Non-Hodgkin Lymphoma and Hepatitis C: Where We are and What Next?

Pathology and Oncology Research

Volumn 21, Issue 1, 2015, Pages

  Sulyok, Mihály ^a   Makara, Mihály ^a   Újhelyi, Eszter ^a   Vályi Nagy, István ^a  

^a Szent Laszlo Hospital   (Hungary)

Author keywords

Cryoglobulinemia; Direct acting antivirals; Hepatitis C; Interferon; Non Hodgkin lymphoma

Indexed keywords

ANTIVIRUS AGENT;

COMPLICATION; DRUG EFFECTS; HEPACIVIRUS; HEPATITIS C; HUMAN; LYMPHOMA, NON-HODGKIN;

ANTIVIRAL AGENTS; HEPACIVIRUS; HEPATITIS C; HUMANS; LYMPHOMA, NON-HODGKIN;

EID: 84921937960     PISSN: 12194956     EISSN: 15322807     Source Type: Journal    
DOI: 10.1007/s12253-014-9845-z     Document Type: Review

References (63)

1. Lavanchy D (2011) Evolving epidemiology of hepatitis C virus. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis 17(2):107–115. doi:10.1111/j.1469-0691.2010.03432.x
2. European Association for the Study of the L (2011) EASL Clinical Practice Guidelines: management of hepatitis C virus infection. J Hepatol 55(2):245–264. doi:10.1016/j.jhep.2011.02.023
3. Monti G, Pioltelli P, Saccardo F, Campanini M, Candela M, Cavallero G, De Vita S, Ferri C, Mazzaro C, Migliaresi S, Ossi E, Pietrogrande M, Gabrielli A, Galli M, Invernizzi F (2005) Incidence and characteristics of non-Hodgkin lymphomas in a multicenter case file of patients with hepatitis C virus-related symptomatic mixed cryoglobulinemias. Arch Intern Med 165(1):101–105. doi:10.1001/archinte.165.1.101
4. Suarez F, Lortholary O, Hermine O, Lecuit M (2006) Infection-associated lymphomas derived from marginal zone B cells: a model of antigen-driven lymphoproliferation. Blood 107(8):3034–3044. doi:10.1182/blood-2005-09-3679
5. Arcaini L, Lazzarino M, Colombo N, Burcheri S, Boveri E, Paulli M, Morra E, Gambacorta M, Cortelazzo S, Tucci A, Ungari M, Ambrosetti A, Menestrina F, Orsucci L, Novero D, Pulsoni A, Frezzato M, Gaidano G, Vallisa D, Minardi V, Tripodo C, Callea V, Baldini L, Merli F, Federico M, Franco V, Iannitto E, Integruppo Italiano L (2006) Splenic marginal zone lymphoma: a prognostic model for clinical use. Blood 107(12):4643–4649. doi:10.1182/blood-2005-11-4659
6. Saadoun D, Suarez F, Lefrere F, Valensi F, Mariette X, Aouba A, Besson C, Varet B, Troussard X, Cacoub P, Hermine O (2005) Splenic lymphoma with villous lymphocytes, associated with type II cryoglobulinemia and HCV infection: a new entity? Blood 105(1):74–76. doi:10.1182/blood-2004-05-1711
7. Arcaini L, Paulli M, Burcheri S, Rossi A, Spina M, Passamonti F, Lucioni M, Motta T, Canzonieri V, Montanari M, Bonoldi E, Gallamini A, Uziel L, Crugnola M, Ramponi A, Montanari F, Pascutto C, Morra E, Lazzarino M, Intergruppo Italiano L (2007) Primary nodal marginal zone B-cell lymphoma: clinical features and prognostic assessment of a rare disease. Br J Haematol 136(2):301–304. doi:10.1111/j.1365-2141.2006.06437.x
8. Cavalli F, Isaacson PG, Gascoyne RD, Zucca E (2001) MALT lymphomas. Hematol/Educ Program Am Soc Hematol Am Soc Hematol Educ Program 2001(1):241–58. doi:10.1182/asheducation202001.1.241
9. Arcaini L, Burcheri S, Rossi A, Paulli M, Bruno R, Passamonti F, Brusamolino E, Molteni A, Pulsoni A, Cox MC, Orsucci L, Fabbri A, Frezzato M, Voso MT, Zaja F, Montanari F, Merli M, Pascutto C, Morra E, Cortelazzo S, Lazzarino M (2007) Prevalence of HCV infection in nongastric marginal zone B-cell lymphoma of MALT. Ann Oncol Off J Eur Soc Med Oncol / ESMO 18(2):346–350. doi:10.1093/annonc/mdl388
10. Ambrosetti A, Zanotti R, Pattaro C, Lenzi L, Chilosi M, Caramaschi P, Arcaini L, Pasini F, Biasi D, Orlandi E, D’Adda M, Lucioni M, Pizzolo G (2004) Most cases of primary salivary mucosa-associated lymphoid tissue lymphoma are associated either with Sjoegren syndrome or hepatitis C virus infection. Br J Haematol 126(1):43–49. doi:10.1111/j.1365-2141.2004.04993.x
11. Ferreri AJ, Viale E, Guidoboni M, Resti AG, De Conciliis C, Politi L, Lettini AA, Sacchetti F, Dolcetti R, Doglioni C, Ponzoni M (2006) Clinical implications of hepatitis C virus infection in MALT-type lymphoma of the ocular adnexa. Ann Oncol Off J Eur Soc Med Oncol / ESMO 17(5):769–772. doi:10.1093/annonc/mdl027
12. Paulli M, Arcaini L, Lucioni M, Boveri E, Capello D, Passamonti F, Merli M, Rattotti S, Rossi D, Riboni R, Berti E, Magrini U, Bruno R, Gaidano G, Lazzarino M (2010) Subcutaneous ‘lipoma-like’ B-cell lymphoma associated with HCV infection: a new presentation of primary extranodal marginal zone B-cell lymphoma of MALT. Ann Oncol Off J Eur Soc Med Oncol / ESMO 21(6):1189–1195. doi:10.1093/annonc/mdp454
13. Leleu X, O’Connor K, Ho AW, Santos DD, Manning R, Xu L, Hatjiharissi E, Moreau AS, Branagan AR, Hunter ZR, Dimmock EA, Soumerai J, Patterson C, Ghobrial I, Treon SP (2007) Hepatitis C viral infection is not associated with Waldenstrom’s macroglobulinemia. Am J Hematol 82(1):83–84. doi:10.1002/ajh.20724
14. Arcaini L, Merli M, Volpetti S, Rattotti S, Gotti M, Zaja F (2012) Indolent B-cell lymphomas associated with HCV infection: clinical and virological features and role of antiviral therapy. Clin Dev Immunol 2012:638185. doi:10.1155/2012/638185
15. Pellicelli AM, Marignani M, Zoli V, Romano M, Morrone A, Nosotti L, Barbaro G, Picardi A, Gentilucci UV, Remotti D, D’Ambrosio C, Furlan C, Mecenate F, Mazzoni E, Majolino I, Villani R, Andreoli A, Barbarini G (2011) Hepatitis C virus-related B cell subtypes in non Hodgkin’s lymphoma. World J Hepatol 3(11):278–284. doi:10.4254/wjh.v3.i11.278
16. Besson C, Canioni D, Lepage E, Pol S, Morel P, Lederlin P, Van Hoof A, Tilly H, Gaulard P, Coiffier B, Gisselbrecht C, Brousse N, Reyes F, Hermine O. (2006) 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 Off J Am Soc Clin Oncol 24(6):953–960. doi:10.1200/JCO.2005.01.5016
17. Visco C, Arcaini L, Brusamolino E, Burcheri S, Ambrosetti A, Merli M, Bonoldi E, Chilosi M, Viglio A, Lazzarino M, Pizzolo G, Rodeghiero F (2006) Distinctive natural history in hepatitis C virus positive diffuse large B-cell lymphoma: analysis of 156 patients from northern Italy. Ann Oncol Off J Eur Soc Med Oncol / ESMO 17(9):1434–1440. doi:10.1093/annonc/mdl131
18. Talamini R, Montella M, Crovatto M, Dal Maso L, Crispo A, Negri E, Spina M, Pinto A, Carbone A, Franceschi S (2004) Non-Hodgkin’s lymphoma and hepatitis C virus: a case-control study from northern and southern Italy. Int J Cancer J Int Cancer 110(3):380–385. doi:10.1002/ijc.20137
19. Guadagnino V, Stroffolini T, Rapicetta M, Costantino A, Kondili LA, Menniti-Ippolito F, Caroleo B, Costa C, Griffo G, Loiacono L, Pisani V, Foca A, Piazza M (1997) Prevalence, risk factors, and genotype distribution of hepatitis C virus infection in the general population: a community-based survey in southern Italy. Hepatology 26(4):1006–1011. doi:10.1002/hep.510260431
20. Collier JD, Zanke B, Moore M, Kessler G, Krajden M, Shepherd F, Heathcote J (1999) No association between hepatitis C and B-cell lymphoma. Hepatology 29(4):1259–1261. doi:10.1002/hep.510290422
21. Gisbert JP, Garcia-Buey L, Pajares JM, Moreno-Otero R (2003) Prevalence of hepatitis C virus infection in porphyria cutanea tarda: systematic review and meta-analysis. J Hepatol 39(4):620–627
22. Matsuo K, Kusano A, Sugumar A, Nakamura S, Tajima K, Mueller NE (2004) Effect of hepatitis C virus infection on the risk of non-Hodgkin’s lymphoma: a meta-analysis of epidemiological studies. Cancer Sci 95(9):745–752
23. Dal Maso L, Franceschi S (2006) Hepatitis C virus and risk of lymphoma and other lymphoid neoplasms: a meta-analysis of epidemiologic studies. Cancer Epidemiol Biomarkers Prev 15(11):2078–2085. doi:10.1158/1055-9965.EPI-06-0308
24. Nieters A, Kallinowski B, Brennan P, Ott M, Maynadie M, Benavente Y, Foretova L, Cocco PL, Staines A, Vornanen M, Whitby D, Boffetta P, Becker N, De Sanjose S (2006) Hepatitis C and risk of lymphoma: results of the European multicenter case-control study EPILYMPH. Gastroenterology 131(6):1879–1886. doi:10.1053/j.gastro.2006.09.019
25. de Sanjose S, Benavente Y, Vajdic CM, Engels EA, Morton LM, Bracci PM, Spinelli JJ, Zheng T, Zhang Y, Franceschi S, Talamini R, Holly EA, Grulich AE, Cerhan JR, Hartge P, Cozen W, Boffetta P, Brennan P, Maynadie M, Cocco P, Bosch R, Foretova L, Staines A, Becker N, Nieters A (2008) Hepatitis C and non-Hodgkin lymphoma among 4784 cases and 6269 controls from the International Lymphoma Epidemiology Consortium. Clin Gastroenterol Hepat Off Clin Pract J Am Gastroenterol Assoc 6(4):451–458. doi:10.1016/j.cgh.2008.02.011
26. Hermine O, Lefrere F, Bronowicki JP, Mariette X, Jondeau K, Eclache-Saudreau V, Delmas B, Valensi F, Cacoub P, Brechot C, Varet B, Troussard X (2002) Regression of splenic lymphoma with villous lymphocytes after treatment of hepatitis C virus infection. N Engl J Med 347(2):89–94. doi:10.1056/NEJMoa013376
27. Kelaidi C, Rollot F, Park S, Tulliez M, Christoforov B, Calmus Y, Podevin P, Bouscary D, Sogni P, Blanche P, Dreyfus F (2004) Response to antiviral treatment in hepatitis C virus-associated marginal zone lymphomas. Leukemia 18(10):1711–1716. doi:10.1038/sj.leu.2403443
28. Tursi A, Brandimarte G, Torello M (2004) Disappearance of gastric mucosa-associated lymphoid tissue in hepatitis C virus-positive patients after anti-hepatitis C virus therapy. J Clin Gastroenterol 38(4):360–363
29. Mazzaro C, De Re V, Spina M, Dal Maso L, Festini G, Comar C, Tirelli U, Pozzato G (2009) Pegylated-interferon plus ribavirin for HCV-positive indolent non-Hodgkin lymphomas. Br J Haematol 145(2):255–257. doi:10.1111/j.1365-2141.2008.07565.x
30. Peveling-Oberhag J, Arcaini L, Hansmann ML, Zeuzem S (2013) Hepatitis C-associated B-cell non-Hodgkin lymphomas. Epidemiology, molecular signature and clinical management. J Hepatol 59(1):169–177. doi:10.1016/j.jhep.2013.03.018
31. Vallisa D, Bernuzzi P, Arcaini L, Sacchi S, Callea V, Marasca R, Lazzaro A, Trabacchi E, Anselmi E, Arcari AL, Moroni C, Berte R, Lazzarino M, Cavanna L (2005) Role of anti-hepatitis C virus (HCV) treatment in HCV-related, low-grade, B-cell, non-Hodgkin’s lymphoma: a multicenter Italian experience. J Clin Oncol Off J Am Soc Clin Oncol 23(3):468–473. doi:10.1200/JCO.2005.06.008
32. Patriarca F, Silvestri F, Fanin R, Zaja F, Sperotto A, Baccarani M (2001) Long-lasting complete remission of hepatitis C virus (HCV) infection and HCV-associated immunocytoma with alpha-interferon treatment. Br J Haematol 112(2):370–372
33. Casato M, Mecucci C, Agnello V, Fiorilli M, Knight GB, Matteucci C, Gao L, Kay J (2002) 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 99(6):2259–2261
34. Caramaschi P, Biasi D, Carletto A, Ambrosetti A, Mocella S, Randon M, Bambara LM (1999) MALT lymphomas of the salivary glands. Review of the literature apropos of a case in a patient with hepatitis C virus infection. Recenti Prog Med 90(11):585–591
35. Bauduer F (1996) MALT non-Hodgkin’s lymphoma associated with hepatitis C virus infection treated by interferon alpha. Am J Hematol 53(3):209. doi:10.1002/(SICI)1096-8652(199611)53:3<209::AID-AJH18>3.0.CO;2-8
36. Pitini V, Arrigo C, Righi M, Scaffidi M, Sturniolo G (2004) Systematic screening for HCV infection should be performed in patients with splenic marginal zone lymphoma. Br J Haematol 124(2):252–253
37. Moccia F, Tognoni E, Boccaccio P (1999) The relationship between splenic marginal zone B-cell lymphoma and chronic liver disease associated with hepatitis C virus infection. Ann Ital Med Int Organo Uff Soc Ital Med Int 14(4):288–293
38. Oda Y, Kou T, Watanabe M, Sakuma Y, Taguchi N, Kato Y, Kudo Y, Yamauchi A, Sugiura Y, Ohashi S, Asada M, Fukunaga T, Kawaguchi K, Ito H, Nakamura T, Yazumi S (2010) Regression of B-cell lymphoma of the liver with hepatitis C virus infection after treatment with pegylated interferon-alpha and ribavirin. Dig Dis Sci 55(6):1791–1793. doi:10.1007/s10620-009-0902-5
39. Mauro E, Pedata M, Ermacora A, Mazzaro C (2012) 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 Transfus Trasfus Sang 10(1):101–103. doi:10.2450/2011.0006-11
40. Takahashi K, Nishida N, Kawabata H, Haga H, Chiba T (2012) Regression of Hodgkin lymphoma in response to antiviral therapy for hepatitis C virus infection. Intern Med 51(19):2745–2747
41. Svoboda J, Andreadis C, Downs LH, Miller WT Jr, Tsai DE, Schuster SJ (2005) Regression of advanced non-splenic marginal zone lymphoma after treatment of hepatitis C virus infection. Leuk Lymphoma 46(9):1365–1368. doi:10.1080/104281905001028289
42. Iannitto E, Ammatuna E, Tripodo C, Marino C, Calvaruso G, Florena AM, Montalto G, Franco V (2004) Long-lasting remission of primary hepatic lymphoma and hepatitis C virus infection achieved by the alpha-interferon treatment. Hematol J Off J Eur Haematol Assoc / EHA 5(6):530–533. doi:10.1038/sj.thj.6200408
43. La Mura V, De Renzo A, Perna F, D’Agostino D, Masarone M, Romano M, Bruno S, Torella R, Persico M (2008) Antiviral therapy after complete response to chemotherapy could be efficacious in HCV-positive non-Hodgkin’s lymphoma. J Hepatol 49(4):557–563. doi:10.1016/j.jhep.2008.06.025
44. De Re V, De Vita S, Marzotto A, Gloghini A, Pivetta B, Gasparotto D, Cannizzaro R, Carbone A, Boiocchi M (2000) 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 J Int Cancer 87(2):211–216
45. Quinn ER, Chan CH, Hadlock KG, Foung SK, Flint M, Levy S (2001) The B-cell receptor of a hepatitis C virus (HCV)-associated non-Hodgkin lymphoma binds the viral E2 envelope protein, implicating HCV in lymphomagenesis. Blood 98(13):3745–3749
46. Flint M, McKeating JA (2000) The role of the hepatitis C virus glycoproteins in infection. Rev Med Virol 10(2):101–117
47. Peveling-Oberhag J, Crisman G, Schmidt A, Doring C, Lucioni M, Arcaini L, Rattotti S, Hartmann S, Piiper A, Hofmann WP, Paulli M, Kuppers R, Zeuzem S, Hansmann ML (2012) Dysregulation of global microRNA expression in splenic marginal zone lymphoma and influence of chronic hepatitis C virus infection. Leukemia 26(7):1654–1662. doi:10.1038/leu.2012.29
48. Schneider P, MacKay F, Steiner V, Hofmann K, Bodmer JL, Holler N, Ambrose C, Lawton P, Bixler S, Acha-Orbea H, Valmori D, Romero P, Werner-Favre C, Zubler RH, Browning JL, Tschopp J (1999) BAFF, a novel ligand of the tumor necrosis factor family, stimulates B cell growth. J Exp Med 189(11):1747–1756
49. Mackay F, Woodcock SA, Lawton P, Ambrose C, Baetscher M, Schneider P, Tschopp J, Browning JL (1999) Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J Exp Med 190(11):1697–1710
50. Fabris M, Quartuccio L, Sacco S, De Marchi G, Pozzato G, Mazzaro C, Ferraccioli G, Migone TS, De Vita S (2007) B-Lymphocyte stimulator (BLyS) up-regulation in mixed cryoglobulinaemia syndrome and hepatitis-C virus infection. Rheumatology 46(1):37–43. doi:10.1093/rheumatology/kel174
51. Sene D, Limal N, Ghillani-Dalbin P, Saadoun D, Piette JC, Cacoub P (2007) Hepatitis C virus-associated B-cell proliferation–the role of serum B lymphocyte stimulator (BLyS/BAFF). Rheumatology 46(1):65–69. doi:10.1093/rheumatology/kel177
52. Rowan AG, Fletcher JM, Ryan EJ, Moran B, Hegarty JE, O’Farrelly C, Mills KH (2008) Hepatitis C virus-specific Th17 cells are suppressed by virus-induced TGF-beta. J Immunol 181(7):4485–4494
53. Forghieri F, Luppi M, Barozzi P, Maffei R, Potenza L, Narni F, Marasca R (2012) Pathogenetic mechanisms of hepatitis C virus-induced B-cell lymphomagenesis. Clin Dev Immunol 2012:807351. doi:10.1155/2012/807351
54. Zuckerman E, Zuckerman T, Sahar D, Streichman S, Attias D, Sabo E, Yeshurun D, Rowe J (2001) bcl-2 and immunoglobulin gene rearrangement in patients with hepatitis C virus infection. Br J Haematol 112(2):364–369
55. Zuckerman E, Zuckerman T, Sahar D, Streichman S, Attias D, Sabo E, Yeshurun D, Rowe JM (2001) The effect of antiviral therapy on t(14;18) translocation and immunoglobulin gene rearrangement in patients with chronic hepatitis C virus infection. Blood 97(6):1555–1559
56. Machida K, Cheng KT, Sung VM, Lee KJ, Levine AM, Lai MM (2004) Hepatitis C virus infection activates the immunologic (type II) isoform of nitric oxide synthase and thereby enhances DNA damage and mutations of cellular genes. J Virol 78(16):8835–8843. doi:10.1128/JVI.78.16.8835-8843.2004
57. Karavattathayyil SJ, Kalkeri G, Liu HJ, Gaglio P, Garry RF, Krause JR, Dash S (2000) Detection of hepatitis C virus RNA sequences in B-cell non-Hodgkin lymphoma. Am J Clin Pathol 113(3):391–398. doi:10.1309/REV9-FDTM-5NGC-HBWY
58. Machida K, Cheng KT, Sung VM, Shimodaira S, Lindsay KL, Levine AM, Lai MY, Lai MM (2004) Hepatitis C virus induces a mutator phenotype: enhanced mutations of immunoglobulin and protooncogenes. Proc Natl Acad Sci U S A 101(12):4262–4267. doi:10.1073/pnas.0303971101
59. Machida K, Cheng KT, Pavio N, Sung VM, Lai MM (2005) Hepatitis C virus E2-CD81 interaction induces hypermutation of the immunoglobulin gene in B cells. J Virol 79(13):8079–8089. doi:10.1128/JVI.79.13.8079-8089.2005
60. Bachy E, Besson C, Suarez F, Hermine O (2010) Hepatitis C virus infection and lymphoma. Mediterr J Hematol Infect Dis 2(1):e2010004. doi:10.4084/MJHID.2010.004
61. Manns MP, McHutchison JG, Gordon SC, Rustgi VK, Shiffman M, Reindollar R, Goodman ZD, Koury K, Ling M, Albrecht JK (2001) Peginterferon alfa-2b plus ribavirin compared with interferon alfa-2b plus ribavirin for initial treatment of chronic hepatitis C: a randomised trial. Lancet 358(9286):958–965
62. Jacobson IM, Gordon SC, Kowdley KV, Yoshida EM, Rodriguez-Torres M, Sulkowski MS, Shiffman ML, Lawitz E, Everson G, Bennett M, Schiff E, Al-Assi MT, Subramanian GM, An D, Lin M, McNally J, Brainard D, Symonds WT, McHutchison JG, Patel K, Feld J, Pianko S, Nelson DR. (2013) Sofosbuvir for hepatitis C genotype 2 or 3 in patients without treatment options. N Engl J Med 368(20):1867–1877. doi:10.1056/NEJMoa1214854
63. Lawitz E, Mangia A, Wyles D, Rodriguez-Torres M, Hassanein T, Gordon SC, Schultz M, Davis MN, Kayali Z, Reddy KR, Jacobson IM, Kowdley KV, Nyberg L, Subramanian GM, Hyland RH, Arterburn S, Jiang D, McNally J, Brainard D, Symonds WT, McHutchison JG, Sheikh AM, Younossi Z, Gane EJ (2013) Sofosbuvir for previously untreated chronic hepatitis C infection. N Engl J Med 368(20):1878–1887. doi:10.1056/NEJMoa1214853