Indolent B-cell lymphomas associated with HCV infection: clinical and virological features and role of antiviral therapy

Luca Arcaini, Michele Merli, Stefano Volpetti, Sara Rattotti, Manuel Gotti, Francesco Zaja, Luca Arcaini, Michele Merli, Stefano Volpetti, Sara Rattotti, Manuel Gotti, Francesco Zaja

Abstract

The association between hepatitis C virus (HCV) infection and B-cell non-Hodgkin's lymphomas (NHL) has been demonstrated by epidemiological studies, in particular in highly endemic geographical areas such as Italy, Japan, and southern parts of United States. In these countries, together with diffuse large B-cell lymphomas, marginal zone lymphomas are the histotypes most frequently associated with HCV infection; in Italy around 20-30% cases of marginal zone lymphomas are HCV positive. Recently, antiviral treatment with interferon with or without ribavirin has been proved to be effective in the treatment of HCV-positive patients affected by indolent lymphoma, prevalently of marginal zone origin. An increasing number of experiences confirmed the validity of this approach in marginal zone lymphomas and in other indolent NHL subtypes like lymphoplasmacytic lymphoma. Across different studies, overall response rate was approximately 75%. Hematological responses resulted significantly associated with the eradication of the virus. This is the strongest evidence of a causative link between HCV and lymphomas. The aim of this paper is to illustrate the relationship between HCV infection and different subtypes of indolent B-cell lymphomas and to systematically summarize the data from the therapeutic studies that reported the use of antiviral treatment as hematological therapy in patients with HCV-associated indolent lymphomas.

References

    1. Gribben JG. How I treat indolent lymphoma. Blood. 2007;109(11):4617–4626.
    1. Isaacson PG, Piris MA, Berger F, et al. Splenic B-cell marginal zone lymphoma. In: Swerdlow S, Campo E, Harris NL, et al., editors. WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues. 4th edition. Lyon, France: IARC Press; 2008. pp. 218–219.
    1. Marcucci F, Mele A. Hepatitis viruses and non-Hodgkin lymphoma: epidemiology, mechanisms of tumorigenesis, and therapeutic opportunities. Blood. 2011;117(6):1792–1798.
    1. Suarez F, Lortholary O, Hermine O, Lecuit M. Infection-associated lymphomas derived from marginal zone B cells: a model of antigen-driven lymphoproliferation. Blood. 2006;107(8):3034–3044.
    1. Hermine O, Lefrère F, Bronowicki JP, et al. Regression of splenic lymphoma with villous lymphocytes after treatment of hepatitis C virus infection. New England Journal of Medicine. 2002;347(2):89–94.
    1. Poordad F, McCone J, Jr., Bacon BR, et al. Boceprevir for untreated chronic HCV genotype 1 infection. New England Journal of Medicine. 2011;364(13):1195–1206.
    1. Hézode C, Forestier N, Dusheiko G, et al. Telaprevir and peginterferon with or without ribavirin for chronic HCV infection. New England Journal of Medicine. 2009;360(18):1839–1850.
    1. Agnello V, Chung RT, Kaplan LM. A role for hepatitis C virus infection in Type II cryoglobulinemia. New England Journal of Medicine. 1992;327(21):1490–1495.
    1. Agnello V, Zhang QX, Abel G, Knight GB. The association of hepatitis C virus infection with monoclonal rheumatoid factors bearing the WA cross-idiotype: implications for the etiopathogenesis and therapy of mixed cryoglobulinemia. Clinical and Experimental Rheumatology. 1995;13(supplement 13):S-101–S-104.
    1. Ferri C, Zignego AL, Pileri SA. Cryoglobulins. Journal of Clinical Pathology. 2002;55(1):4–13.
    1. Monti G, Pioltelli P, Saccardo F, et al. Incidence and characteristics of non-Hodgkin lymphomas in a multicenter case file of patients with hepatitis C virus-related symptomatic mixed cryoglobulinemias. Archives of Internal Medicine. 2005;165(1):101–105.
    1. Zignego AL, Giannelli F, Marrocchi ME, et al. Frequency of bcl-2 rearrangement in patients with mixed cryoglobulinemia and HCV-positive liver diseases. Clinical and Experimental Rheumatology. 1997;15(6):711–712.
    1. Mazzaro C, Monti G, Saccardo F, et al. Efficacy and safety of peginterferon alfa-2b plus ribavirin for HCV-positive mixed cryoglobulinemia: a multicentre open-label study. Clinical and Experimental Rheumatology. 2011;29(6):933–941.
    1. Saadoun D, Rigon MR, Sene D, et al. Rituximab plus Peg-interferon-α/ribavirin compared with Peg-interferon-α/ribavirin in hepatitis C-related mixed cryoglobulinemia. Blood. 2010;116(3):326–334.
    1. Dammacco F, Tucci FA, Lauletta G, et al. Pegylated interferon-α, ribavirin, and rituximab combined therapy of hepatitis C virus-related mixed cryoglobulinemia: a long-term study. Blood. 2010;116(3):343–353.
    1. Arcaini L, Lazzarino M, Colombo N, et al. Splenic marginal zone lymphoma: a prognostic model for clinical use. Blood. 2006;107(12):4643–4649.
    1. Saadoun D, Suarez F, Lefrere F, et al. Splenic lymphoma with villous lymphocytes, associated with type II cryoglobulinemia and HCV infection: a new entity? Blood. 2005;105(1):74–76.
    1. Arcaini L, Paulli M, Burcheri S, et al. Primary nodal marginal zone B-cell lymphoma: clinical features and prognostic assessment of a rare disease. British Journal of Haematology. 2007;136(2):301–304.
    1. Arcaini L, Burcheri S, Rossi A, et al. Nongastric marginal-zone B-cell MALT lymphoma: prognostic value of disease dissemination. Oncologist. 2006;11(3):285–291.
    1. Ferreri AJM, Viale E, Guidoboni M, et al. Clinical implications of hepatitis C virus infection in MALT-type lymphoma of the ocular adnexa. Annals of Oncology. 2006;17(5):769–772.
    1. Paulli M, Arcaini L, Lucioni M, et al. Subcutaneous ’lipoma-like’ B-cell lymphoma associated with HCV infection: a new presentation of primary extranodal marginal zone B-cell lymphoma of MALT. Annals of Oncology. 2009;21(6):1189–1195.
    1. Tedeschi A, Vismara E, Varettoni M, et al. Clinical and biological implications of hepatitis C virus positivity in waldenstrom's macroglobulinemia patients. Proceedings of the ASH Annual Meeting Abstracts; 2009; p. p. 2934.
    1. Arcaini L, Varettoni M, Boveri E, et al. Distinctive clinical and histological features of Waldenström’s macroglobulinemia and splenic marginal zone lymphoma. Clinical Lymphoma, Myeloma and Leukemia. 2011;11(1):103–105.
    1. Goldaniga MC, Ferrario A, Cortelazzo S, et al. A multicenter retrospective clinical study of CD5/CD10-negative chronic B cell leukemias. American Journal of Hematology. 2008;83(5):349–354.
    1. Wasley A, Alter MJ. Epidemiology of hepatitis C: geographic differences and temporal trends. Seminars in Liver Disease. 2000;20(1):1–16.
    1. Shepard CW, Finelli L, Alter MJ. Global epidemiology of hepatitis C virus infection. The Lancet Infectious Diseases. 2005;5(9):558–567.
    1. Talamini R, Montella M, Crovatto M, et al. Non-Hodgkin’s lymphoma and hepatitis C virus: a case-control study from northern and southern Italy. International Journal of Cancer. 2004;110(3):380–385.
    1. Collier JD, Zanke B, Moore M, et al. No association between hepatitis C and B-cell lymphoma. Hepatology. 1999;29(4):1259–1261.
    1. Gisbert JP, García-Buey L, Pajares MJ, Moreno-Otero R. Prevalence of hepatitis C virus infection in B-cell non-hodgkin’s lymphoma: systematic, review and meta-analysis. Gastroenterology. 2003;125(6):1723–1732.
    1. Nieters A, Kallinowski B, Brennan P, et al. Hepatitis C and risk of lymphoma: results of the European multicenter case-control study EPILYMPH. Gastroenterology. 2006;131(6):1879–1886.
    1. De Sanjose S, Benavente Y, Vajdic CM, et al. Hepatitis C and non-hodgkin lymphoma among 4784 cases and 6269 controls from the international lymphoma epidemiology consortium. Clinical Gastroenterology and Hepatology. 2008;6(4):451–458.
    1. Arcaini L, Burcheri S, Rossi A, et al. Prevalence of HCV infection in nongastric marginal zone B-cell lymphoma of MALT. Annals of Oncology. 2007;18(2):346–350.
    1. Tomita N, Kodama F, Takabayashi M, et al. Clinical features and outcome in HCV-positive aggressive non-Hodgkin’s lymphoma. Leukemia and Lymphoma. 2003;44(7):1159–1164.
    1. Visco C, Arcaini L, Brusamolino E, et al. Distinctive natural history in hepatitis C virus positive diffuse large B-cell lymphoma: analysis of 156 patients from northern Italy. Annals of Oncology. 2006;17(9):1434–1440.
    1. Lecuit M, Abachin E, Martin A, et al. Immunoproliferative small intestinal disease associated with campylobacter jejuni. New England Journal of Medicine. 2004;350(3):239–248.
    1. Roggero E, Zucca E, Mainetti C, et al. Eradication of Borrelia burgdorferi infection in primary marginal zone B-cell lymphoma of the skin. Human Pathology. 2000;31(2):263–268.
    1. Ferreri AJM, Guidoboni M, Ponzoni M, et al. Evidence for an association between Chlamydia psittaci and ocular adnexal lymphomas. Journal of the National Cancer Institute. 2004;96(8):586–594.
    1. Ferreri AJM, Ponzoni M, Guidoboni M, et al. Regression of ocular adnexal lymphoma after Chlamydia psittaci-eradicating antibiotic therapy. Journal of Clinical Oncology. 2005;23(22):5067–5073.
    1. Arcaini L, Paulli M, Boveri E, Magrini U, Lazzarino M. Marginal zone-related neoplasms of splenic and nodal origin. Haematologica. 2003;88(1):80–93.
    1. Melo JV, Hegde U, Parreira A. Splenic B cell lymphoma with circulating villous lymphocytes: differential diagnosis of B cell leukaemias with large spleens. Journal of Clinical Pathology. 1987;40(6):642–651.
    1. Melo JV, Robinson DSF, Gregory C, Catovsky D. Splenic B cell lymphoma with ’villous’ lymphocytes in the peripheral blood: a disorder distinct from hairy cell leukemia. Leukemia. 1987;1(4):294–298.
    1. Isaacson PG, Matutes E, Burke M, Catovsky D. The histopathology of splenic lymphoma with villous lymphocytes. Blood. 1994;84(11):3828–3834.
    1. Marasca R, Vaccari P, Luppi M, et al. Immunoglobulin gene mutations and frequent use of VH1-69 and VH4-34 segments in hepatitis C virus-positive and hepatitis C virus-negative nodal marginal zone B-cell lymphoma. American Journal of Pathology. 2001;159(1):253–261.
    1. Armitage JO. A clinical evaluation of the International Lymphoma Study Group classification of non-Hodgkin's lymphoma. The Non-Hodgkin's Lymphoma Classification Project. Blood. 1997;89(11):3909–3918.
    1. Cavalli F, Isaacson PG, Gascoyne RD, Zucca E. MALT Lymphomas. Hematology. 2001:241–258.
    1. Thieblemont C. Clinical presentation and management of marginal zone lymphomas. Hematology. 2005:307–313.
    1. Thieblemont C, Berger F, Dumontet C, et al. Mucosa-associated lymphoid tissue lymphoma is a disseminated disease in one third of 158 patients analyzed. Blood. 2000;95(3):802–806.
    1. Thieblemont C, de la Fouchardière A, Coiffier B. Nongastric mucosa-associated lymphoid tissue lymphomas. Clinical Lymphoma. 2003;3(4):212–224.
    1. Zucca E, Conconi A, Pedrinis E, et al. Nongastric marginal zone B-cell lymphoma of mucosa-associated lymphoid tissue. Blood. 2003;101(7):2489–2495.
    1. Coiffier B, Osmanov EA, Hong X, et al. Bortezomib plus rituximab versus rituximab alone in patients with relapsed, rituximab-naive or rituximab-sensitive, follicular lymphoma: a randomised phase 3 trial. The Lancet Oncology. 2011;12(8):773–784.
    1. Luppi M, Longo G, Ferrari MG, et al. Additional neoplasms and HCV infection in low-grade lymphoma of MALT type. British Journal of Haematology. 1996;94(2):373–375.
    1. Ambrosetti A, Zanotti R, Pattaro C, et al. Most cases of primary salivary mucosa-associated lymphoid tissue lymphoma are associated either with Sjoegren syndrome or hepatitis C virus infection. British Journal of Haematology. 2004;126(1):43–49.
    1. Ramos-Casals M, La Civita L, De Vita S, et al. Characterization of B cell lymphoma in patients with Sjögren’s syndrome and hepatitis C virus infection. Arthritis Care and Research. 2007;57(1):161–170.
    1. Leleu X, O’Connor K, Ho AW, et al. Hepatitis C viral infection is not associated with Waldenstrom’s Macroglobulinemia. American Journal of Hematology. 2007;82(1):83–84.
    1. Arcaini L, Sacchi P, Jemos V, et al. Splenic marginal zone B-cell lymphoma in a HIV-positive patient: a case report. Annals of Hematology. 2009;88(4):379–381.
    1. Arcaini L, Pascutto C, Passamonti F, et al. Bayesian models identify specific lymphoproliferative disorders associated with hepatitis C virus infection. International Journal of Cancer. 2009;124(9):2246–2249.
    1. Matutes E, Owusu-Ankomah K, Morilla R, et al. The immunological profile of B-cell disorders and proposal of a scoring system for the diagnosis of CLL. Leukemia. 1994;8(10):1640–1645.
    1. Ugo V, Leporrier N, Salaun V, et al. Deciphering leukemic B-cell chronic lymphoproliferative disorders. Leukemia and Lymphoma. 2006;47(10):2088–2095.
    1. Fried MW, Shiffman ML, Rajender Reddy K, et al. Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection. New England Journal of Medicine. 2002;347(13):975–982.
    1. Hadziyannis SJ, Sette H, Jr., Morgan TR, et al. Peginterferon-α2a and ribavirin combination therapy in chronic hepatitis C: a randomized study of treatment duration and ribavirin dose. Annals of Internal Medicine. 2004;140(5):346–355.
    1. Ghany MG, Strader DB, Thomas DL, Seeff LB. Diagnosis, management, and treatment of hepatitis C: an update. Hepatology. 2009;49(4):1335–1374.
    1. Jesudian AB, Gambarin-Gelwan M, Jacobson IM. Advances in the treatment of hepatitis C virus infection. Gastroenterology & Hepatology. 2012;8:91–101.
    1. Bauduer F. MALT non-Hodgkin's lymphoma associated with hepatitis C virus infection treated by interferon alpha. American Journal of Hematology. 1996;53:p. 209.
    1. Caramaschi P, Biasi D, Carletto A, et al. Mucosa-associated lymphoid tissue (MALT) lymphoma of salivary glands. Report of a case in a patient with hepatitis C virus infection and review of the literature. Recenti Progressi in Medicina. 1999;90(11):585–591.
    1. Moccia F, Tognoni E, Boccaccio P. The relationship between splenic marginal zone B-cell lymphoma and chronic liver disease associated with hepatitis C virus infection. Annali Italiani di Medicina Interna. 1999;14(4):288–293.
    1. Patriarca F, Silvestri F, Fanin R, Zaja F, Sperotto A, Baccarani M. Long-lasting complete remission of hepatitis C virus (HCV) infection and HCV-associated immunocytoma with alpha-interferon treatment. British Journal of Haematology. 2001;112(2):370–372.
    1. Casato M, Mecucci C, Agnello V, et al. Regression of lymphoproliferative disorder after treatment for hepatitis C virus infection in a patient with partial trisomy 3, Bcl-2 overexpression, and type II cryoglobulinemia. Blood. 2002;99(6):2259–2261.
    1. Pitini V, Arrigo C, Righi M, Scaffidi M, Sturniolo G. Systematic screening for HCV infection should be performed in patients with splenic marginal zone lymphoma. British Journal of Haematology. 2004;124(2):252–253.
    1. Tursi A, Brandimarte G, Torello M. Disappearance of gastric mucosa-associated lymphoid tissue in hepatitis C virus-positive patients after anti-hepatitis C virus therapy. Journal of Clinical Gastroenterology. 2004;38(4):360–363.
    1. Kelaidi C, Rollot F, Park S, et al. Response to antiviral treatment in hepatitis C virus-associated marginal zone lymphomas. Leukemia. 2004;18(10):1711–1716.
    1. Vallisa D, Bernuzzi P, Arcaini L, et al. Role of anti-hepatitis C virus (HCV) treatment in HCV-related, low-grade, B-cell, non-Hodgkin’s lymphoma: a multicenter Italian experience. Journal of Clinical Oncology. 2005;23(3):468–473.
    1. Svoboda J, Andreadis C, Downs LH, Miller WT, Tsai DE, Schuster SJ. Regression of advanced non-splenic marginal zone lymphoma after treatment of hepatitis C virus infection. Leukemia and Lymphoma. 2005;46(9):1365–1368.
    1. Oda Y, Kou T, Watanabe M, et al. Regression of B-cell lymphoma of the liver with hepatitis C virus infection after treatment with pegylated interferon-α and ribavirin. Digestive Diseases and Sciences. 2010;55(6):1791–1793.
    1. Mauro E, Pedata M, Ermacora A, Mazzaro C. An additional line of therapy with pegylated interferon and ribavirin after rituximab in a patient with hepatitis C virus-related mixed cryoglobulinaemia and indolent non-Hodgkin's lymphoma previously treated with interferon. Blood Transfusion. 2012;10(1):101–103.
    1. Mazzaro C, De Re V, Spina M, et al. Pegylated-interferon plus ribavirin for HCV-positive indolent non-Hodgkin lymphomas. British Journal of Haematology. 2009;145(2):255–257.
    1. Gisbert JP, García-Buey L, Pajares JM, Moreno-Otero R. Systematic review: regression of lymphoproliferative disorders after treatment for hepatitis C infection. Alimentary Pharmacology and Therapeutics. 2005;21(6):653–662.
    1. Zuckerman E, Zuckerman T, Sahar D, et al. The effect of antiviral therapy on t(14;18) translocation and immunoglobulin gene rearrangement in patients with chronic hepatitis C virus infection. Blood. 2001;97(6):1555–1559.
    1. Paulli M, Arcaini L, Lucioni M, et al. Subcutaneous ’lipoma-like’ B-cell lymphoma associated with HCV infection: a new presentation of primary extranodal marginal zone B-cell lymphoma of MALT. Annals of Oncology. 2009;21(6):1189–1195.
    1. Iannitto E, Ammatuna E, Tripodo C, et al. Long-lasting remission of primary hepatic lymphoma and hepatitis C virus infection achieved by the alpha-interferon treatment. Hematology Journal. 2004;5(6):530–533.
    1. Levine AM, Shimodaira S, Lai MMC. Treatment of HCV-related mantle-cell lymphoma with ribavirin and pegylated interferon alfa. New England Journal of Medicine. 2003;349(21):2078–2079.
    1. Ennishi D, Maeda Y, Niitsu N, et al. Hepatic toxicity and prognosis in hepatitis C virus-infected patients with diffuse large B-cell lymphoma treated with rituximab-containing chemotherapy regimens: a Japanese multicenter analysis. Blood. 2010;116(24):5119–5125.
    1. Musto P, Dell'Olio M, La Sala A, Mantuano S, Cascavilla N. Diffuse B-large cell lymphomas (DBLCL) with hepatitis-C virus (HCV) infection: clinical outcome and preliminary results of a pilot study combining R-CHOP with antiviral therapy. Proceedings of the ASH Annual Meeting Abstracts; 2005; p. p. 2447.
    1. La Mura V, De Renzo A, Perna F, et al. Antiviral therapy after complete response to chemotherapy could be efficacious in HCV-positive non-Hodgkin's lymphoma. Journal of Hepatology. 2008;49:557–563.

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