 1 ), S47 – S49 ( 1995. ). [DOI] [PubMed] [Google Scholar]
  • 25. ) Chen , D.‐S.Natural history of chronic hepatitis B virus infection: new light on an old story . J. Gastroenterol. Hepatol. , 8 , 470 – 475 ( 1993. ). [DOI] [PubMed] [Google Scholar]

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