Abstract
Several reports recently found that patients with B cell non-Hodgkin’s lymphoma (NHL) had a higher carrier rate of hepatitis B surface antigen (HBsAg). The current study aimed to examine the hepatitis B virus (HBV) infection status of NHL patients in Taiwan, an HBV-endemic area. Serum HBV and serum hepatitis C virus were measured in 471 NHL patients and 1,013 non-lymphoma cancer patients enrolled between February 2000 and March 2007. Furthermore, nested polymerase chain reaction of HBV-DNA was used to examine the sera from selected patients in these two populations and healthy volunteers for the presence of occult HBV infection. The infection rates (as indicated by the rates of HBsAg and occult HBV) were compared between different groups. There was a higher incidence of HBV infection in B cell NHL patients (23.5%), especially patients with diffuse large B lymphoma, than solid tumor patients (15.6%, P = 0.001). Among HbsAg-negative patients, those with B cell NHL had a higher prevalence of occult HBV infection (6%) than those with non-lymphoma solid tumors and healthy volunteers, 0% and 0.9%, respectively (P = 0.005). B cell NHL patients, even HBsAg-negative B cell NHL patients, but not T cell NHL patients, have a higher incidence of HBV infection than patients with solid tumors. Our findings support the etiologic role of HBV infection in B cell NHL.
Similar content being viewed by others
References
Chuang WL, Chang WY, Lu SN, Su WP, Lin ZY, Chen SC, Hsieh MY, Wang LY, You SL, Chen CJ (1992) The role of hepatitis B and C viruses in hepatocellular carcinoma in a hepatitis B endemic area. A case-control study. Cancer 69:2052–2054
Beasley RP (1988) Hepatitis B virus. The major etiology of hepatocellular carcinoma. Cancer 61:1942–1956
Tsukuma H, Hiyama T, Tanaka S, Nakao M, Yabuuchi T, Kitamura T, Nakanishi K, Fujimoto I, Inoue A, Yamazaki H et al. (1993) Risk factors for hepatocellular carcinoma among patients with chronic liver disease. N Engl J Med 328:1797–1801
Ferri C, Monti M, La Civita L, Longombardo G, Greco F, Pasero G, Gentilini P, Bombardieri S, Zignego AL (1993) Infection of peripheral blood mononuclear cells by hepatitis C virus in mixed cryoglobulinemia. Blood 82:3701–3704
Pasquinelli C, Laure F, Chatenoud L, Beaurin G, Gazengel C, Bismuth H, Degos F, Tiollais P, Bach JF, Brechot C (1986) Hepatitis B virus DNA in mononuclear blood cells. A frequent event in hepatitis B surface antigen-positive and -negative patients with acute and chronic liver disease. J Hepatol 3:95–103
De Vita S, Sacco C, Sansonno D, Gloghini A, Dammacco F, Crovatto M, Santini G, Dolcetti R, Boiocchi M, Carbone A, Zagonel V (1997) Characterization of overt B-cell lymphomas in patients with hepatitis C virus infection. Blood 90:776–782
Giordano TP, Henderson L, Landgren O, Chiao EY, Kramer JR, El-Serag H, Engels EA (2007) Risk of non-Hodgkin lymphoma and lymphoproliferative precursor diseases in US veterans with hepatitis C virus. JAMA 297:2010–2017
Wang F, Xu RH, Han B, Shi YX, Luo HY, Jiang WQ, Lin TY, Huang HQ, Xia ZJ, Guan ZZ (2007) High incidence of hepatitis B virus infection in B-cell subtype non-Hodgkin lymphoma compared with other cancers. Cancer 109:1360–1364
Marcucci F, Mele A, Spada E, Candido A, Bianco E, Pulsoni A, Chionne P, Madonna E, Cotichini R, Barbui A, De Renzo A, Dore F, Iannitto E, Liso V, Martino B, Montanaro M, Pagano L, Musto P, Rapicetta M (2006) High prevalence of hepatitis B virus infection in B-cell non-Hodgkin’s lymphoma. Haematologica 91:554–557
Takai S, Tsurumi H, Ando K, Kasahara S, Sawada M, Yamada T, Hara T, Fukuno K, Takahashi T, Oyama M, Onishi H, Tomita E, Takami T, Imawari M, Moriwaki H (2005) Prevalence of hepatitis B and C virus infection in haematological malignancies and liver injury following chemotherapy. Eur J Haematol 74:158–165
Cucuianu A, Patiu M, Duma M, Basarab C, Soritau O, Bojan A, Vasilache A, Mates M, Petrov L (1999) Hepatitis B and C virus infection in Romanian non-Hodgkin’s lymphoma patients. Br J Haematol 107:353–356
Kim JH, Bang YJ, Park BJ, Yoo T, Kim CW, Kim TY, Heo DS, Lee HS, Kim NK (2002) Hepatitis B virus infection and B-cell non-Hodgkin’s lymphoma in a hepatitis B endemic area: a case-control study. Jpn J Cancer Res 93:471–477
Brechot C, Thiers V, Kremsdorf D, Nalpas B, Pol S, Paterlini-Brechot P (2001) Persistent hepatitis B virus infection in subjects without hepatitis B surface antigen: clinically significant or purely “occult”? Hepatology 34:194–203
Cacciola I, Pollicino T, Squadrito G, Cerenzia G, Orlando ME, Raimondo G (1999) Occult hepatitis B virus infection in patients with chronic hepatitis C liver disease. N Engl J Med 341:22–26
Pollicino T, Squadrito G, Cerenzia G, Cacciola I, Raffa G, Craxi A, Farinati F, Missale G, Smedile A, Tiribelli C, Villa E, Raimondo G (2004) Hepatitis B virus maintains its pro-oncogenic properties in the case of occult HBV infection. Gastroenterology 126:102–110
Torbenson M, Thomas DL (2002) Occult hepatitis B. Lancet Infect Dis 2:479–486
Conjeevaram HS, Lok AS (2001) Occult hepatitis B virus infection: a hidden menace? Hepatology 34:204–206
Raimondo G, Pollicino T, Cacciola I, Squadrito G (2007) Occult hepatitis B virus infection. J Hepatol 46:160–170
Filippini P, Coppola N, Pisapia R, Scolastico C, Marrocco C, Zaccariello A, Nacca C, Sagnelli C, De Stefano G, Ferraro T, De Stefano C, Sagnelli E (2006) Impact of occult hepatitis B virus infection in HIV patients naive for antiretroviral therapy. AIDS 20:1253–1260
Mphahlele MJ, Lukhwareni A, Burnett RJ, Moropeng LM, Ngobeni JM (2006) High risk of occult hepatitis B virus infection in HIV-positive patients from South Africa. J Clin Virol 35:14–20
Wagner AA, Denis F, Weinbreck P, Loustaud V, Autofage F, Rogez S, Alain S (2004) Serological pattern ‘anti-hepatitis B core alone’ in HIV or hepatitis C virus-infected patients is not fully explained by hepatitis B surface antigen mutants. AIDS 18:569–571
Chemin I, Trepo C (2005) Clinical impact of occult HBV infections. J Clin Virol 34 1:15–21
Torbenson M, Kannangai R, Astemborski J, Strathdee SA, Vlahov D, Thomas DL (2004) High prevalence of occult hepatitis B in Baltimore injection drug users. Hepatology 39:51–57
Toyoda H, Hayashi K, Murakami Y, Honda T, Katano Y, Nakano I, Goto H, Kumada T, Takamatsu J (2004) Prevalence and clinical implications of occult hepatitis B viral infection in hemophilia patients in Japan. J Med Virol 73:195–199
Minuk GY, Sun DF, Greenberg R, Zhang M, Hawkins K, Uhanova J, Gutkin A, Bernstein K, Giulivi A, Osiowy C (2004) Occult hepatitis B virus infection in a North American adult hemodialysis patient population. Hepatology 40:1072–1077
Siagris D, Christofidou M, Triga K, Pagoni N, Theocharis GJ, Goumenos D, Lekkou A, Thomopoulos K, Tsamandas AC, Vlachojannis J, Labropoulou-Karatza C (2006) Occult hepatitis B virus infection in hemodialysis patients with chronic HCV infection. J Nephrol 19:327–333
Jaffe ES, Harris NL, Stein H, Vardiman JW (2001) WHO classification tumours of haematopoietic and lymphoid tissues. IARC, Lyon, France
Hui CK, Sun J, Au WY, Lie AK, Yueng YH, Zhang HY, Lee NP, Hou JL, Liang R, Lau GK (2005) Occult hepatitis B virus infection in hematopoietic stem cell donors in a hepatitis B virus endemic area. J Hepatol 42:813–819
Paraskevis D, Haida C, Tassopoulos N, Raptopoulou M, Tsantoulas D, Papachristou H, Sypsa V, Hatzakis A (2002) Development and assessment of a novel real-time PCR assay for quantitation of HBV DNA. J Virol Methods 103:201–212
Chen IL, Lu SN, Wu CL (1999) HBsAg and Anti-HCV prevalence among villages in an endemic township: a community study in Tzukuan, Kaohsiung. Taiwan J Public Health 18:313–318
Lai SW, Ng KC, Li CI (2004) Descriptive analysis of HBsAg and HCV antibody prevalence in patients receiving health check-ups: a hospital-based study. Mid Taiwan J Med 9:64–69
Minuk GY, Sun DF, Uhanova J, Zhang M, Caouette S, Nicolle LE, Gutkin A, Doucette K, Martin B, Giulivi A (2005) Occult hepatitis B virus infection in a North American community-based population. J Hepatol 42:480–485
Chen CJ (2005) Time-dependent events in natural history of occult hepatitis B virus infection: the importance of population-based long-term follow-up study with repeated measurements. J Hepatol 42:438–440
Pozzato G, Mazzaro C, Crovatto M, Modolo ML, Ceselli S, Mazzi G, Sulfaro S, Franzin F, Tulissi P, Moretti M et al. (1994) Low-grade malignant lymphoma, hepatitis C virus infection, and mixed cryoglobulinemia. Blood 84:3047–3053
Kawatani T, Suou T, Tajima F, Ishiga K, Omura H, Endo A, Ohmura H, Ikuta Y, Idobe Y, Kawasaki H (2001) Incidence of hepatitis virus infection and severe liver dysfunction in patients receiving chemotherapy for hematologic malignancies. Eur J Haematol 67:45–50
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
Acknowledgments
We thank Ms. Shu-Chou Chaou and Ms. Chia-Min Shih for performing the laboratory analyses of HBV and HCV markers and Ms. Pui-Ching Lee for statistical analysis. The study was supported by the grants from Taiwan Cancer Clinic Foundation, Taipei Veterans General Hospital (VGH93-192 and 94-236 for PMC, and 96B2-012 for LTH) and National Science Council (NSC), Taiwan (NSC94-2314-B075-049 for PMC, and NSC95-2745-B-075-008 & 96-2321-B-075-008 for LTH).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Chen, MH., Hsiao, LT., Chiou, TJ. et al. High prevalence of occult hepatitis B virus infection in patients with B cell non-Hodgkin’s lymphoma. Ann Hematol 87, 475–480 (2008). https://doi.org/10.1007/s00277-008-0469-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00277-008-0469-9