Pragmatic Treatment of Patients With Systemic Lupus Erythematosus With Rituximab: Long-Term Effects on Serum Immunoglobulins

Arthritis Care and Research

Volumn 69, Issue 6, 2017, Pages 857-866

  Reddy, Venkat ^a   Martinez, Lina ^b   Isenberg, David A ^a   Leandro, Maria J ^a   Cambridge, Geraldine ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b HOSPITAL GENERAL UNIVERSITARIO GREGORIO MARAÑÓN   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AZATHIOPRINE; CD27 ANTIGEN; CORTICOSTEROID; CYCLOPHOSPHAMIDE; DOUBLE STRANDED DNA ANTIBODY; HYDROXYCHLOROQUINE; IMMUNOGLOBULIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN D; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; IMMUNOSUPPRESSIVE AGENT; METHOTREXATE; MYCOPHENOLATE MOFETIL; RITUXIMAB; ANTIRHEUMATIC AGENT; BIOLOGICAL MARKER;

ADOLESCENT; ADULT; AGED; ARTICLE; CLINICAL PRACTICE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; FLOW CYTOMETRY; FOLLOW UP; HUMAN; HUMAN CELL; IMMUNE CELL FUNCTION ASSAY; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOGLOBULIN DEFICIENCY; IMMUNOPHENOTYPING; LONG TERM CARE; LOW DRUG DOSE; MAJOR CLINICAL STUDY; MULTIPLE CYCLE TREATMENT; OBSERVATIONAL STUDY; PREDICTIVE VALUE; RECEIVER OPERATING CHARACTERISTIC; SINGLE DRUG DOSE; SYSTEMIC LUPUS ERYTHEMATOSUS; TREATMENT DURATION; BLOOD; FEMALE; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MIDDLE AGED; TIME FACTOR; TREATMENT OUTCOME; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; ANTIRHEUMATIC AGENTS; BIOMARKERS; CROSS-SECTIONAL STUDIES; FEMALE; FOLLOW-UP STUDIES; HUMANS; IMMUNOGLOBULIN M; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MIDDLE AGED; RITUXIMAB; TIME FACTORS; TREATMENT OUTCOME; YOUNG ADULT;

EID: 85018743852     PISSN: 2151464X     EISSN: 21514658     Source Type: Journal    
DOI: 10.1002/acr.22993     Document Type: Article

References (54)

1. Makatsori M, Kiani-Alikhan S, Manson AL, Verma N, Leandor M. et al. Hypogammaglobulinaemia after rituximab treatment: incidence and outcomes. QJM 2014;107:821–8.
2. Besada E, Koldingsnes W, Nossent JC. Serum immunoglobulin levels and risk factors for hypogammaglobulinaemia during long-term maintenance therapy with rituximab in patients with granulomatosis with polyangiitis. Rheumatology (Oxford) 2014;53:1818–24.
3. Roberts DM, Jones RB, Smith RM, Alberici F, Kumaratne DS, Burns S, et al. Rituximab-associated hypogammaglobulinemia: incidence, predictors and outcomes in patients with multi-system autoimmune disease. J Autoimmun 2015;57:60–5.
4. Marco H, Smith RM, Jones RB, Guerry MJ, Catapano F, Burns S, et al. The effect of rituximab therapy on immunoglobulin levels in patients with multisystem autoimmune disease. BMC Musculoskelet Disord 2014;15:178.
5. Eisenberg RA, Jawad AF, Boyer J, Maurer K, McDonald K, Prak ET, et al. Rituximab-treated patients have a poor response to influenza vaccination. J Clin Immunol 2013;33:388–96.
6. Westra J, van Assen S, Wilting KR, Land J, Horst G, de Haan A, et al. Rituximab impairs immunoglobulin (Ig)M and IgG (subclass) responses after influenza vaccination in rheumatoid arthritis patients. Clin Exp Immunol 2014;178:40–7.
7. Albert D, Dunham J, Khan S, Stansberry J, Kolasinski S, Tsai D, et al. Variability in the biological response to anti-CD20 B cell depletion in systemic lupus erythematosus. Ann Rheum Dis 2008;67:1724–31.
8. Condon MB, Ashby D, Pepper RJ, Cook HT, Levy JB, Griffith M, 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;72:1280–6.
9. Witt M, Grunke M, Proft F, Baeuerle M, Aringer M, Burmester G, et al. Clinical outcomes and safety of rituximab treatment for patients with systemic lupus erythematosus (SLE): results from a nationwide cohort in Germany (GRAID). Lupus 2013;22:1142–9.
10. Leandro MJ, Cambridge G, Edwards JC, Ehrenstein MR, Isenberg DA. B-cell depletion in the treatment of patients with systemic lupus erythematosus: a longitudinal analysis of 24 patients. Rheumatology (Oxford) 2005;44:1542–5.
11. Diaz-Lagares C, Croca S, Sangle S, Vital EM, Catapano F, Martinez-Berriotxoa, et al. Efficacy of rituximab in 164 patients with biopsy-proven lupus nephritis: pooled data from European cohorts. Autoimmun Rev 2012;11:357–64.
12. Baum CG, Chiorazzi N, Frankel S, Shepherd GM Conversion of systemic lupus erythematosus to common variable hypogammaglobulinemia. Am J Med 1989;87:449–56.
13. Fernandez-Castro M, Mellor-Pita S, Citores MJ, Munoz P, Tutor-Ureta P, Silva L, et al. Common variable immunodeficiency in systemic lupus erythematosus. Semin Arthritis Rheum 2007;36:238–45.
14. Takeuchi T, Nakagawa T, Maeda Y, Hirano S, Sasaki-Hayashi M, Makino S, et al. Functional defect of B lymphocytes in a patient with selective IgM deficiency associated with systemic lupus erythematosus. Autoimmunity 2001;34:115–22.
15. Mantovani AP, Monclaro MP, Skare TL. Prevalence of IgA deficiency in adult systemic lupus erythematosus and the study of the association with its clinical and autoantibody profiles. Rev Bras Reumatol 2010;50:273–82.
16. Tsokos GC, Smith PL, Balow JE. Development of hypogammaglobulinemia in a patient with systemic lupus erythematosus. Am J Med 1986;81:1081–4.
17. Mino Y, Naito T, Shimoyama K, Ogawa N, Kawakami J. Pharmacokinetic variability of mycophenolic acid and its glucuronide in systemic lupus erythematosus patients in remission maintenance phase. Biol Pharm Bull 2011;34:755–9.
18. Yap D, Yung S, Ma M, Mok M, Kwan L, Chan G, et al. Serum immunoglobulin G level in patients with lupus nephritis and the effect of treatment with corticosteroids and mycophenolate mofetil. Lupus 2014;23:678–83.
19. Bakri Hassan A, Ronnelid J, Gunnarsson I, Karlsson G, Berg L, Lundberg I. Increased serum levels of immunoglobulins, C-reactive protein, type 1 and type 2 cytokines in patients with mixed connective tissue disease. J Autoimmun 1998;11:503–8.
20. Lipsky PE. Systemic lupus erythematosus: an autoimmune disease of B cell hyperactivity. Nat Immunol 2001;2:764–6.
21. Olsen NJ, Karp DR. Autoantibodies and SLE: the threshold for disease. Nat Rev Rheumatol 2014;10:181–6.
22. Arbuckle MR, McClain MT, Rubertone MV, Scofield RH, Dennis GJ, James JA, et al. Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N Engl J Med 2003;349:1526–33.
23. Isenberg DA, Manson JJ, Ehrenstein MR, Rahman A. Fifty years of anti-ds DNA antibodies: are we approaching journey's end? Rheumatology (Oxford) 2007;46:1052–6.
24. Spronk PE, Horst G, van der Gun BT, Limburg PC, Kallenberg CG. Anti-dsDNA production coincides with concurrent B and T cell activation during development of active disease in systemic lupus erythematosus (SLE). Clin Exp Immunol 1996;104:446–53.
25. Vinuesa CG, Sanz I, Cook MC. Dysregulation of germinal centres in autoimmune disease. Nat Rev Immunol 2009;9:845–57.
26. Odendahl M, Jacobi A, Hansen A, Feist E, Hiepe F, Burmester GR, et al. Disturbed peripheral B lymphocyte homeostasis in systemic lupus erythematosus. J Immunol 2000;165:5970–9.
27. Anolik JH, Friedberg JW, Zheng B, Barnard J, Owen T, Cushing E, et al. B cell reconstitution after rituximab treatment of lymphoma recapitulates B cell ontogeny. Clin Immunol 2007;122:139–45.
28. Leandro MJ, Cambridge G, Ehrenstein MR, Edwards JC. Reconstitution of peripheral blood B cells after depletion with rituximab in patients with rheumatoid arthritis. Arthritis Rheum 2006;54:613–20.
29. Ehrenstein MR, Notley CA. The importance of natural IgM: scavenger, protector and regulator. Nat Rev Immunol 2010;10:778–86.
30. Hochberg MC, for the Diagnostic and Therapeutic Criteria Committee of the American College of Rheumatology. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus [letter]. Arthritis Rheum 1997;40:1725.
31. Ng KP, Cambridge G, Leandro MJ, Edwards JC, Ehrenstein M, Isenberg DA. B cell depletion therapy in systemic lupus erythematosus: long-term follow-up and predictors of response. Ann Rheum Dis 2007;66:1259–62.
32. Turner-Stokes T, Lu TY, Ehrenstein MR, Giles I, Rahman A, Isenberg D. The efficacy of repeated treatment with B-cell depletion therapy in systemic lupus erythematosus: an evaluation. Rheumatology (Oxford) 2011;50:1401–8.
33. Aguiar R, Araujo C, Martins-Coelho G, Isenberg D. Use of rituximab in systemic lupus erythematosus: a single center experience over 14 years. Arthritis Care Res (Hoboken) 2017;69:257–62.
34. De la Torre I, Leandro MJ, Valor L, Becerra E, Edwards JC, Cambridge G. Total serum immunoglobulin levels in patients with RA after multiple B-cell depletion cycles based on rituximab: relationship with B-cell kinetics. Rheumatology (Oxford) 2012;51:833–40.
35. Levy J, Barnett EV, MacDonald NS, Klinenberg JR. Altered immunoglobulin metabolism in systemic lupus erythematosus and heumatoid arthritis. J Clin Invest 1970;49:708–15.
36. Lim SH, Zhang Y, Wang Z, Varadarajan R, Periman P, Esler WV. Rituximab administration following autologous stem cell transplantation for multiple myeloma is associated with severe IgM deficiency. Blood 2004;103:1971–2.
37. Hicks LK, Woods A, Buckstein R, Mangel J, Pennell N, Zhang L, et al. Rituximab purging and maintenance combined with auto-SCT: long-term molecular remissions and prolonged hypogammaglobulinemia in relapsed follicular lymphoma. Bone Marrow Transplant 2009;43:701–8.
38. Weill JC, Weller S, Reynaud CA. Human marginal zone B cells. Ann Rev Immunol 2009;27:267–85.
39. Cambridge G, Perry HC, Nogueira L, Serre G, Parsons HM, de la Torre I, et al. The effect of B-cell depletion therapy on serological evidence of B-cell and plasmablast activation in patients with rheumatoid arthritis over multiple cycles of rituximab treatment. J Autoimmun 2014;50:67–76.
40. Mino Y, Naito T, Shimoyama K, Ogawa N, Kawakami J. Effective plasma concentrations of mycophenolic acid and its glucuronide in systemic lupus erythematosus patients in the remission-maintenance phase. J Clin Pharm Ther 2012;37:217–20.
41. Eickenberg S, Mickholz E, Jung E, Nofer JR, Pavenstadt HJ, Jacobi AM. Mycophenolic acid counteracts B cell proliferation and plasmablast formation in patients with systemic lupus erythematosus. Arthritis Res Ther 2012;14:R110.
42. Isenberg DA. Meryl Streep and the problems of clinical trials. Arthritis Res Ther 2012;14:113.
43. Van Zelm MC, Szczepanski T, van der Burg M, van Dongen JJ. Replication history of B lymphocytes reveals homeostatic proliferation and extensive antigen–induced B cell expansion. J Exp Med 2007;204:645–55.
44. Mahevas M, Patin P, Huetz F, Descatoire M, Cagnard N, Bole-Feysot C, et al. B cell depletion in immune thrombocytopenia reveals splenic long-lived plasma cells. J Clin Invest 2013;123:432–42.
45. Leandro MJ, Edwards JC, Cambridge G, Ehrenstein MR. B-cell repopulation occurs mainly from naive B cells in patients with rheumatoid arthritis and systemic lupus erythematosus treated with rituximab [abstract]. Arthritis Rheum 2003;48:S464.
46. Reddy V, Cambridge G, Isenberg DA, Glennie MJ, Cragg MS, Leandro M. Internalization of rituximab and the efficiency of B cell depletion in rheumatoid arthritis and systemic lupus erythematosus. Arthritis Rheumatol 2015;67:2046–55.
47. Rodriguez-Bayona B, Ramos-Amaya A, Perez-Venegas JJ, Rodriguez C, Brieva JA. Decreased frequency and activated phenotype of blood CD27 IgD IgM B lymphocytes is a permanent abnormality in systemic lupus erythematosus patients. Arthritis Res Ther 2010;12:R108.
48. Lee HJ, Pawlak K, Nguyen BT, Robins RK, Sadee W. Biochemical differences among four inosinate dehydrogenase inhibitors, mycophenolic acid, ribavirin, tiazofurin, and selenazofurin, studied in mouse lymphoma cell culture. Cancer Res 1985;45:5512–20.
49. Natsumeda Y, Carr SF. Human type I and II IMP dehydrogenases as drug targets. Ann N Y Acad Sci 1993;696:88–93.
50. Mysler EF, Spindler AJ, Guzman R, Bijl M, Jayne D, Furie RA, et al. Efficacy and safety of ocrelizumab in active proliferative lupus nephritis: results from a randomized, double-blind, phase III study. Arthritis Rheum 2013;65:2368–79.
51. Ginzler EM, Wax S, Rajeswaran A, Copt S, Hillson J, Ramos E, et al. Atacicept in combination with MMF and corticosteroids in lupus nephritis: results of a prematurely terminated trial. Arthritis Res Ther 2012;14:R33.
52. Mei HE, Frolich D, Giesecke C, Loddenkemper C, Reiter K, Schmidt S, et al. Steady-state generation of mucosal IgA+ plasmablasts is not abrogated by B-cell depletion therapy with rituximab. Blood 2010;116:5181–90.
53. Cambridge G, Isenberg DA, Edwards JC, Leandro MJ, Migone TS, Teodorescu M, et al. B cell depletion therapy in systemic lupus erythematosus: relationships among serum B lymphocyte stimulator levels, autoantibody profile and clinical response. Ann Rheum Dis 2008;67:1011–6.
54. Teng YK, Wheater G, Hogan VE, Stocks P, Levarht EW, Huizinga TW, et al. Induction of long-term B-cell depletion in refractory rheumatoid arthritis patients preferentially affects autoreactive more than protective humoral immunity. Arthritis Res Ther 2012;14:R57.