Hepatitis c associated b-cell non-hodgkin lymphoma: Clinical features and the role of antiviral therapy

Journal of Clinical and Translational Hepatology

Volumn 3, Issue 2, 2015, Pages 134-139

  Tasleem, Syed ^a   Sood, Gagan K ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Hepatitis C; Mixed cryoglobulinemia; Non Hodgkin lymphoma; Rituximab

Indexed keywords

EID: 84962939782     PISSN: 22250719     EISSN: 23108819     Source Type: Journal    
DOI: 10.14218/JCTH.2015.00011     Document Type: Review

References (67)

1. Zuckerman E, Zuckerman T, Levine AM, Douer D, Gutekunst K, Mizokami M, et al. Hepatitis C virus infection in patients with B-cell non-hodgkin lym-phoma. Ann Intern Med 1997;127:423–428. doi:10.7326/0003-4819-127-6-199709150-00002.
2. Paydas S, Kilic B, Yavuz S, Disel U, Tanriverdi K, Sahin B, et al. Anti-HCV and HCV-RNA prevalence and clinical correlations in cases with non-hodgkin’s lymphoma. Am J Hematol 2003;74:89–93. doi:10.1002/ajh.10386.
3. Paydas S. Hepatitis C virus and lymphoma. Crit Rev Oncol Hematol 2015;93: 246–256. doi:S1040-8428(14)00168-1.
4. Peveling-Oberhag J, Arcaini L, Hansmann ML, Zeuzem S. Hepatitis C-associated B-cell non-hodgkin lymphomas. epidemiology, molecular signature and clinical management. J Hepatol 2013;59:169–177. doi:10.1016/j.jhep.2013.03.018.
5. Arcaini L, Vallisa D, Rattotti S, Ferretti VV, Ferreri AJ, Bernuzzi P, et al. Antiviral treatment in patients with indolent B-cell lymphomas associated with HCV infection: A study of the fondazione italiana linfomi. Ann Oncol 2014;25: 1404–1410. doi:10.1093/annonc/mdu166.
6. Pawlotsky JM. New hepatitis C virus (HCV) drugs and the hope for a cure: Concepts in anti-HCV drug development. Semin Liver Dis 2014;34:22–29. doi:10.1055/s-0034-1371007.
7. Agnello V, Chung RT, Kaplan LM. A role for hepatitis C virus infection in type II cryoglobulinemia. N Engl J Med 1992;327:1490–1495. doi:10. 1056/NEJM199211193272104.
8. Cacoub P, Maisonobe T, Thibault V, Gatel A, Servan J, Musset L, et al. Systemic vasculitis in patients with hepatitis C. J Rheumatol 2001;28:109–118.
9. Ferri C, Sebastiani M, Giuggioli D, Cazzato M, Longombardo G, Antonelli A, et al. Mixed cryoglobulinemia: Demographic, clinical, and serologic features and survival in 231 patients. Semin Arthritis Rheum 2004;33:355–374. doi: S0049017203001793.
10. Monti G, Pioltelli P, Saccardo F, Campanini M, Candela M, Cavallero G, et al. Incidence and characteristics of non-hodgkin lymphomas in a multicenter case file of patients with hepatitis C virus-related symptomatic mixed cryo-globulinemias. Arch Intern Med 2005;165:101–105.
11. Gragnani L, Fognani E, Piluso A, Boldrini B, Urraro T, Fabbrizzi A, et al . Long-term effect of HCV eradication in patients with mixed cryoglobulinemia: A prospective, controlled, open-label, cohort study. Hepatology 2015;61: 1145–1153. doi:10.1002/hep.27623.
12. Talamini R, Montella M, Crovatto M, Dal Maso L, Crispo A, Negri E, et al. Non-hodgkin’s lymphoma and hepatitis C virus: A case-control study from northern and southern italy. Int J Cancer 2004;110:380–385. doi:10.1002/ijc.20137.
13. Collier JD, Zanke B, Moore M, Kessler G, Krajden M, Shepherd F, et al. No association between hepatitis C and B-cell lymphoma. Hepatology 1999;29: 1259–1261. doi:S0270913999001913.
14. Gisbert JP, Garcia-Buey L, Arranz R, Blas C, Pinilla I, Khorrami S, et al. The prevalence of hepatitis C virus infection in patients with non-hodgkin’s lymphoma. Eur J Gastroenterol Hepatol 2004;16:135–138. doi:00042737-200402000-00003.
15. Dal Maso L, Franceschi S. Hepatitis C virus and risk of lymphoma and other lymphoid neoplasms: A meta-analysis of epidemiologic studies. Cancer Epidemiol Biomarkers Prev 2006;15:2078–2085. doi:10.1158/1055-9965. EPI-06-0308.
16. de Sanjose S, Benavente Y, Vajdic CM, Engels EA, Morton LM, Bracci PM, et al. Hepatitis C and non-hodgkin lymphoma among 4784 cases and 6269 con-con-trols from the international lymphoma epidemiology consortium. Clin Gastroenterol Hepatol 2008;6:451–458. doi:10.1016/j.cgh.2008.02.011. trols
17. Guadagnino V, Stroffolini T, Rapicetta M, Costantino A, Kondili LA, Menniti-Ippolito F, et al. Prevalence, risk factors, and genotype distribution of hepatitis C virus infection in the general population: A community-based survey in southern italy. Hepatology 1997;26:1006–1011. doi:S0270913997004527.
18. Matsuo K, Kusano A, Sugumar A, Nakamura S, Tajima K, Mueller NE. Effect of hepatitis C virus infection on the risk of non-hodgkin’s lymphoma: A meta-analysis of epidemiological studies. Cancer Sci 2004;95:745–752. doi:10.1111/j.1349-7006.2004.tb03256.x.
19. Arcaini L, Paulli M, Boveri E, Vallisa D, Bernuzzi P, Orlandi E, et al. Splenic and nodal marginal zone lymphomas are indolent disorders at high hepatitis C virus seroprevalence with distinct presenting features but similar morpho-logic and phenotypic profiles. Cancer 2004;100:107–115. doi:10.1002/cncr. 11893.
20. Torres HA, Mahale P. Most patients with HCV-associated lymphoma present with mild liver disease: A call to revise antiviral treatment prioritization. Liver Int 2015;35(6):1661–1664. doi:10.1111/liv.12825.
21. Arcaini L, Burcheri S, Rossi A, Paulli M, Bruno R, Passamonti F, et al. Prevalence of HCV infection in nongastric marginal zone B-cell lymphoma of MALT. Ann Oncol 2007;18:346–350. doi:10.1093/annonc/mdl388.
22. Arcaini L, Merli M, Volpetti S, Rattotti S, Gotti M, Zaja F. Indolent B-cell lymphomas associated with HCV infection: Clinical and virological features and role of antiviral therapy. Clin Dev Immunol 2012;2012:638185. doi: 10.1155/2012/638185.
23. Sulyok M, Makara M, Ujhelyi E, Valyi-Nagy I. Non-hodgkin lymphoma and hepatitis C: Where we are and what next? Pathol Oncol Res 2015;21:1–7. doi:10.1007/s12253-014-9845-z.
24. Luppi M, Grazia Ferrari M, Bonaccorsi G, Longo G, Narni F, Barozzi P, et al. Hepatitis C virus infection in subsets of neoplastic lymphoproliferations not associated with cryoglobulinemia. Leukemia 1996;10:351–355.
25. De Vita S, De Re V, Sansonno D, Sorrentino D, Corte RL, Pivetta B, et al. Gastric mucosa as an additional extrahepatic localization of hepatitis C virus: Viral detection in gastric low-grade lymphoma associated with auto-immune disease and in chronic gastritis. Hepatology 2000;31:182–189. doi: S0270913900783480.
26. Arcaini L, Burcheri S, Rossi A, Paulli M, Bruno R, Passamonti F, et al. Prevalence of HCV infection in nongastric marginal zone B-cell lymphoma of MALT. Ann Oncol 2007;18:346–350. doi:10.1093/annonc/mdl388.
27. Pellicelli AM, Marignani M, Zoli V, Romano M, Morrone A, Nosotti L, et al. Hepatitis C virus-related B cell subtypes in non hodgkin’s lymphoma. World J Hepatol 2011;3:278–284. doi:10.4254/wjh.v3.i11.278.
28. Arcaini L, Paulli M, Boveri E, Vallisa D, Bernuzzi P, Orlandi E, et al. Splenic and nodal marginal zone lymphomas are indolent disorders at high hepatitis C virus seroprevalence with distinct presenting features but similar morpho-logic and phenotypic profiles. Cancer 2004;100:107–115. doi:10.1002/cncr. 11893.
29. Ferreri AJ, Viale E, Guidoboni M, Resti AG, De Conciliis C, Politi L, et al. Clinical implications of hepatitis C virus infection in MALT-type lymphoma of the ocular adnexa. Ann Oncol 2006;17:769–772. doi:10.1093/annonc/mdl027.
30. Arcaini L, Lazzarino M, Colombo N, Burcheri S, Boveri E, Paulli M, et al. Splenic marginal zone lymphoma: A prognostic model for clinical use. Blood 2006;107:4643–4649.
31. Saadoun D, Suarez F, Lefrere F, Valensi F, Mariette X, Aouba A, et al. Splenic lymphoma with villous lymphocytes, associated with type II cryoglobuline-mia and HCV infection: A new entity? Blood 2005;105:74–76. doi:10. 1182/blood-2004-05-1711.
32. Arcaini L, Varettoni M, Boveri E, Orlandi E, Rattotti S, Zibellini S, et al. Dis-tinctive clinical and histological features of waldenstrom’s macroglobuline-mia and splenic marginal zone lymphoma. Clin Lymphoma Myeloma Leuk 2011;11:103–105. doi:10.3816/CLML.2011.n.020.
33. de Re V, Caggiari L, Simula MP, de Vita S, Sansonno D, Dolcetti R. B-cell lymphomas associated with HCV infection. Gastroenterology 2007;132: 1205–1207. doi:S0016-5085(07)00356-3.
34. Michot JM, Canioni D, Driss H, Alric L, Cacoub P, Suarez F, et al. Antiviral therapy is associated with a better survival in patients with hepatitis C virus and B-cell non-hodgkin lymphomas, ANRS HC-13 lympho-C study. Am J Hematol 2015;90:197–203. doi:10.1002/ajh.23889.
35. Visco C, Finotto S. Hepatitis C virus and diffuse large B-cell lymphoma: Pathogenesis, behavior and treatment. World J Gastroenterol 2014;20: 11054–11061. doi:10.3748/wjg.v20.i32.11054.
36. Pellicelli AM, Marignani M, Zoli V, Romano M, Morrone A, Nosotti L, et al. Hepatitis C virus-related B cell subtypes in non hodgkin’s lymphoma. World J Hepatol 2011;3:278–284. doi:10.4254/wjh.v3.i11.278.
37. De Re V, De Vita S, Marzotto A, Gloghini A, Pivetta B, Gasparotto D, et al. Pre-malignant and malignant lymphoproliferations in an HCV-infected type II mixed cryoglobulinemic patient are sequential phases of an antigen-driven pathological process. Int J Cancer 2000;87:211–216. doi:10.1002/1097-0215(20000715)87:2<211::AID-IJC9>3.0.CO;2-8.
38. Zignego AL, Gragnani L, Piluso A, Sebastiani M, Giuggioli D, Fallahi P, et al. Virus-driven autoimmunity and lymphoproliferation: The example of HCV infection. Expert Rev Clin Immunol 2015;11:15–31. doi:10.1586/1744666X.2015.997214.
39. Hermine O, Lefrere F, Bronowicki JP, Mariette X, Jondeau K, Eclache-Sau-dreau V, et al. Regression of splenic lymphoma with villous lymphocytes after treatment of hepatitis C virus infection. N Engl J Med 2002;347: 89–94. doi:10.1056/NEJMoa013376.
40. Vallisa D, Bernuzzi P, Arcaini L, Sacchi S, Callea V, Marasca R, et al. Roleof anti-hepatitis C virus (HCV) treatment in HCV-related, low-grade, B-cell, non-hodgkin’s lymphoma: A multicenter italian experience. J Clin Oncol 2005;23:468–473. doi:10.1200/JCO.2005.06.008.
41. Kelaidi C, Rollot F, Park S, Tulliez M, Christoforov B, Calmus Y, et al. Response to antiviral treatment in hepatitis C virus-associated marginal zone lympho-mas. Leukemia 2004;18:1711–1716. doi:10.1038/sj.leu.2403443.
42. 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. J Clin Gastroenterol 2004;38:360–363. doi: 00004836-200404000-00011.
43. Saadoun D, Resche Rigon M, Pol S, Thibault V, Blanc F, Pialoux G, et al. PegIFNalpha/ribavirin/protease inhibitor combination in severe hepatitis C virus-associated mixed cryoglobulinemia vasculitis. J Hepatol 2015;62: 24–30. doi:10.1016/j.jhep.2014.08.015.
44. Mazzaro C, De Re V, Spina M, Dal Maso L, Festini G, Comar C, et al. Pegy-lated-interferon plus ribavirin for HCV-positive indolent non-hodgkin lym-phomas. Br J Haematol 2009;145:255–257. doi:10.1111/j.1365-2141. 2008.07565.x.
45. Pellicelli AM, Zoli V. Role of ribavirin in hepatitis flare in HCV-infected patients with B cell non hodgkin’s lymphoma treated with rituximab-containing regi-mens. Dig Liver Dis 2011;43:501–502. doi:10.1016/j.dld.2010.12.018.
46. Michot JM, Canioni D, Driss H, Alric L, Cacoub P, Suarez F, et al. Antiviral therapy is associated with a better survival in patients with hepatitis C virus and B-cell non-hodgkin lymphomas, ANRS HC-13 lympho-C study. Am J Hematol 2015;90:197–203. doi:10.1002/ajh.23889.
47. Rai D, Wang L, Jiang X, Zhan P, Jia H, De Clercq E, et al. The changing face of hepatitis C: Recent advances on HCV inhibitors targeting NS5A. Curr Med Chem 2015, Feb 9.
48. Rossotti R, Travi G, Pazzi A, Baiguera C, Morra E, Puoti M. Rapid clearance of HCV-related splenic marginal zone lymphoma under an interferon-free, NS3/NS4A inhibitor-based treatment. A case report. J Hepatol 2015;62: 234–237. doi:10.1016/j.jhep.2014.09.031.
49. Miller MH, Agarwal K, Austin A, Brown A, Barclay ST, Dundas P, et al. Review article: 2014 UK consensus guidelines-hepatitis C management and direct-acting anti-viral therapy. Aliment Pharmacol Ther 2014;39:1363–1375. doi: 10.1111/apt.12764.
50. Sultanik P, Klotz C, Brault P, Pol S, Mallet V. Regression of an HCV-associated disseminated marginal zone lymphoma under IFN-free antiviral treatment. Blood 2015;125:2446–2447. doi:10.1182/blood-2014-12-618652.
51. Butt AA, Yan P, Shaikh OS, Freiberg MS, Lo Re V 3rd, Justice AC, et al. Virologic response and haematologic toxicity of boceprevir-and telaprevir-containing regimens in actual clinical settings. J Viral Hepat 2014, Dec 18. doi:10.1111/jvh.12375.
52. Bourliere M, Bronowicki JP, de Ledinghen V, Hézode C, Zoulim F, Mathurin P, et al. Ledipasvir-sofosbuvir with or without ribavirin to treat patients with HCV genotype 1 infection and cirrhosis non-responsive to previous protease-inhibitor therapy: A randomised, double-blind, phase 2 trial (SIRIUS). Lancet Infect Dis 2015;15:397–404. doi:10.1016/S1473-3099 (15)70050-2.
53. Lawitz E, Poordad FF, Pang PS, Hyland RH, Ding X, Mo H, et al. Sofosbuvir and ledipasvir fixed-dose combination with and without ribavirin in treatment-treatment-naive and previously treated patients with genotype 1 hepatitis C virus infection (LONESTAR): An open-label, randomised, phase 2 trial. Lancet 2014;383:515–523. doi:10.1016/S0140-6736(13)62121-2. naive
54. Sulkowski MS, Gardiner DF, Rodriguez-Torres M, Reddy KR, Hassanein T, Jacobson I, et al . Daclatasvir plus sofosbuvir for previously treated or untreated chronic HCV infection. N Engl J Med 2014;370:211–221. doi:10. 1056/NEJMoa1306218.
55. Kowdley KV, Gordon SC, Reddy KR, Rossaro L, Bernstein DE, Lawitz E, et al. Ledipasvir and sofosbuvir for 8 or 12 weeks for chronic HCV without cirrhosis. N Engl J Med 2014;370:1879–1888. doi:10.1056/NEJMoa1402355.
56. Gane EJ, Stedman CA, Hyland RH, Ding X, Svarovskaia E, Subramanian GM, et al. Efficacy of nucleotide polymerase inhibitor sofosbuvir plus the NS5A inhibitor ledipasvir or the NS5B non-nucleoside inhibitor GS-9669 against HCV genotype 1 infection. Gastroenterology 2014;146:736–743.e1. doi: 10.1053/j.gastro.2013.11.007.
57. Keating GM. Sofosbuvir: A review of its use in patients with chronic hepatitis C. Drugs 2014;74:1127–1146. doi:10.1007/s40265-014-0247-z.
58. Nishikawa H, Tsudo M, Osaki Y. Clinical outcome in diffuse large B-cell lymphoma with hepatitis C virus infection in the rituximab era: A single center experience. Oncol Rep 2012;28:835–840. doi:10.3892/or.2012. 1883.
59. Chen TT, Chiu CF, Yang TY, Lin CC, Sargeant AM, Yeh SP, et al. Hepatitis C infection is associated with hepatic toxicity but does not compromise the survival of patients with diffuse large B cell lymphoma treated with rituximab-based chemotherapy. Leuk Res 2015;39:151–156. doi:10. 1016/j.leukres.2014.11.015.
60. La Mura V, De Renzo A, Perna F, D’Agostino D, Masarone M, Romano M, et al. Antiviral therapy after complete response to chemotherapy could be effica-cious in HCV-positive non-hodgkin’s lymphoma. J Hepatol 2008;49: 557–563. doi:10.1016/j.jhep.2008.06.025.
61. Besson C, Canioni D, Lepage E, Pol S, Morel P, Lederlin P, et al. Characteristics and outcome of diffuse large B-cell lymphoma in hepatitis C virus-positive patients in LNH 93 and LNH 98 groupe d’etude des lymphomes de l’adulte programs. J Clin Oncol 2006;24:953–960. doi:10.1200/JCO.2005.01. 5016.
62. Zaky AH, Bakry R, El-sayed MI, Elwanis MA, Nabih O. Impact of treatment-related toxicity on outcome of HCV-positive diffuse large B-cell lymphoma in rituximab era. Hematology 2014;19:412–416. doi:10.1179/1607845413Y. 0000000147.
63. Salah-Eldin MA, Ebrahim MA, El-Sadda W. Clinical outcome of HCV-positive patients with diffuse large B-cell lymphoma treated with rituximab-based chemotherapy. Ann Hematol 2014;93:1903–1911. doi:10.1007/s00277-014-2138-5.
64. Ennishi D, Maeda Y, Niitsu N, Kojima M, Izutsu K, Takizawa J, et al. Hepatic toxicity and prognosis in hepatitis C virus-infected patients with diffuse large B-cell lymphoma treated with rituximab-containing chemotherapy regi-mens: A japanese multicenter analysis. Blood 2010;116:5119–5125. doi: 10.1182/blood-2010-06-289231.
65. Salah-Eldin MA, Ebrahim MA, El-Sadda W. Clinical outcome of HCV-positive patients with diffuse large B-cell lymphoma treated with rituximab-based chemotherapy. Ann Hematol 2014;93:1903–1911. doi:10.1007/s00277-014-2138-5.
66. Zaky AH, Bakry R, El-sayed MI, Elwanis MA, Nabih O. Impact of treatment-related toxicity on outcome of HCV-positive diffuse large B-cell lymphoma in rituximab era. Hematology 2014;19:412–416. doi:10.1179/1607845413Y. 0000000147.
67. Michot JM, Canioni D, Driss H, Alric L, Cacoub P, Suarez F, et al. Antiviral therapy is associated with a better survival in patients with hepatitis C virus and B-cell non-hodgkin lymphomas, ANRS HC-13 lympho-C study. Am J Hematol 2015;90:197–203. doi:10.1002/ajh.23889.