HCV-ассоциированная смешанная криоглобулинемия и В-клеточная неходжкинская лимфома – патогенетически связанные проблемы
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В-НХЛ. В обзоре обсуждаются также возможности лечения HCV-ассоциированной В-НХЛ с помощью противовирусной терапии или с использованием других терапевтических вариантов, таких как химиотерапия.
Ключевые слова: хронический гепатит С, смешанная криоглобулинемия, В-клеточная неходжкинская лимфома, противовирусная терапия, химиотерапия.
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Hepatitis C virus (HCV) is a global population problem due to its high prevalence, usually late diagnosis, the difficulties of treatment. In the prognosis of patients with HCV not only hepatic, but increasingly frequent of extrahepatic HCV manifestations, such as mixed cryoglobulinemia (CG), are important. Mixed CG is currently considered as a B-cell benign lymphoproliferative disorders. The role of HCV virus in the pathogenesis of lymphoproliferative diseases is confirmed by a large number of epidemiological studies, as well as by the effectiveness of antiviral therapy in patients with non-Hodgkin’s lymphoma (NHL). The purpose of the review was to provide an overview of recent literature data and the meta-analysis of epidemiological data explaining the role of HCV in the development of NHL. The review also discusses the treatment for HCV-associated NHL by antiviral therapy or other therapeutic options, such as chemotherapy.
Keywords: chronic hepatitis C, mixed cryoglobulinemia, B-cell non-Hodgkin’s lymphoma, antiviral therapy, chemotherapy.
2. Monteverde A, Rivano MT, Allegra GC, et al. Essential mixed cryoglobulinemia, type II: a manifestation of a low grade malignant lymphoma? Clinical morphological study of 12 cases with special reference to immunohistoclinical findings in liver frozen section. Acta Haematol. 1988;79:20-5.
3. Monteverde A, Ballare M, Pileris S. Hepatic lymphoid aggregates in chronic hepatitis C and mixed cryoglobulinemia. Springer Semin Immunopathol. 1997;19:99-110.
4. 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;15:2078-85.
5. De Sanjose S, Benavente Y, Vajdic CM, Engels EA, Morton LM, et al. Hepatitis C and non-Hodgkin lymphoma among 4784 cases and 6269 controls from the International Lymphoma Epidemiology Consortium. Clin Gastroenterol Hepatol. 2008;6:451-8.
6. Giordano TP, Henderson L, Langren O. Risk of non-Hodgkin lymphoma and lymphoproliferative precursor diseases in US veterans with hepatitis C virus. JAMA. 2007;18:2010-7.
7. 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-Hodgkins lymphoma. Eur J Gastroenterol Hepatol. 2004; 16:135-8.
8. Gisbert JP, Garcia-Buey L, Pajares JM, Moreno-Otero R. Prevalence of hepatitis C virus infection in B-cell non-Hodgkins lymphoma: systematic review and meta-analysis. Gastroenterology. 2003;125:1723-32.
9. Matsuo K, Kusano A, Sugumar A, Nakamura S, Tajima K, Mueller NE. Effect of hepatitis C virus infection on the risk of non-hodgkins lymphoma: A meta-analysis of epidemiological studies. Cancer Sci. 2004; 95:745-52.
10. Mele A, Pulsoni A, Bianco E, Musto P, Szklo A, et al. Hepatitis C virus and B-cell non-Hodgkin lymphomas: an Italian multicenter case-control study. Blood. 2003;102:996-9.
11. Monti G, Pioltelli P, Saccardo F, Campanini M, Candela M, et al. Incidence and characteristics of non-Hodgkin lymphomas in a multicenter case of patients with hepatitis C virus-related symptomatic mixed cryoglobulinemia. Arch Intern Med. 2005;165:101-5.
12. Pozzato G, Mazzaro C, Crovatto M, Modolo ML, Ceselli S, Mazzi G, et al. Low-grade malignant lymphoma, hepatitis C virus infection, and mixed cryoglobulinemia. Blood. 1994;84:3047-53.
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23. Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F, Petracca R, et al. Binding of hepatitis C virus to CD81. Science. 1998;282:938-41.
24. Zuckerman E, Slobodin G, Kessel A, Sabo E, Yeshurun D, Halas K, et al. Peripheral B-cell CD5 expansion and CD81 overexpression and their association with disease severity and autoimmune markers in chronic hepatitis C virus infection. Clin Exp Immunol. 2002;128:353-8.
25. Carter RH, Fearon DT. CD19: lowering the threshold for antigen receptor stimulation of B lymphocytes. Science. 1992;256:105-7.
26. Matsumoto AK, Martin DR, Carter RH, Klickstein LB, Ahearn JM, Fearon DT. Functional dissection of the CD21/CD19/Leu-13 complex of B lymphocytes. J Exp Med. 1993;178:1407-17.
27. Rosa D, Saletti G, de Gregorio E, Zorat F, Comar C, et al. Activation of naïve B lymphocytes via CD81, a pathogenetic mechanism for hepatitis C virus-associated B lymphocyte disorders. Proc Natl Acad Sci USA. 2005;102:18544-9.
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36. Conca P, Tarantino G. Hepatitis C virus lymphotropism and peculiar immunological phenotype: effect on natural history and antiviral therapy. World J Gastroenterol. 2009;15:2305-8.
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41. Zignego AL, Giannelli F, Marrocchi ME, Mazzocca A, Ferri C, Giannini C, et al. T(14;18) translocation in chronic hepatitis C virus infection. Hepalology. 2000;31:474-9.
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1. Shultz DR, Yunis AA. Immunoblastic lymphadenopathy with mixed cryoglobulinemia. A detailed case study. N Engl J Med. 1975 Jan 2; 292(1):8-12.
2. Monteverde A, Rivano MT, Allegra GC, et al. Essential mixed cryoglobulinemia, type II: a manifestation of a low grade malignant lymphoma? Clinical morphological study of 12 cases with special reference to immunohistoclinical findings in liver frozen section. Acta Haematol. 1988;79:20-5.
3. Monteverde A, Ballare M, Pileris S. Hepatic lymphoid aggregates in chronic hepatitis C and mixed cryoglobulinemia. Springer Semin Immunopathol. 1997;19:99-110.
4. 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;15:2078-85.
5. De Sanjose S, Benavente Y, Vajdic CM, Engels EA, Morton LM, et al. Hepatitis C and non-Hodgkin lymphoma among 4784 cases and 6269 controls from the International Lymphoma Epidemiology Consortium. Clin Gastroenterol Hepatol. 2008;6:451-8.
6. Giordano TP, Henderson L, Langren O. Risk of non-Hodgkin lymphoma and lymphoproliferative precursor diseases in US veterans with hepatitis C virus. JAMA. 2007;18:2010-7.
7. 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-Hodgkins lymphoma. Eur J Gastroenterol Hepatol. 2004; 16:135-8.
8. Gisbert JP, Garcia-Buey L, Pajares JM, Moreno-Otero R. Prevalence of hepatitis C virus infection in B-cell non-Hodgkins lymphoma: systematic review and meta-analysis. Gastroenterology. 2003;125:1723-32.
9. Matsuo K, Kusano A, Sugumar A, Nakamura S, Tajima K, Mueller NE. Effect of hepatitis C virus infection on the risk of non-hodgkins lymphoma: A meta-analysis of epidemiological studies. Cancer Sci. 2004; 95:745-52.
10. Mele A, Pulsoni A, Bianco E, Musto P, Szklo A, et al. Hepatitis C virus and B-cell non-Hodgkin lymphomas: an Italian multicenter case-control study. Blood. 2003;102:996-9.
11. Monti G, Pioltelli P, Saccardo F, Campanini M, Candela M, et al. Incidence and characteristics of non-Hodgkin lymphomas in a multicenter case of patients with hepatitis C virus-related symptomatic mixed cryoglobulinemia. Arch Intern Med. 2005;165:101-5.
12. Pozzato G, Mazzaro C, Crovatto M, Modolo ML, Ceselli S, Mazzi G, et al. Low-grade malignant lymphoma, hepatitis C virus infection, and mixed cryoglobulinemia. Blood. 1994;84:3047-53.
13. Talamini R, Montella M, Crovatto M, Dal Maso Crispo A, Negri E, et al. Non-hodgkins lymphoma and hepatitis C virus: A case-control study from northern and southern Italy. Int J Cancer. 2004;110:380-5.
14. 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;29:1259-61.
15. Ferri C, Sebastiani M, Giuggioli D, Colaci M, Antonelli A, Zignego AL. Hepatitis C virus syndrome: A constellation of organ- and non-organ specific autoimmune disorders, B-cell non-Hodgkins lymphoma, and cancer. W J Hepatol. 2015;7(3):327-43.
16. Nieters A, Kallinowski B, Brennan P, Ott M, et al. Hepatitis c virus and risk of lymphoma:results of the European multicenter case-control study EPILYMPH. Gastroenterology. 2006;131:1879-86.
17. [Lepkov V, Storozhakov GI, Kosyura SD, et al. Chronic viral hepatitis C and lymphoproliferative diseases. Sovremennaya Onkologiya. 2006;(2):57-60 (In Russ.)].
18. Sung VM, Shimodaira S, Doughty AL, Picchio GR, Can H, Yen TS, et al. Establishment of B-cell lymphoma cell lines persistently infected with hepatitis C virus in vivo and in vitro: the apoptotic effects of virus infection. J Virol. 2003;77:2134-46.
19. Lanford RE, Chavez D, Chisari FV, Sureau C. Lack of detection of negative-strand hepatitis C virus RNA in peripheral blood mononuclear cells and other extrahepatic tissues by the highly strand-specific rTth reverse transcriptase PCR. J Virol. 1995;69:8079-83.
20. Lerat H, Berby F, Trabaud MA, Vidalin O, Major M, Trepo C, et al. Specific detection of hepatitis C virus minus strand RNA in hematopoietic cells. J Clin Invest. 1996;97:845-51.
21. Peveling-Oberhag J, Arcani L, Yasmann M-L, Zeuzem S. Hepatitis C-associated B-cell non-Hodgkin Lymphomas. Epidemiology, molecular signature and clinical management. J Hepatol. 2013;59:169-77.
22. Allander T, Drakenberg K, Beyene A, Rosa D, Abrignani S, Houghton M, et al. Recombinant human monoclonal antibodies against different conformational epitopes of the E2 envelope glycoprotein of hepatitis C virus that inhibit its interaction with CD81. J Gen Virol. 2000;81:2451-9.
23. Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F, Petracca R, et al. Binding of hepatitis C virus to CD81. Science. 1998;282:938-41.
24. Zuckerman E, Slobodin G, Kessel A, Sabo E, Yeshurun D, Halas K, et al. Peripheral B-cell CD5 expansion and CD81 overexpression and their association with disease severity and autoimmune markers in chronic hepatitis C virus infection. Clin Exp Immunol. 2002;128:353-8.
25. Carter RH, Fearon DT. CD19: lowering the threshold for antigen receptor stimulation of B lymphocytes. Science. 1992;256:105-7.
26. Matsumoto AK, Martin DR, Carter RH, Klickstein LB, Ahearn JM, Fearon DT. Functional dissection of the CD21/CD19/Leu-13 complex of B lymphocytes. J Exp Med. 1993;178:1407-17.
27. Rosa D, Saletti G, de Gregorio E, Zorat F, Comar C, et al. Activation of naïve B lymphocytes via CD81, a pathogenetic mechanism for hepatitis C virus-associated B lymphocyte disorders. Proc Natl Acad Sci USA. 2005;102:18544-9.
28. 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;38:360-3.
29. Cacoub P, Renou C, Kerr G, Hue S, Rosenthal E, et al. Influence of HLA-DR phenotype on the risk of hepatitis C virus-associated mixed cryoglobulinemia. Arthritis Rheum. 2001;44:2118-24.
30. Charles ED, Dustin LB. Hepatitis C virus induced cryoglobulinemia. Kidney Int. 2009;76(8):818-24.
31. De Re V, Caggiari L, Monti G, Libra M, Spina M, et al. HLA DR-DQ combination associated with the increased risk of developing human HCV positive non-Hodgkins lymphoma is related to the type II mixed cryoglobulinemia. Tissue Antigens. 2010;75:127-35.
32. [Ignatova TM, Milovanova SYu, Chernova OA. B-lymphoma in a patient with chronic hepatitis C and mixed cryoglobulinemia type II. Terapevticheskiy Arkhiv. 2011;3(4):69-71 (In Russ.)].
33. [Milovanova SYu, Ignatova TM, Kozlovskaya LV. Features of the course of chronic hepatitis C with cryoglobulinemia. Klinicheskaya Gepatologiya. 2006;2(1):15-8 (In Russ.)].
34. Agnello V, Zhang QX, Abel G, Knight GB. The association of hepatitis C virus infection with monoclonal rheumatoid factors bearing the WA cross-idiottype: implications for the etiopathogenesis and therapy of mixed cryoglobulinemia. Clin Exp Rheumatol. 1995;13:S101-4.
35. Chan CH, Hadlock KG, Foung SK, Levy S. V(H)1-69 gene is preferentially used by hepatitis c virus-associated B-cell lymphomas and by normal B cells responding to the E2 viral antigen. Blood. 2001; 97:1023-6.
36. Conca P, Tarantino G. Hepatitis C virus lymphotropism and peculiar immunological phenotype: effect on natural history and antiviral therapy. World J Gastroenterol. 2009;15:2305-8.
37. Agnello V, Chung RT, Kaplan LM. A role for hepatitis C virus infection in type II cryoglobulinemia. N Engl J Med. 1992;327:1490-5.
38. Fabris M, Quartuccio L, Sacco S, de Marchi G, Pozzato G, Mazzaro C, et al. B-Lymphocyte stimulator (BlyS) up-regulation in mixed cryoglobulinemia syndrome and hepatitis C virus infection. Rheumatology. 2007;46:37-43.
39. Kitay-Cohen Y, Amiel A, Hilzenrat N, Buskila D, Ashur Y, Fejgin M, et al. Bcl-2 rearrangement in patients with chronic hepatitis C associated with essential mixed cryoglobulinemia type II. Blood. 2000; 96:2910-2.
40. Libra M, Gloghini A, Malaponte G, Gangemi P, de Re V, Cacopardo B, et al. Association of t(14;18) translocation with HCV infection in gastrointestinal MALT lymphomas. J Hepatol. 2008;49:170-4.
41. Zignego AL, Giannelli F, Marrocchi ME, Mazzocca A, Ferri C, Giannini C, et al. T(14;18) translocation in chronic hepatitis C virus infection. Hepalology. 2000;31:474-9.
42. [Mixed cryoglobulinemia associated with chronic hepatitis C: importance in the development of extrahepatic manifestations, methods of treatment. Author's abstract. diss. ... Doct. Med Sci]. Moscow; 2013 (In Russ.)].
43. Sanjose S, Nieters A, Goedert JJ, et al. Role of hepatitis C virus infection in malignant lymphoma in Spain. Int J Cancer. 2005 Aug 10;111(1):81-5.
44. Zignego AL, Macchina D, Monti M, et al. Infection of peripheral mononuclear cells by hepatitis C virus. J Hepatol. 1992;15:382-6.
45. Zuckerman E, Zuckerman T, Sahar D, et al. Bcl-2 and immunoglobulin gene rearrangement in patients with hepatitis C virus infection.
Br J Haematol. 2001;112(2):364.
46. [Clinical recommendations for the diagnosis and treatment of non-Hodgkin's lymphomas in patients infected with hepatitis B and C. Hematological Society, Russian professional society of oncohematologists]. 2014 (In Russ.)].
47. Hermine O, Lefrere F, Bronowicki JP, Mariette X, Jondeu K, et al. Regression of splenic lymphoma with villous lymphocytes after treatment of hepatitis C virus infection. N Engl J Med. 2002; 347:89-94.
48. Kelaidi C, Rollot F, Park S, Tulliez M, Christoforov B, et al. Response to antiviral treatment in hepatitis C virus-associated marginal zone lymphomas. Leukemia. 2004;18:1711-6.
49. Mazzaro C, de Re V, Spina M, Dal Maso L, Festini G, Comar C, et al. pegylated-interferon plus ribavirin for HCV positive indolent non-Hodgkin lymphomas. Br J Haematol. 2009;145:255-7.
50. Vallisa D, Bernuzzi P, Arcaini L, Sacchi S, Callea V, Marasca R, et al. Role of anti-hepatitis C virus (HCV) treatment in HCV-related, low-grade, B-cell, non-Hodgkins lymphomas: a multicenter Italian experience. J Clin Oncol. 2005;23:468-73.
51. Arcaini L, Vallisa D, Rattotti S, 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(7):1404-10.
52. Michot JM, Canioni D, Driss H, Alric L, Cacoub P, 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(3):197-203.
53. Carrier P, Jaccard A, Tabouret T, Debette-Gratien M, Abraham J, et al. HCV-associated B-cell non-Hodgkin Lymphomas and new direct antiviral agents. Liver Int. 2015;35:2222-7.
54. Sultanik P, Klotz C, Brault P, Pol S, Mallet V. Regression of an HCV-associated disseminated marginal zone lymphoma under INF-free treatment. Blood. 2015;125:2446-7.
55. Rossotti R, et al. Hodgkin lymphomas and new direct antiviral agents. Liver Int. 2015;l.35(10):125-32.
56. Lim S, Wykeret B, Bartley K, Eisenhower D.Measurement
Error and Physical Activity. Am J Epidemiol. 2015;181(9):659-60.
doi: 10.1093/aje/kwu473
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А.В. Русских 2, Н.А. Мухин 1
1 ФГАОУ ВО «Первый Московский государственный медицинский университет им. И.М. Сеченова Минздрава России (Сеченовский Университет), Москва, Россия;
2 Клинический госпиталь ФКУЗ «Медико-санитарная часть МВД России по г. Москве», Москва, Россия
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S.Yu. Milovanova 1, L.V. Lysenko (Kozlovskaya) 1, L.Yu. Milovanova 1, N.N. Mrykhin 1, A.V. Russkih 2, N.A. Muchin 1
1 I.M. Sechenov First Moscow State Medical Univesity, Ministry Health of Russia (Sechenov University), Moscow, Russia;
2 Clinical Hospital of Moscow Department of Ministry of Internal Affairs of the Russian Federation Health care Unit, Moscow, Russia