Systemic lupus erythematosus: new horizons for diagnosis and therapy
https://doi.org/10.14412/1995-4484-2020-5-14
Abstract
Systemic lupus erythematosus (SLE) is a systemic autoimmune rheumatic disease of unknown etiology, characterized by the overproduction of organ-specific autoantibodies to various components of the cell nucleus and by the development of immune-mediated inflammatory damage to internal organs. SLE is the prototype of a systemic human autoimmune disease; it is an extremely heterogeneous disease in terms of both clinical manifestations and a genetic predisposition and pathogenetic mechanisms, which often complicates the early diagnosis of the diseases and makes it impossible to personify therapy. Despite the fact that in the 21st century, the 15-year survival rate for SLE has increased up to 85%, the inadequate control of disease activity and the need for almost constant intake of glucocorticoids and immunosuppressive drugs result in the accrual of irreversible damages to internal organs and, as a consequence, in decreases in quality of life, disability, social maladaptation, and premature death. The paper considers the new 2019 EULAR/ACR diagnostic criteria for SLE, the contemporary 2019 EULAR recommendations for the management of SLE, and new pharmacotherapy options for this condition, which are based on the deciphering of the mechanisms of SLE immunopathogenesis.
About the Authors
S. K. Solovyev
V.A. Nasonova Research Institute of Rheumatology
Russian Federation
Competing Interests:
Russian Federation
34A, Kashirskoe Shosse, Moscow 115522
Competing Interests:
гонорары за консультационные услуги в области научной и педагогической деятельности (образовательные услуги, научные статьи, участие в экспертных советах, участие в исследованиях и др.)
E. A. Aseeva
V.A. Nasonova Research Institute of Rheumatology
Russian Federation
Competing Interests:
Russian Federation
34A, Kashirskoe Shosse, Moscow 115522
Competing Interests:
гонорары за консультационные услуги в области научной и педагогической деятельности (образовательные услуги, научные статьи, участие в экспертных советах, участие в исследованиях и др.)
T. V. Popkova
V.A. Nasonova Research Institute of Rheumatology
Russian Federation
Competing Interests:
Russian Federation
34A, Kashirskoe Shosse, Moscow 115522
Competing Interests:
гонорары за консультационные услуги в области научной и педагогической деятельности (образовательные услуги, научные статьи, участие в экспертных советах, участие в исследованиях и др.)
A. M. Lila
V.A. Nasonova Research Institute of Rheumatology; Russian Medical Academy of Continuing Professional Education, Ministry of Health of Russia
Russian Federation
Competing Interests:
Russian Federation
34A, Kashirskoe Shosse, Moscow 115522; 2/1, Barrikadnaya St., Build. 1, Moscow 125993
Competing Interests:
гонорары за консультационные услуги в области научной и педагогической деятельности (образовательные услуги, научные статьи, участие в экспертных советах, участие в исследованиях и др.)
V. I. Mazurov
I.I. Mechnikov NorthWestern State Medical University, Ministry of Health of Russia
Russian Federation
Competing Interests:
Russian Federation
41, Kirochnaya St., Saint Petersburg 191015
Competing Interests:
гонорары за консультационные услуги в области научной и педагогической деятельности (образовательные услуги, научные статьи, участие в экспертных советах, участие в исследованиях и др.)
E. L. Nasonov
V.A. Nasonova Research Institute of Rheumatology; I.M. Sechenov First Moscow State Medical University (Sechenov University), Ministry of Health of Russia
Russian Federation
Competing Interests:
Russian Federation
Evgeny Nasonov
34A, Kashirskoe Shosse, Moscow 115522; 8, Trubetskaya St., Build. 2, Moscow 119991
Competing Interests:
гонорары за консультационные услуги в области научной и педагогической деятельности (образовательные услуги, научные статьи, участие в экспертных советах, участие в исследованиях и др.)
References
1. Kaul A, Gordon C, Crow MK, et al. Systemic lupus erythematosus. Nat Rev Dis Primers. 2016;2:16039. doi: 10.1038/nrdp.2016.39
2. Nasonov EL, editor. Systemic lupus erythematosus. In: Rossiiskie klinicheskie rekomendatsii [Russian clinical guidelines]. Moscow: GEOTAR-Media; 2017. P. 113-41 (In Russ.).
3. Tsokos GC, Lo MS, Costa Reis P, Sullivan KE. New insights into the immunopathogenesis of systemic lupus erythematosus. Nat Rev Rheumatol. 2016;12(12):716-30. doi: 10.1038/nrrheum.2016.186
4. Lo MS, Tsokos GC. Recent developments in systemic lupus erythematosus pathogenesis and applications for therapy. Curr Opin Rheumatol. 2018;30(2):222-8. doi: 10.1097/BOR.0000000000
5. Tektonidou MG, Lewandowski LB, Hu J, et al. Survival in adults and children with systemic lupus erythematosus: a systematic review and Bayesian meta-analysis of studies from 1950 to 2016. Ann Rheum Dis. 2017;76:2009-16. doi: 10.1136/annrheumdis-2017-211663
6. Tektonidou MG, Dasgupta A, Ward MM. Risk of end-stage renal disease in patients with lupus nephritis, 1971-2015: A systematic review and Bayesian meta-analysis. Arthritis Rheum. 2016;68(6):1432-41. doi: 10.1002/art.39594
7. Aringer M, Costenbader K, Daikh D, et al. 2019 European League Against Rheumatism/American College of Rheumatology classification criteria for systemic lupus erythematosus. Ann Rheum Dis. 2019;78(9):1151-9. doi: 10.1136/annrheumdis-2018-214819
8. Fanouriakis A, Kostopoulou M, Alunno A, et al. 2019 update of the EULAR recommendations for the management of systemic lupus erythematosus. Ann Rheum Dis. 2019;78(6):736-45. doi: 10.1136/annrheumdis-2019-215089
9. Gordon C, Amissah-Arthur MB, Gayed M, et al.; British Society for Rheumatology Standards, Audit and Guidelines Working Group. The British Society for Rheumatology guideline for the management of systemic lupus erythematosus in adults. Rheumatology (Oxford). 2018;57(1):e1-e45. doi: 10.1093/rheuma-tology/kex286
10. Pons-Estel BA, Bonfa E, Soriano ER, et al. First Latin American clinical practice guidelines for the treatment of systemic lupus erythematosus: Latin American Group for the Study of Lupus (GLADEL, Grupo Latino Americano de Estudio del Lupus) — Pan-American League of Associations of Rheumatology (PANLAR). Ann Rheum Dis. 2018 Nov;77(11):1549-57. doi: 10.1136/annrheumdis-2018-213512
11. Tektonidou MG, Andreoli L, Limper M, et al. EULAR recommendations for the management of antiphospholipid syndrome in adults. Ann Rheum Dis. 2019;78(10):1296-304. doi: 10.1136/annrheumdis-2019-215213
12. Hochberg MC. Updating the American College of rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1997;40(9):1725. doi: 10.1002/art.1780400928
13. Petri M, Orbai A-M, Alarcon GS, et al. Derivation and validation of the systemic lupus international collaborating clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum. 2012;64:2677-86. doi: 10.1002/art.34473
14. Leuchten N, Hoyer A, Brinks R, et al. Performance of antinuclear antibodies for classifying systemic lupus erythematosus: a systematic literature review and meta-regression of diagnostic data. Arthritis Care Res. 2018;70:428-38. doi: 10.1002/acr.23292
15. Choi MY, Clarke AE, St Pierre Y, et al. Antinuclear antibodynegative systemic lupus erythematosus in an international inception cohort. Arthritis Care Res (Hoboken). 2019;71(7):893-902. doi: 10.1002/acr.23712
16. Pisetsky DS, Bossuyt X, Meroni PL. ANA as an entry criterion for the classification of SLE. Autoimmun Rev. 2019 Oct 19:102400. doi: 10.1016/j.autrev.2019.102400
17. Agmon-Levin N, Damoiseaux J, Kallenberg C, et al. International recommendations for the assessment of autoantibodies to cellular antigens referred to as anti-nuclear antibodies. Ann Rheum Dis. 2014;73:17-23. doi: 10.1136/annrheumdis-2013-203863
18. Pisetsky DS, Spencer DM, Lipsky PE, Rovin BH. Assay variation in the detection of antinuclear antibodies in the sera of patients with established SLE. Ann Rheum Dis. 2018;77:911-3. doi: 10.1136/annrheumdis-2017-212599
19. Choi MY, Clarke AE, St Pierre Y, et al. The prevalence and determinants of anti-DFS70 autoantibodies in an international inception cohort of systemic lupus erythematosus patients. Lupus. 2017;26(10):1051-9. doi: 10.1177/0961203317692437
20. Mosca M, Costenbader KH, Johnson SR, et al. Brief report: How do patients with newly diagnosed systemic lupus erythematosus present? A multicenter cohort of early systemic lupus erythematosus to inform the development of new classification criteria. Arthritis Rheum. 2019;71(1):91-8. doi: 10.1002/art.40674
21. Qi S, Chen Q, Xu D, et al. Clinical application of protein biomarkers in lupus erythematosus and lupus nephritis. Lupus. 2018;27(10):1582-90. doi: 10.1177/0961203318773643
22. Nicolaou O, Kousios A, Hadjisavvas A, et al. Biomarkers of systemic lupus erythematosus identified using mass spectrometry-based proteomics: a systematic review. J Cell Mol Med. 2017;21(5):993-1012. doi: 10.1111/jcmm.13031
23. Van Vollenhoven RF, Mosca M, Bertsias G, et al. Treat-to-target in systemic lupus erythematosus: recommendations from an international task force. Ann Rheum Dis. 2014;73(6):958-67. doi: 10.1136/annrheumdis-2013-205139
24. Gatto M, Zen M, Iaccarino L, Doria A. New therapeutic strategies in systemic lupus erythematosus management. Nat Rev Rheumatol. 2019;15(1):30-48. doi: 10.1038/s41584-018-0133-2
25. Dorner T, Furie R. Novel paradigms in systemic lupus erythematosus. Lancet. 2019;393(10188):2344-58. doi: 10.1016/S0140-6736(19)30546-X
26. Durcan L, O'Dwyer T, Petri M. Management strategies and future directions for systemic lupus erythematosus in adults. Lancet. 2019;393(10188):2332-43. doi: 10.1016/S0140-6736(19)30237-5
27. Aseeva EA, Soloviev SK, Popkova TV, et al. Management of patients with systemic lupus erythematosus in real clinical practice. Nauchno-Prakticheskaya Revmatologiya = Rheumatology Science and Practice. 2019;57(2):191-6 (In Russ.). doi: 10.14412/1995-4484-2019-191-196
28. Franklyn K, Lau CS, Navarra SV, et al. Definition and initial validation of a lupus low disease activity state (LLDAS). Ann Rheum Dis. 2016;75:1615-21. doi: 10.1136/annrheumdis-2015-207726
29. Van Vollenhoven R, Voskuyl A, Bertsias G, et al. A framework for remission in SLE: consensus findings from a large international task force on definitions of remission in SLE (DORIS). Ann Rheum Dis. 2017;76:554-61. doi: 10.1136/annrheumdis-2016-209519
30. Soloviev SK, Aseeva EA, Zotkin EG, et al. Problems of low activity and remission in systemic lupus erythematosus. Nauchno-Prakticheskaya Revmatologiya = Rheumatology Science and Practice. 2019;57(2):218-21 (In Russ.). doi: 10.14412/1995-4484-2019-218-221
31. Felten R, Sagez F, Gavand PE, et al. 10 most important contemporary challenges in the management of SLE. Lupus Sci Med. 2019 Jan 10;6(1):e000303. doi: 10.1136/lupus-2018-000303
32. Ugarte A, Danza A, Ruiz-Irastorza G. Glucocorticoids and anti-malarials in systemic lupus erythematosus: an update and future directions. Curr Opin Rheumatol. 2018 Sep;30(5):482-9. doi: 10.1097/BOR.0000000000000527
33. Floris A, Piga M, Mangoni AA, et al. Protective effects of hydroxychloroquine against accelerated atherosclerosis in systemic lupus erythematosus. Mediat Inflamm. 2018 Feb 18;2018:3424136. doi: 10.1155/2018/3424136
34. Marmor MF, Kellner U, Lai TY, et al; American Academy of Ophthalmology. Recommendations on screening for chloroquine and hydroxychloroquine retinopathy (2016 revision). Ophthalmology. 2016;123:1386-94. doi: 10.1016/j.oph-tha.2016.01.058
35. Cain DW, Cidlowski JA. Immune regulation by glucocorticoids. Nat Rev Immunol. 2017;17(4):233-47. doi: 10.1038/nri.2017.1
36. Strehl C, Ehlers L, Gaber T, Buttgereit F. Glucocorticoids -all-rounders tackling the versatile players of the immune system. Front Immunol. 2019;10:1744. doi: 10.3389/fimmu.2019.01744
37. Apostolopoulos D, Kandane-Rathnayake R, Raghunath S, et al. Independent association of glucocorticoids with damage accrual in SLE. Lupus SciMed. 2016;3(1):e000157. eCollection 2016. doi: 10.1136/lupus-2016-000157
38. Sciascia S, Mompean E, Radin M, et al. Rate of adverse effects of medium- to high-dose glucocorticoid therapy in systemic lupus erythematosus: A systematic review of randomized control trials. Clin DrugInvestig. 2017;37(6):519-24. doi: 10.1007/s40261-017-0518-z
39. Ruiz-Irastorza G, Garcia M, Espinosa G, et al. First month prednisone dose predicts prednisone burden during the following 11 months: an observational study from the RELES cohort. Lupus Sci Med. 2016;3(1):e000153. doi: 10.1136/lupus-2016-000153
40. Singh JA, Hossain A, Kotb A, et al. Treatments for lupus nephritis: A systematic review and network metaanalysis. J Rheumatol. 2016;43(10):1801-15. doi: 10.3899/jrheum.160041
41. Lightstone L, Doria A, Wilson H, et al. Can we manage lupus nephritis without chronic corticosteroids administration? Independent association of glucocorticoids with damage accrual in SLE. Autoimmun Rev. 2018;17(1):4-10. doi: 10.1016/j.autrev.2017.11.002
42. Ruiz-Irastorza G, Ruiz-Estevez B, Lazaro E, et al. Prolonged remission in SLE is possible by using reduced doses of prednisone: An observational study from the Lupus-Cruces and Lupus-Bordeaux inception cohorts. Autoimmun Rev. 2019;18(9):102359. doi: 10.1016/j.autrev.2019.102359
43. Little J, Parker B, Lunt M, et al. Glucocorticoid use and factors associated with variability in this use in the systemic lupus international collaborating clinics inception cohort. Rheumatology. 2018;57:677-87. doi: 10.1093/rheumatology/kex444
44. Davidson A. Targeting BAFF in autoimmunity. Curr Opin Immunol. 2010;22(6):732-9. doi: 10.1016/j.coi.2010.09.010
45. Stohl W. The discovery and development of belimumab: the anti-BlyS-lupus connection. Nature Biotechnol. 2012;30:69-77. doi: 10.1038/nbt.2076
46. Nasonov EL, Reshetnyak TM, Denisov LN, et al. Belimumab: advances in drug therapy for systemic lupus erythematosus. Nauchno-Prakticheskaya Revmatologiya = Rheumatology Science and Practice. 2012;50(5):13-9 (In Russ.). doi: 10.14412/1995-4484-2012-1174
47. Jackson SW, Davidson A. BAFF inhibition in SLE-Is tolerance restored? Immunol Rev. 2019;292(1):102-19. doi: 10.1111/imr.12810
48. Yap DYH, Chan TM. B cell abnormalities in systemic lupus erythematosus and lupus nephritis - role in pathogenesis and effect of immunosuppressive treatments. Int J Mol Sci. 2019;20(24). doi: 10.3390/ijms20246231
49. Hamilton JA, Hsu HC, Mountz JD. Autoreactive B cells in SLE, villains or innocent bystanders? Immunol Rev. 2019;292(1):120-38. doi: 10.1111/imr.12815
50. Smulski CR, Eibel H. BAFF and BAFF-receptor in B Cell selection and survival. Front Immunol. 2018;9:2285. doi: 10.3389/fimmu.2018.02285
51. Vincent FB, Morand EF, Schneider P, Mackay F. The BAFF/APRIL system in SLE pathogenesis. Nat Rev Rheumatol. 2014;10(6):365-73. doi: 10.1038/nrrheum.2014.33
52. Bruce IN, Urowitz M, van Vollenhoven R, et al. Long-term organ damage accrual and safety in patients with SLE treated with beli-mumab plus standard of care. Lupus. 2016;25:699-709. doi: 10.1177/0961203315625119
53. Urowitz MB, Ohsfeldt RL, Wielage RC, et al. Organ damage in patients treated with belimumab versus standard of care: a propensity score-matched comparative analysis. Ann Rheum Dis. 2019;78:372-9. doi: 10.1136/annrheumdis-2018-214043
54. Trentin F, Gatto M, Zen M, et al. Effectiveness, tolerability, and safety of belimumab in patients with refractory SLE: a review of observational clinical-practice-based studies. Clin Rev Allergy Immunol. 2018;54(2):331-43. doi: 10.1007/s12016-018-8675-2
55. Stohl W. Inhibition of B cell activating factor (BAFF) in the management of systemic lupus erythematosus (SLE). Expert Rev Clin Immunol. 2017;13(6):623-33. doi: 10.1080/1744666X.2017.1291343
56. Bertsias GK, Tektonidou M, Amoura Z, et al. Joint European League Against Rheumatism and European Renal Association-European Dialysis and Transplant Association (EULAR/ERA-EDTA) recommendations for the management of adult and paediatric lupus nephritis. Ann Rheum Dis. 2012;71:1771-82. doi: 10.1136/annrheumdis-2012-201940
57. Hahn BH, McMahon MA, Wilkinson A, et al. American College of Rheumatology guidelines for screening, treatment, and management of lupus nephritis. Arthritis Care Res (Hoboken). 2012;64:797-808. doi: 10.1002/acr.21664
58. Houssiau FA, Vasconcelos C, D'Cruz D, et al. The 10-year follow-up data of the Euro-Lupus Nephritis Trial comparing low-dose and high-dose intravenous cyclophosphamide. Ann Rheum Dis. 2010;69:61-4. doi: 10.1136/ard.2008.102533
59. Lee YH, Song GG. Relative efficacy and safety of tacrolimus, mycophenolate mofetil, and cyclophosphamide as induction therapy for lupus nephritis: a Bayesian network meta-analysis of randomized controlled trials. Lupus. 2015;24:1520-8. doi: 10.1177/0961203315595131
60. Deng J, Xie H, Zhu L, et al. Maintenance therapy for lupus nephritis with mycophenolate mofetil or azathioprine. A metaanalysis. Clin Nephrol. 2019;91(3):172-9. doi: 10.5414/CN109450
61. Tunnicliffe DJ, Palmer SC, Henderson L, et al. Immunosuppressive treatment for proliferative lupus nephritis. Cochrane Database Syst Rev. 2018;6:CD002922. doi: 10.1002/14651858.CD002922.pub4
62. Allison AC, Eugui EM. Mycophenolate mofetil and its mechanisms of action. Immunopharmacology. 2000;47:85-118. doi: 10.1016/S0162-3109(00)00188-0
63. Mok CC. Calcineurin inhibitors in systemic lupus erythematosus. Best Pract Res Clin Rheumatol. 2017;31(3):429-38. doi: 10.1016/j.berh.2017.09.010
64. Palmer SC, Tunnicliffe DJ, Singh-Grewal D, et al. Induction and maintenance immunosuppression treatment of proliferative lupus nephritis: a network meta-analysis of randomized trials. Am J Kidney Dis. 2017;70:324-36.
65. Liu Z, Zhang H, Liu Z, et al. Multitarget therapy for induction treatment of lupus nephritis: a randomized trial. Ann Intern Med. 2015;162:18-26. doi: 10.7326/M14-1030
66. Zhang H, Liu Z, Zhou M, et al. Multitarget therapy for maintenance treatment of lupus nephritis. J Am Soc Nephrol. 2017;28:3671-8. doi: 10.1681/ASN.2017030263
67. Wong T, Goral S. Lupus nephritis and kidney transplantation: where are we today? Adv Chronic Kidney Dis. 2019;26(5):313-22. doi: 10.1053/j.ackd.2019.08.007
68. Almaani S, Rovin BH. B-cell therapy in lupus nephritis: an overview. Nephrol Dial Transplant. 2019;34(1):22-9. doi: 10.1093/ndt/gfy267
69. Nasonov EL, editor. Anti-B-kletochnaya terapiya v revmatologii: fokus na rituksimab [Anti-B cell therapy in rheumatology: focus on rituximab]. Moscow: IMA-PRESS; 2012. P. 119-52 (In Russ.).
70. Condon MB, Ashby D, Pepper RJ, et al. Prospective observational single-centre cohort study to evaluate the effectiveness of treating lupus nephritis with rituximab and mycophenolate mofetil but no oral steroids. Ann Rheum Dis. 2013;72(8):1280-6. doi: 10.1136/annrheumdis-2012-202844
71. Trouw LA, Pickering MC, Blom AM. The complement system as a potential therapeutic target in rheumatic disease. Nat Rev Rheumatol. 2017;13(9):538-47. doi: 10.1038/nrrheum.2017.125
72. Guillot M, Rafat C, Buob D, et al. Eculizumab for catastrophic antiphospholipid syndrome — a case report and literature review. Rheumatology (Oxford). 2018;57(11):2055-7. doi: 10.1093/rheumatology/key228
73. Nasonov EL, Solovyev SK. Prospects for pharmacotherapy of systemic lupus erythematosus. Nauchno-Prakticheskaya Revmatologiya = Rheumatology Science and Practice. 2014;52(3):311-21 (In Russ.). doi: 10.14412/1995-4484-2014-311-321
74. Chasset F, Arnaud L. Targeting interferons and their pathways in systemic lupus erythematosus. Autoimmun Rev. 2018;17(1):44-52. doi: 10.1016/j.autrev.2017.11.009
75. Nasonov EL, Avdeeva AS. Immunoinflammatory rheumatic diseases associated with type I interferon: new evidence. Nauchno-Prakticheskaya Revmatologiya = Rheumatology Science and Practice. 2019;57(4):452-61 (In Russ.). doi: 10.14412/1995-4484-2019-452-461
76. Morel L. Immunometabolism in systemic lupus erythematosus. Nat Rev Rheumatol. 2017;13(5):280-90. doi: 10.1038/nrrheum.2017
77. Schwartz DM, Kanno Y, Villarino A, et al. JAK inhibition as a therapeutic strategy for immune and inflammatory diseases. Nat Rev Drug Discov. 2017;16(12):843-62. doi: 10.1038/nrd.2017.201
78. Nasonov EL, Lila AM. Janus kinase inhibitors in immuno-inflammatory rheumatic diseases: new opportunities and prospects. Nauchno-Prakticheskaya Revmatologiya = Rheumatology Science and Practice. 2019;57(1):8-16 (In Russ.). doi: 10.14412/1995-4484-2019-8-16
79. Dorner T, Lipsky PE. Beyond pan-B-cell-directed therapy — new avenues and insights into the pathogenesis of SLE. Nat Rev Rheumatol. 2016;12:645-57. doi: 10.1038/nrrheum.2016.158
80. Chang HD, Tokoyoda K, Hoyer B, et al. Pathogenic memory plasma cells in autoimmunity. Curr Opin Immunol. 2019;61:86-91. doi: 10.1016/j.coi.2019.09.005
81. Sattwika PD, Mustafa R, Paramaiswari A, Herningtyas EH. Stem cells for lupus nephritis: a concise review of current knowledge. Lupus. 2018;27(12):1881-97. doi: 10.1177/0961203318793206
82. Ballesteros-Tato A, Papillion A. Mechanisms of action of low-dose IL-2 restoration therapies in SLE. Curr Opin Immunol. 2019 Dec;61:39-45. doi: 10.1016/j.coi.2019.07.003
83. Mizui M, Tsokos GC. Targeting Regulatory T Cells to Treat Patients With Systemic Lupus Erythematosus. Front Immunol. 2018;9:786. doi: 10.3389/fimmu.2018.00786
84. Kingsmore KM, Grammer AC, Lipsky PE. Drug repurposing to improve treatment of rheumatic autoimmune inflammatory diseases. Nat Rev Rheumatol. 2020;16(1):32-52. doi: 10.1038/s41584-019-0337-0
85. Ryden-Aulin M, Boumpas D, Bultink I, et al. Off-label use of rituximab for systemic lupus erythematosus in Europe. Lupus SciMed. 2016;3:e000163. doi: 10.1136/lupus-2016-000163
86. Merrill JT, Neuwelt CM, Wallace DJ, et al. Efficacy and safety of rituximab in moderately-to-severely active systemic lupus erythematosus: the randomized, double-blind, phase II/III systemic lupus erythematosus evaluation of rituximab trial. Arthritis Rheum. 2010;62(1):222-33. doi: 10.1002/art.27233
87. Rovin BH, Furie R, Latinis K, et al. Efficacy and safety of ritux-imab in patients with active proliferative lupus nephritis: the Lupus Nephritis Assessment with Rituximab study. Arthritis Rheum. 2012;64(4):1215-26. doi: 10.1002/art.34359
88. Isenberg DA, Merrill JT. Why, why, why de-lupus (does so badly in clinical trials). Expert Rev Clin Immunol. 2016;2:95-8. doi: 10.1586/1744666X.2016.1112270
89. Wallace DJ, Stohl W, Ginzler EM, et al. A phase II, randomized, double-blind, placebo-controlled, dose-ranging study of beli-mumab in patients with active systemic lupus erythematosus. Arthritis Rheum. 2009;61:1168-78. doi: 10.1002/art.24699
90. Furie RA, Petri MA, Wallace DJ, et al. Novel evidence-based systemic lupus erythematosus responder index. Arthritis Rheum. 2009;61:1143-51. doi: 10.1002/art.24698
91. Furie R, Wang L, Illei G, Drappa J. Systemic Lupus Erythematosus (SLE) Responder Index response is associated with global benefit for patients with SLE. Lupus. 2018;27(6):955-62. doi: 10.1177/0961203318758506
92. Nasonov EL. Prospects for anti-B-cell therapy in rheumatology. Nauchno-Prakticheskaya Revmatologiya = Rheumatology Science and Practice. 2018;56(5):539-48 (In Russ.). doi: 10.14412/1995-4484-2018-539-548
93. Md Yusof MY, Shaw D, El-Sherbiny YM, et al. Predicting and managing primary and secondary non-response to rituximab using B-cell biomarkers in systemic lupus erythematosus. Ann Rheum Dis. 2017 Nov;76(11):1829-36. doi: 10.1136/annrheumdis-2017-211191
94. Masoud S, McAdoo SP, Bedi R, et al. Ofatumumab for B cell depletion in patients with systemic lupus erythematosus who are allergic to rituximab. Rheumatology (Oxford). 2018 Mar 19. doi: 10.1093/rheumatology/key042
95. Ehrenstein MR, Wing C. The BAFFling effects of rituximab in lupus: danger ahead? Nat Rev Rheumatol. 2016;12:367-72. doi: 10.1038/nrrheum.2016.18
96. Kraaij T, Huizinga TW, Rabelink TJ, et al. Belimumab after ritux-imab as maintenance therapy in lupus nephritis. Rheumatology. 2014;53:2122-4. doi: 10.1093/rheumatology/keu369
97. Simonetta F, Allali D, Roux-Lombard P, et al. Successful treatment of refractory lupus nephritis by the sequential use of rituximab and belimumab. Joint Bone Spine. 2017;84(2):235-6. doi: 10.1016/j.jbspin.2016.01.008
98. Gonzalez-Echavarri C, Ugarte A, Ruiz-Irastorza G. Rituximab-refractory lupus nephritis successfully treated with belimumab. Clin Exp Rheumatol. 2016;34:355-6.
99. De Vita S, Quartuccio L, Salvin S, Picco L, et al. Sequential therapy with belimumab followed by rituximab in Sjo gren's syndrome associated with B-cell lymphoproliferation and overexpression of BAFF: evidence for long-term efficacy. Clin Exp Rheumatol. 2014;32:490-4.
100. Gualtierotti R, Borghi MO, Gerosa M, et al. Successful sequential therapy with rituximab and belimumab in patients with active systemic lupus erythematosus: a case series. Clin Exp Rheumatol. 2018 Feb 27.
101. Kraaij T, Kamerling SWA, de Rooij ENM, et al. The NET-effect of combining rituximab with belimumab in severe systemic lupus erythematosus. JAutoimmun. 2018;91:45-54. doi: 10.1016/j.jaut.2018.03.003
102. Mesnyankina AA, Solovyev SK, Aleksandrova EN, et al. Dual therapy with biologicals in patients with systemic lupus erythematosus. Nauchno-Prakticheskaya Revmatologiya = Rheumatology Science and Practice. 2016;54(3):281-8 (In Russ.). doi: 10.14412/1995-4484-2016-281-288
103. Mesnyankina AA, Solovyev SK, Aseeva EA, Nasonov EL. The efficiency of biological therapy and the features of humoral immunity in patients with systemic lupus erythematosus. Nauchno-Prakticheskaya Revmatologiya = Rheumatology Science and Practice. 2018;56(3):302-9 (In Russ.). doi: 10.14412/1995-4484-2018-302-309
104. Larosa M, Zen M, Gatto M, et al. IL-12 and IL-23/Th17 axis in systemic lupus erythematosus. Exp Biol Med (Maywood). 2019;244(1):42-51. doi: 10.1177/1535370218824547
105. Ueno H. The IL-12-STAT4 axis in the pathogenesis of human systemic lupus erythematosus. Eur JImmunol. 2020;50(1):10-6. doi: 10.1002/eji.201948134
106. Wang X, Wei Y, Xiao H, et al. A novel IL-23p19/Ebi3 (IL-39) cytokine mediates inflammation in Lupus-like mice. Eur J Immunol. 2016;46(6):1343-50. doi: 10.1002/eji.201546095
107. Dai H, He F, Tsokos GC, Kyttaris VC. IL-23 Limits the production of IL-2 and promotes autoimmunity in lupus. J Immunol. 2017;199(3):903-10. doi: 10.4049/jimmunol.1700418
108. Van Vollenhoven RF, Hahn BH, Tsokos GC, et al. Efficacy and safety of ustekinumab, an IL-12 and IL-23 inhibitor, in patients with active systemic lupus erythematosus: results of a multicentre, double-blind, phase 2, randomised, controlled study. Lancet. 2018;392(10155):1330-9. doi: 10.1016/S0140-6736(18)32167-6
109. Van Vollenhoven RF, Hahn BH, Tsokos GC, et al. Maintenance of efficacy and safety of ustekinumab through 1 year in a randomized phase II trial of patients with active systemic lupus erythematosus. Arthritis Rheum. 2019 Nov 25. doi: 10.1002/art.41179
110. Satoh Y, Nakano K, Yoshinari H, et al. A case of refractory lupus nephritis complicated by psoriasis vulgaris that was controlled with secukinumab. Lupus. 2018;27(7):1202-6. doi: 10.1177/0961203318762598
111. Al Khalili A, Scott L, Dutz JP. New-onset autoantibody-mediated nephritis during ustekinumab therapy for psoriasis in patients with and without prior systemic lupus erythematosus. JAAD Case Rep. 2019;5(8):682-5. doi: 10.1016/j.jdcr.2019.05.022
112. Tierney E, Kirthi S, Ramsay B, Ahmad K. Ustekinumab-induced subacute cutaneous lupus. JAAD Case Rep. 2019;5(3):271-3. doi: 10.1016/j.jdcr.2019.01.015
113. Her M, Kavanaugh A. Alterations in immune function with biologic therapies for autoimmune disease. J Allergy Clin Immunol. 2016;137(1):19-27. doi: 10.1016/j.jaci.2015.10.023
114. Felten R, Scher F, Sagez F, et al. Spotlight on anifrolumab and its potential for the treatment of moderate-to-severe systemic lupus erythematosus: evidence to date. Drug Des Devel Ther. 2019;13:1535-43. doi: 10.2147/DDDT.S170969
115. Furie R, Khamashta M, Merrill JT, et al. Anifrolumab, an anti-interferon-a receptor monoclonal antibody, in moderate-to-severe systemic lupus erythematosus. Arthritis Rheum. 2017;69:376-86. doi: 10.1002/art.39962
116. Merrill JT, Furie R, Werth VP, et al. Anifrolumab effects on rash and arthritis: impact of the type I interferon gene signature in the phase IIb MUSE study in patients with systemic lupus erythematosus. Lupus Sci Med. 2018;5(1):e000284. doi: 10.1136/lupus-2018-000284
117. Casey KA, Guo X, Smith MA, et al. Type I interferon receptor blockade with anifrolumab corrects innate and adaptive immune perturbations of SLE. Lupus Sci Med. 2018;5(1):e000286. doi: 10.1136/lupus-2018-000286
118. Furie RA, Morand EF, Bruce I, et al. on behave of the TULIP-1 study investigator. Type I interferon inhibitor anifrolumab in active systemic lupus erythematosus (TULIP01): a randomized, controlled phase 3 trial. Lancet Rheumatol. 2019;1:e208-19. doi: 10.1016/S2665-9913(19)30076-1
119. Morand E, Furie R, Tanaka Y, et al. Efficacy and safety of ani-frolumab in patients with moderate to severe systemic lupus erythematosus: results of the second phase 3 randomized controlled Trial [abstract]. Arthritis Rheum. 2019;71 Suppl 10.
120. Mok CC. The Jakinibs in systemic lupus erythematosus: progress and prospects. Expert Opin Investig Drugs. 2019;28(1):85-92. doi: 10.1080/13543784.2019.1551358
121. Psarras A, Emery P, Vital EM. Type I interferon-mediated autoimmune diseases: pathogenesis, diagnosis and targeted therapy. Rheumatology (Oxford). 2017;56(10):1662-75. doi: 10.1093/rheumatology/kew431
122. Muskardin TLW, Niewold TB. Type I interferon in rheumatic diseases. Nat Rev Rheumatol. 2018;14(4):214-28. doi: 10.1038/nrrheum.2018.31
123. Sanchez GAM, Reinhardt A, Ramsey S, et al. JAK1/2 inhibition with baricitinib in the treatment of autoinflammatory interfer-onopathies. J Clin Invest. 2018;128(7):3041-52. doi: 10.1172/JCI98814
124. Ko nig N, Fiehn C, Wolf C, et al. Familial chilblain lupus due to a gain-of-function mutation in STING. Ann Rheum Dis. 2017;76(2):468-72. doi: 10.1136/annrheumdis-2016-209841
125. Rodero MP, Fremond M-L, Rice GI, et al. JAK inhibition in STING-associated interferonopathy. Ann Rheum Dis. 2016;75(12):e75-5. doi: 10.1136/annrheumdis-2016-210504
126. You H, Zhang G, Wang Q, et al. Successful treatment of arthritis and rash with tofacitinib in systemic lupus erythematosus: the experience from a single centre. Ann Rheum Dis. 2019 Apr 20. doi: 10.1136/annrheumdis-2019-215455
127. Wallace DJ, Furie RA, Tanaka Y, et al. Baricitinib for systemic lupus erythematosus: a double-blind, randomised, placebo-controlled, phase 2 trial. Lancet. 2018;392(10143):222-31. doi: 10.1016/S0140-6736(18)31363-1
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Solovyev S.K., Aseeva E.A., Popkova T.V., Lila A.M., Mazurov V.I., Nasonov E.L. Systemic lupus erythematosus: new horizons for diagnosis and therapy. Rheumatology Science and Practice. 2020;58(1):5-14. (In Russ.) https://doi.org/10.14412/1995-4484-2020-5-14
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