Cryoglobulinemic vasculitis associated with HCV infection: still a problem?
S. Yu. Milovanova,
L. V. Lysenko (Kozlovskaya),
L. Yu. Milovanova,
D. T. Abdurahmanov,
M. V. Taranova,
A. V. Volkov https://doi.org/10.36485/1561-6274-2022-26-3-30-39
Abstract
The review presents the main data on the problem of cryoglobulinemic vasculitis associated with HCV infection. The options for the course are considered, and modern diagnostic criteria, the choice of tactics, and the effectiveness of various treatment regimens are presented. The use of modern antiviral drugs makes it possible to achieve the eradication of the virus in 95 % of patients. However, in some patients, clinical and immunologic markers of vasculitis persist despite viral clearance. The article discusses the concept that the persistence of B-cell clones after achieving a sustained virological response may underlie the pathogenesis of HCV-independent CV reactivation.
About the Authors
S. Yu. Milovanova
First Moscow State Medical University named after I. I. Sechenov (Sechenov University)
Russian Federation
Russian Federation
Svetlana Yu. Milovanova, Professor, Doctor of Medical Sciences
Department of Internal, Occupational Diseases and Rheumatology
119435
Rossolimo str., 11, b. 4-5
Moscow
tel. +79031435050
L. V. Lysenko (Kozlovskaya)
First Moscow State Medical University named after I. I. Sechenov (Sechenov University)
Russian Federation
Russian Federation
Lydia V. Lysenko (Kozlovskaya), Doctor of Medical Sciences
Department of Internal, Occupational Diseases and Rheumatology
119435
Rossolimo str., 11, b. 4-5
Moscow
phone: +79163044629
L. Yu. Milovanova
First Moscow State Medical University named after I. I. Sechenov (Sechenov University)
Russian Federation
Russian Federation
Lyudmila Yu. Milovanova, Professor, Doctor of Medical Sciences
Department of Internal, Occupational Diseases and Rheumatology
119435
Rossolimo str., 11, b. 4-5
Moscow
phone: +79161641400
D. T. Abdurahmanov
First Moscow State Medical University named after I. I. Sechenov (Sechenov University)
Russian Federation
Russian Federation
Jamal T. Abdurakhmanov, Professor, Doctor of Medical Sciences
Department of Internal, Occupational Diseases and Rheumatology
119435
Rossolimo str., 11, b. 4-5
Moscow
phone: +79262803431
M. V. Taranova
First Moscow State Medical University named after I. I. Sechenov (Sechenov University)
Russian Federation
Russian Federation
Marina V. Taranova, Associate Professor, Candidate of Medical Sciences
Department of Internal, Occupational Diseases and Rheumatology
119435
Rossolimo str., 11, b. 4-5
Moscow
phone: +79166151255
A. V. Volkov
First Moscow State Medical University named after I. I. Sechenov (Sechenov University)
Russian Federation
Russian Federation
Alekseй V. Volkov, Associate professor, MD, PhD
Department of Psychiatry and Narcology
119435
ul. Rossolimo, D. 11, b. 9
Moscow
phone: +79035892937
References
1. World Health Organization. Global hepatitis report 2017. Geneva: WHO. 2017; 83
2. World Health Organization. Guidelines for the care and treatment of persons diagnosed with chronic hepatitis C virus infection: July 2018. Geneva: WHO. 2018; 108
3. Игнатова Т. М. Внепеченочные проявления хронического гепатита C / Т. М. Игнатова // Тер Арх. – 1998. – 70 (11): 9–16 / Ignatova T. M. Extrahepatic manifestation of chronic hepatitis C virus infection. Ter Arh 1998; 70 (11): 9–16
4. Gorevic P. D., Kassab H. J., Levo Y. et al. Mixed cryoglobulinemia: Clinical aspects and long-term follow-up of 40 patients. Am J Med 1980; 69: 287–308. doi: 10.1016/0002-9343(80)90390-3
5. Zignego A. L., Giannelli F., Marrocchi M. E. et al. T(14;18) translocation in chronic hepatitis C virus infection. Hepatology 2000; 31 (2): 474–479. doi:10.1002/HEP.510310230
6. Meltzer M., Franklin E. C., Elisa K. et al. Cryoglobulinemia – a clinical and laboratory study. II. Cryoglobulins with rheumatoid factor activity. Am J Med 1966; 40:837–856. doi: 10.1016/0002-9343(66)90200-2
7. Brouet J. C., Clouvel J. P., Danon F et al. Biologic and clinical significance of cryoglobulins. Am J Med 1974; 57: 775–788. doi: 10.1016/0002-9343(74)90852-3
8. Lauletta G., Russi S., Conteduca V. et al. Impact of cryoglobulinemic syndrome on the outcome of chronic hepatitis C virus infection: a 15 – year prospective study. Medicine (Baltimore) 2013; 92 (5): 245–256. doi: 10.1097/MD.0b013e31829d2abc
9. Dammacco F., Lauletta G., Russi S., Leone P. et al. Clinical practice: hepatitis C virus infection? Cryoglobulinemia and cryoglobulinemic vasculitis. Clinical and Experimental medicine 2019; 19: 1–21. doi: 10.1007/s10238-018-0536-z
10. Casato M., Taliani G., Pucillo L. P. et al. Cryoglobulinemia and hepatitis C virus. Lancet 1991; 337 (8748): 1047–1048. doi: 10.1016/0140-6736(91)92715-e
11. Charles E. D., Dustin L. B. Hepatitis C virus induced cryoglobulinemia. Kidney Int 2009; 76 (8): 818–824. doi: 10.1038/ki.2009.247
12. Ferri C. Mixed cryoglobulinemia. Orphanet J of Rare 2008; 3: 25. doi: 10.1186/1750-1172-3-25
13. Тэгай С. В. Поражение почек, ассоциированное с вирусами гепатитов В и С / С. В. Тэгай [и др.] // Consilium Med. – 2002. – 4 (7): 337–341 / Tegai S. V., Lopatkina T. N., Kosminkova E. N. et al. Kidney disease associated with hepatitis C and B. Consilium Med 2002; 4 (7): 337–341
14. Милованова С. Ю. Особенности течения хронического гепатита С с криоглобулинемией / С. Ю. Милованова, Т. М. Игнатова, Л. В. Козловская // Клиническая гепатология. – 2006. – 2 (1): 15–18 / Milovanova S. Y., Ignatova T. M., Kozlovskaya L. V. Flow features of Chronic hepatits C with cryoglobulinemia. Clinical hepat 2006; 2 (1): 15–18
15. Игнатова Т. М. Криоглобулинемический васкулит, ассоциированный с вирусом гепатита С: 20-летний опыт лечения / Т. М. Игнатова [и др.] // Тер арх. – 2017. – 5: 46–52. doi: 10.17116/terarkh201789546-52 / Ignatova T. M., Lysenko (Kozlovskaya) L. V., Gordovskay N. B. et al. Hepatitis C virus-associated cryoglobulinemic vasculitis: A 20-year experience with treatment. Ter arh 2017; 5: 46–52. doi: 10.17116/terarkh201789546-52
16. Ferri C., Mascia M. T. et al. Cryoglobulinemic vasculitis: Review. Curr Opin Rheumatol 2006; 18: 54–63. doi: 10.1097/01.bor.0000198002.42826.c2
17. Zignego A. L., Wojcik G. L., Cacoub P. et al. Genome-wide association study of hepatitis C virus- and cryoglobulin-related vasculitis. Genes Immun 2014; 15: 500–505. doi: 10.1038/gene.2014.41
18. Artemova M., Abdurakhmanov D., Krasnova T., Mukhin N. Digestive and Liver. Disease 2018; 50: 318–320. doi: https://doi.org/10.1016/j.dld.2017.11.021
19. Fabris M., Quartuccio L., Sacco S., De Marchi G., Pozzato G., Mazzaro C. et al. B-Lymphocyte stimulator (BlyS) upegulation in mixed cryoglobulinemia syndrome and hepatitis C virus infection. Rheumatology 2007; 46: 37–43. doi: 10.1093/rheumatology/kel174
20. Saadoun D., Landau D. A., Calabrese L. H., Cacoub P. Hepatitis C-associated mixed cryoglobulinemia: a crossroad between autoimmunity and lymphoproliferation. Rheumatology 2007; 46: 1234–1242. doi: 10.1093/rheumatology/kem132
21. 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: 2910–2912. doi: https://doi.org/10.1182/blood.V96.8.2910
22. Zignego A. L., Ramos-Casals M., Ferri C., Saadoun D. et al. International therapeutic guidelines for patients with HCV-related extrahepatic disorders. A multidisciplinary expert statement. Autoimmun Rev 2017;16(5):523–541. doi: 10.1016/j.autrev.2017.03.004
23. Jennette J. C., Falk R. J., Bacon P. A. et al. 2012 revised International Chapel Hill Consensus Conference Nomenclature of Vasculitides. Artritis rheum 2013; 65 (1): 1–11. doi: 10.1002/art.37715
24. Monaco S., Mariotto S., Ferrari S., Calabrese M. et al. Hepatits C virus-fssociated neurocognitive and neuropsychiatric disorders: advances in 2015. World J Gastroenterol 2015; 21: 11974–11983. doi: 10.3748/wjg.v21.i42.11974
25. McGuire B. M., Julian B. A., Bynon J. S. et al. Brief communication: Glomerulonephritis in patients with hepatitis C cirrhosis undergoing liver transplantation. Ann Intern Med 2006; 144: 735–741. doi: 10.7326/0003-4819-144-10-200605160-00007
26. Zackrison L. H., Katz P. Bronchiolitis obliterans organizing pneumonia associated with ssential mixed cryoglobulinemia. Arthritis Rheum 1993; 36: 1627–1630. doi: 10.1002/art.1780361119
27. Terrier B., Saadoun D., Sène D., Scerra S., Musset L., Cacoub P. Presentation and outcome of gastrointestinal involvement in hepatitis C virus-related systemic vasculitis: a case-control study from a single-centre cohort of 163 patients. Gut 2010; 59: 1709–15.51. doi: 10.1136/gut.2010.218123
28. Cacoub P., Saadoun D. Hepatitis C virus infection induced vasculitis. Clin Rev Allergy Immunol 2008; 35: 30–39. doi: 10.1007/s12016-007-8070-x
29. Karras A., Potier L., Reboux A. H., Coldea N., Perdrix L., Jacquot C. et al. Cryoglobulin-induced cardiomyopathy. J Am Coll Cardiol 2010; 55: e13. doi: 10.1016/j.jacc.2009.09.042
30. Terrier B., Karras A., Cluzel P., Collet J. P., Sène D., Saadoun D., et al. Presentation and prognosis of cardiac involvement in hepatitis C virus-related vasculitis. Am J Cardiol 2013; 111: 265–272. doi: 10.1016/j.amjcard.2012.09.028
31. Lormeau C., Falgarone G., Roulot D., Boissier M. C. Rheumatologic manifestations of chronic hepatitis C infection. Joint Bone Spine 2006; 73: 633–638. doi: 10.1016/j.jbspin.2006.05.005
32. Ferri C., Sebastiani M., Antonelli A., Colaci M., Manfredi A., Giug-gioli D. Current treatment of hepatitis C-associated rheumatic diseases. Arthritis Res Ther 2012; 14: 215. doi: 10.1186/ar3865
33. Fiore C. E., Riccobene S., Mangiafico R., Santoro F., Pennisi P. Hepatitis C-associated osteosclerosis (HCAO): report of a new case with involvement of the OPG/RANKL system. Osteoporos Int 2005; 16: 2180-2184. doi: 10.1007/s00198-005-1858-8
34. Manganelli P., Giuliani N., Fietta P., Mancini C., Lazzaretti M., Pollini A. et al. OPG/RANKL system imbalance in a case of hepatitis C-associated osteosclerosis: the pathogenetic key? Clin Rheumatol 2005; 24: 296–300. doi: 10.1007/s10067-004-1031-3
35. De Sanjose S., Benavente Y., Vajdic C. M., Engels E. A., Morton L. M., Bracci P. M. 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: 451–458. doi: 10.1016/j.cgh.2008.02.011
36. Iqbal T., Mahale P., Turturro F., Kyvernitakis A., Torres H. A. Prevalence and association of hepatitis C virus infection with different types of lymphoma. Int J Cancer 2016; 138: 1035-1037. doi: 10.1002/ijc.29845
37. Милованова С. Ю., HCV-ассоциированная смешанная криоглобулинемия и В-клеточная неходжкинская лимфома – патогенетически связанные проблемы / С. Ю. Милованова [и др.] // Тер арх. – 2018. – 6112–6121. URL: https://cyberleninka.ru/article/n/hcv-assotsiirovannaya-smeshannaya-krioglobulinemiya-i-v-kletochnaya-nehodzhkinskaya-limfoma-patogeneticheski-svyazannye-problemy?ysclid=l7ubspd3wi568301613 / Milovanova S. Y., Lysenko (Kozlovskay) L. V., Milovanova L. Y. et al. HCV-associated mixed cryoglobulinemia and B-cell non-Hodgkin`s Lymphoma – pathogenetically related problems. Ter arh 2018; 6112–6121. URL: https://cyberleninka.ru/article/n/hcv-assotsiirovannaya-smeshannaya-krioglobulinemiya-i-v-kletochnaya-nehodzhkinskaya-limfoma-patogeneticheski-svyazannye-problemy?ysclid=l7ubspd3wi568301613
38. Nesterova E., Tanaschuk E., Abdurakhmanov D. et al. Hematological Oncology 2020; 38:604–606. doi: 10.1002/hon.2751
39. Evidence – based recommendations on the management of extrahepatic manifestations of chronic hepatitis C virus infection. J Hepatology 2017; 66 (6): 1282–1299. doi: 10.1016/j.jhep.2017.02.010
40. Ferri C., Sebastiani M., Antonelli A. et al. Current treatment of hepatitis C-associated rheumatic diseases. Arthritis Res Ther 2012; 14: 215–221. doi: 10.1186/ar3865
41. Bonacci M., Lens S., Londoño M. C., Mariño Z., Cid M. C., Ramos-Casals M. et al. Virologic, clinical, and immune response outcomes of patients with hepatitis C virus-associated cryoglobulinemia treated with direct-acting antivirals. Clin Gastroenterol Hepatol 2017; 15: 575–583. doi: 10.1016/j.cgh.2016.09.158
42. Gragnani L., Visentini M., Fognani E., Urraro T., De Santis A., Petraccia L., et al. Prospective study of guideline-tailored therapy with direct-acting antivirals for hepatitis C virus-associated mixed cryoglobulinemia. Hepatology 2016; 64:1473–1482. doi: 10.1002/hep.28753
43. Emery J. S., Kuczynsky M., La D. et al. Efficacy and safety of direct acting antiviral for the treatment of mixed cryoglobulinemia. Am J Gastroenterol 2017; 112: 1298–1308. doi: 10.1038/ajg.2017.49
44. Saadoun D., Pol S., Ferfar Y. et al. Efficacy and safety of sofosbuvir plus daclatasvir for treatment of HCV-associated cryoglobulinemia vasculitis. Gastroenterol Hepatol 2017; 15: 575–583. doi: 10.1053/j.gastro.2017.03.006
45. Gragnani L., Piluso A., Urraro T. et al. Virological and clinical response to interferon-free regimens in patients with HCV-related mixed cryoglobulinemia: preliminary results of a prospective pilot study. Curr drug Targets 2017; 18: 772–785. doi: 10.2174/1389450117666160208145432
46. Van der Meer A. J., Veldt B. J., Feld J. J., Wedemeyer H., Dufour J. F., Lammert F., et al. Association between sustained virological response and all-cause mortality among patients with chronic hepatitis C and advanced hepatic fibrosis. JAMA 2012; 308: 2584–93.104. doi: 10.1001/jama.2012.144878
47. Saadoun D., Thibault V., Ahmed S. N. S. et al. Sofosbuvir plus ribavirin for hepatitis C virus-associated cryoglobulinemia vasculitis: VASCUVALDIC study. Ann Rheum Dis 2015; 75: 1777–1782. doi: 10.1136/annrheumdis-2015-208339
48. Sollima S., Milazzo L., Peri A. M., Torre A., Antinori S., Galli M. Persistent mixed cryoglobulinaemia vasculitis despite hepatitis C virus eradication after interferon-free antiviral therapy. Rheuatology (Oxford) 2016; 55: 2084–2085. doi: 10.1093/rheumatology/kew268
49. M. L. Zubkin, D. T. Abdurakhmanov, O. I. Sagalova et al. Scandinavian J of Gastroenterology 2018; 53 (7): 883–884
50. Pozzato G., Mazzaro C., Artemova M. et al. Direct-acting antiviral agents for hepatitis C virus-mixed cryoglobulinaemia: dissociated virological and haematological responses. British Journal of Haematology 2020; 191: 775–783. doi: 10.1111/bjh.17036
51. Visentini M., Conti V., Cagliuso M., Siciliano G. et al. Persistence of a large population of exhausted monoclonal B cells in mixed cryoglobuliemia after the eradication of hepatitis C virus infection. J Clin Immunol 2012 Aug; 32 (4): 729–735. doi: 10.1007/s10875-012-9677-0
52. Bonacci M., Lens S., Londoño M. C., Mariño Z., Cid M. C., Ramos-Casals M. et al. Virologic, clinical, and immune response outcomes of patients with hepatitis C virus-associated cryoglobulinemia treated with direct-acting antivirals. Clin Gastroenterol Hepatol 2017; 15: 575–583. doi: 10.1016/j.cgh.2016.09.158
53. Cacoub P., Delluc A., Saadoun D. et al. Anti-CD20 monoclonal antibody (rituximab) treatment for cryoglobulinemic vaskulitis: where do we stand? Ann Rheum Dis 2008; 67 (3): 283–287. doi: 10.1136/ard.2006.065565
54. Comarmond C., Garrido M., Pol S. et al. Direct-acting antiviral therapy restores immune tolerance to patients with hepatitis C virus-induced cryoglobulinemia vasculitis. Gastroenterology 2017; 152: 2052–2062. doi: 10.1053/j.gastro.2017.02.037
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For citations:
Milovanova S.Yu., Lysenko (Kozlovskaya) L.V., Milovanova L.Yu., Abdurahmanov D.T., Taranova M.V., Volkov A.V. Cryoglobulinemic vasculitis associated with HCV infection: still a problem? Nephrology (Saint-Petersburg). 2022;26(3):30-39. (In Russ.) https://doi.org/10.36485/1561-6274-2022-26-3-30-39
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