B-cell depletion in SLE: Clinical and trial experience with rituximab and ocrelizumab and implications for study design

Arthritis Research and Therapy

Volumn 15, Issue SUPPL.1, 2013, Pages

  Reddy, Venkat ^a   Jayne, David ^b   Close, David ^c   Isenberg, David ^a  

^a Centre for Rheumatology   (United Kingdom)

^b CAMBRIDGE UNIVERSITY HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

^c MEDIMMUNE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AZATHIOPRINE; CORTICOSTEROID; CREATININE; CYCLOPHOSPHAMIDE; METHOTREXATE; METHYLPREDNISOLONE; MYCOPHENOLIC ACID; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; OCRELIZUMAB; PREDNISOLONE; RITUXIMAB; IMMUNOLOGIC FACTOR; MONOCLONAL ANTIBODY;

ANAPHYLAXIS; ARTHRALGIA; CREATININE BLOOD LEVEL; DEEP VEIN THROMBOSIS; DISEASE ACTIVITY; DISEASE EXACERBATION; DRUG EFFICACY; DRUG ERUPTION; DRUG MEGADOSE; DRUG SAFETY; DRUG TOLERABILITY; DYSPEPSIA; DYSPNEA; FEVER; FOLLOW UP; HEART FAILURE; HERPES ZOSTER; HISTOPLASMOSIS; HUMAN; HUMORAL IMMUNE DEFICIENCY; IMMUNOGLOBULIN DEFICIENCY; INSOMNIA; LOW DRUG DOSE; LUNG EMBOLISM; LUNG HEMORRHAGE; LUPUS ERYTHEMATOSUS NEPHRITIS; MALAISE; NECROTIZING FASCIITIS; NEUTROPENIA; PERICARDITIS; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHENOTYPE; PNEUMONIA; PRURITUS; PSEUDOMONAS INFECTION; QUALITY OF LIFE; RANDOMIZED CONTROLLED TRIAL (TOPIC); REMISSION; RESPIRATORY FAILURE; REVIEW; SEPTICEMIA; SINGLE DRUG DOSE; SKIN ABSCESS; STUDY DESIGN; SYSTEMIC LUPUS ERYTHEMATOSUS; TACHYCARDIA; TRANSIENT ISCHEMIC ATTACK; TREATMENT DURATION; TREATMENT RESPONSE; URINARY TRACT INFECTION; URTICARIA; B LYMPHOCYTE; DOSE RESPONSE; DRUG EFFECT; PATHOLOGY; PATHOPHYSIOLOGY; TREATMENT OUTCOME;

ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; B-LYMPHOCYTES; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; IMMUNOLOGIC FACTORS; LUPUS ERYTHEMATOSUS, SYSTEMIC; RANDOMIZED CONTROLLED TRIALS AS TOPIC; TREATMENT OUTCOME;

EID: 84873599778     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar3910     Document Type: Review

References (78)

1. Edwards JC, Cambridge G. B-cell targeting in rheumatoid arthritis and other autoimmune diseases. Nat Rev Immunol 2006, 6:394-403. 10.1038/nri1838, 16622478.
2. Pego-Reigosa JM, Isenberg DA. Systemic lupus erythematosus: pharmacological developments and recommendations for a therapeutic strategy. Expert Opin Investig Drugs 2008, 17:31-41. 10.1517/13543784.17.1.31, 18095917.
3. Gorman C, Leandro M, Isenberg D. B cell depletion in autoimmune disease. Arthritis Res Ther 2003, 5(Suppl 4):S17-S21. 10.1186/ar1007, 2833439, 15180893.
4. Gorman C, Leandro M, Isenberg D. Does B cell depletion have a role to play in the treatment of systemic lupus erythematosus?. Lupus 2004, 13:312-316. 10.1191/0961203304lu1018oa, 15230284.
5. Jayne D. Role of rituximab therapy in glomerulonephritis. J Am Soc Nephrol 2010, 21:14-17. 10.1681/ASN.2008070786, 18799717.
6. Reff ME, Carner K, Chambers KS, Chinn PC, Leonard JE, Raab R, Newman RA, Hanna N, Anderson DR. Depletion of B cells in vivo by a chimeric mouse human monoclonal antibody to CD20. Blood 1994, 83:435-445.
7. McLaughlin P, Grillo-Lopez AJ, Link BK, Levy R, Czuczman MS, Williams ME, Heyman MR, Bence-Bruckler I, White CA, Cabanillas F, Jain V, Ho AD, Lister J, Wey K, Shen D, Dallaire BK. Rituximab chimeric anti-CD20 monoclonal antibody therapy for relapsed indolent lymphoma: half of patients respond to a four-dose treatment program. J Clin Oncol 1998, 16:2825-2833.
8. Cartron G, Trappe RU, Solal-Celigny P, Hallek M. Interindividual variability of response to rituximab: from biological origins to individualized therapies. Clin Cancer Res 2011, 17:19-30. 10.1158/1078-0432.CCR-10-1292, 21208903.
9. Lim S H, Vaughan AT, Ashton-Key M, Williams EL, Dixon SV, Chan HT, Beers SA, French RR, Cox KL, Davies AJ, Potter KN, Mockridge CI, Oscier DG, Johnson PW, Cragg MS, Glennie MJ. Fc gamma receptor IIb on target B cells promotes rituximab internalization and reduces clinical efficacy. Blood 2011, 118:2530-2540. 10.1182/blood-2011-01-330357, 21768293.
10. Edwards JC, Cambridge G. Sustained improvement in rheumatoid arthritis following a protocol designed to deplete B lymphocytes. Rheumatology (Oxford) 2001, 40:205-211.
11. Edwards JC, Szczepanski L, Szechinski J, Filipowicz-Sosnowska A, Emery P, Close DR, Stevens RM, Shaw T. Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N Engl J Med 2004, 350:2572-2581. 10.1056/NEJMoa032534, 15201414.
12. Emery P, Fleischmann R, Filipowicz-Sosnowska A, Schechtman J, Szczepanski L, Kavanaugh A, Racewicz AJ, van Vollenhoven RF, Li NF, Agarwal S, Hessey EW, Shaw TM, . DANCER Study Group The efficacy and safety of rituximab in patients with active rheumatoid arthritis despite methotrexate treatment: results of a phase IIB randomized, double-blind, placebo-controlled, doseranging trial. Arthritis Rheum 2006, 54:1390-1400. 10.1002/art.21778, 16649186, DANCER Study Group.
13. Cohen SB, Emery P, Greenwald MW, Dougados M, Furie RA, Genovese MC, Keystone EC, Loveless JE, Burmester GR, Cravets MW, Hessey EW, Shaw T, Totoritis MC, . REFLEX Trial Group Rituximab for rheumatoid arthritis refractory to anti-tumor necrosis factor therapy: Results of a multicenter, randomized, double-blind, placebo-controlled, phase III trial evaluating primary efficacy and safety at twenty-four weeks. Arthritis Rheum 2006, 54:2793-2806. 10.1002/art.22025, 16947627, REFLEX Trial Group.
14. Leandro MJ, Edwards JC, Cambridge G, Ehrenstein MR, Isenberg DA. An open study of B lymphocyte depletion in systemic lupus erythematosus. Arthritis Rheum 2002, 46:2673-2677. 10.1002/art.10541, 12384926.
15. 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, 44:1542-1545.
16. Ng KP, Leandro MJ, Edwards JC, Ehrenstein MR, Cambridge G, Isenberg DA. Repeated B cell depletion in treatment of refractory systemic lupus erythematosus. Ann Rheum Dis 2006, 65:942-945. 1798232, 16269424.
17. 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, 66:1259-1262. 10.1136/ard.2006.067124, 1955162, 17412738.
18. Smith KG, Jones RB, Burns SM, Jayne DR. Long-term comparison of rituximab treatment for refractory systemic lupus erythematosus and vasculitis: rmission, relapse, and re-treatment. Arthritis Rheum 2006, 54:2970-2982. 10.1002/art.22046, 16947528.
19. Catapano F, Chaudhry AN, Jones RB, Smith KG, Jayne DW. Long-term efficacy and safety of rituximab in refractory and relapsing systemic lupus erythematosus. Nephrol Dial Transplant 2010, 25:3586-3592. 10.1093/ndt/gfq256, 20466686.
20. Turner-Stokes T, Lu TY, Ehrenstein MR, Giles I, Rahman A, Isenberg DA. The efficacy of repeated treatment with B-cell depletion therapy in systemic lupus erythematosus: an evaluation. Rheumatology (Oxford) 2011, 50:1401-1408.
21. Cambridge G, Leandro MJ, Teodorescu M, Manson J, Rahman A, Isenberg DA, Edwards JC. B cell depletion therapy in systemic lupus erythematosus: effect on autoantibody and antimicrobial antibody profiles. Arthritis Rheum 2006, 54:3612-3622. 10.1002/art.22211, 17075806.
22. Tew GW, Rabbee N, Wolslegel K, Hsieh HJ, Monroe JG, Behrens TW, Brunetta PG, Keir ME. Baseline autoantibody profiles predict normalization of complement and anti-dsDNA autoantibody levels following rituximab treatment in systemic lupus erythematosus. Lupus 2010, 19:146-157. 10.1177/0961203309350752, 19946034.
23. Pego-Reigosa JM, Lu TY, Fontanillo MF, del Campo-Perez V, Rahman A, Isenberg DA. Long-term improvement of lipid profile in patients with refractory systemic lupus erythematosus treated with B-cell depletion therapy: a retrospective observational study. Rheumatology (Oxford) 2010, 49:691-696.
24. Ezeonyeji AN, Isenberg DA. Early treatment with rituximab in newly diagnosed systemic lupus erythematosus patients: a steroid-sparing regimen. Rheumatology (Oxford) 2011, 51:476-481.
25. Ramos-Casals M, Diaz-Lagares C, Khamashta MA. Rituximab and lupus: good in real life, bad in controlled trials. Comment on the article by Lu et al. Arthritis Rheum 2009, 61:1281-1282. 10.1002/art.24726, 19714598.
26. Looney RJ, Anolik JH, Campbell D, Felgar RE, Young F, Arend LJ, Sloand JA, Rosenblatt J, Sanz I. B cell depletion as a novel treatment for systemic lupus erythematosus: a phase I/II dose-escalation trial of rituximab. Arthritis Rheum 2004, 50:2580-2589. 10.1002/art.20430, 15334472.
27. Diaz-Lagares C, Croca S, Sangle S, Vital EM, Catapano F, Martinez-Berriotxoa A, Garcia-Hernandez F, Callejas-Rubio JL, Rascon J, D'Cruz D, Jayne D, Ruiz-Irastorza G, Emery P, Isenberg D, Remos-Casals M, Khamashta MA. Efficacy of rituximab in 164 patients with biopsy-proven lupus nephritis: pooled data from European cohorts. Autoimmun Rev 2011, 11:357-364.
28. Tokunaga M, Saito K, Kawabata D, Imura Y, Fujii T, Nakayamada S, Tsujimura S, Nawata M, Iwata S, Azuma T, Mimori T, Tanaka Y. Efficacy of rituximab (anti- CD20) for refractory systemic lupus erythematosus involving the central nervous system. Ann Rheum Dis 2007, 66:470-475. 1856059, 17107983.
29. Zandi M, Catapano F, Burns S, Hall FC, Smith KGC, Jayne DRW, Coles AJ. Rituximab in neuropsychiatric systemic lupus erythematosus: a retrospective study of the Cambridge experience. J Neurol Neurosurg Psychiatry Pract Neurol 2010, 81:e54.
30. Merrill JT, Neuwelt CM, Wallace DJ, Shanahan JC, Latinis KM, Oates JC, Utset TO, Gordon C, Isenberg DA, Hsieh HJ, Zhang D, Brunetta PG. 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, 62:222-233. 10.1002/art.27233, 20039413.
31. Merrill J, Buyon J, Furie R, Latinis K, Gordon C, Hsieh HJ, Brunetta P. Assessment of flares in lupus patients enrolled in a phase II/III study of rituximab (EXPLORER). Lupus 2011, 20:709-716. 10.1177/0961203310395802, 21478286.
32. Alarcon GS, Roseman JM, McGwin G, Uribe A, Bastian HM, Fessler BJ, Baethge BA, Friedman AW, Reveille JD. Systemic lupus erythematosus in three ethnic groups. XX. Damage as a predictor of further damage. Rheumatology (Oxford) 2004, 43:202-205.
33. Ahuja A, Shupe J, Dunn R, Kashgarian M, Kehry MR, Shlomchik MJ. Depletion of B cells in murine lupus: efficacy and resistance. J Immunol 2007, 179:3351-3361.
34. Shlomchik MJ, Madaio MP, Ni D, Trounstein M, Huszar D. The role of B cells in lpr/lpr-induced autoimmunity. J Exp Med 1994, 180:1295-1306. 10.1084/jem.180.4.1295, 2191708, 7931063.
35. Vital EM, Dass S, Buch MH, Henshaw K, Pease CT, Martin MF, Ponchel F, Rawstron AC, Emery P. B cell biomarkers of rituximab responses in systemic lupus erythematosus. Arthritis Rheum 2011, 63:3038-3047. 10.1002/art.30466, 21618204.
36. Rovin BH, Furie R, Latinis K, Looney RJ, Fervenza FC, Sanchez-Guerrero J, Maciuca R, Zhang D, Garg JP, Brunetta P, Appel G, . LUNAR Investigator Group Efficacy and safety of rituximab in patients with active proliferative lupus nephritis: the Lupus Nephritis Assessment with Rituximab study. Arthritis Rheum 2012, 64:1215-1226. 10.1002/art.34359, 22231479, LUNAR Investigator Group.
37. Rigby WFC, Tony HPT, Oelke KR, Combe BG, Laster AJ, Travers H, Von Muhlen C, Fisheleua E, Matin C, Dummer W. Efficacy and safety of ocrelizumab in patients with active rheumatoid arthritis who had an inadequate response to methotrexate: results from the phase III STAGE trial [abstract]. Arthritis Rheum 2010, 62(Suppl 10):383..
38. Tak PP, Mease PJ, Genovese MC, Kremer JM, Haraoui B, Tanaka Y, Bingham C, Ashrafzadeh A, Travers H, Safa-Leathers S, Dummer W. Efficacy and safety of ocrelizumab in patients with active rheumatoid arthritis who have an inadequate response to at least one TNF inhibitor: results from the phase III SCRIPT Trial [abstract]. Arthritis Rheum 2010, 62(Suppl 10):2169.
39. Emery P, Rigby W, Tak PP, Dorner T, Genovese MC, Ferracioli G, Marin-Mola E. Serious infections with ocrelizumab in rheumatoid arthritis: pooled results from double-blind periods of the ocrelizumab phase III RA program. Arthritis Rheum 2010, 62(Suppl 10):414..
40. Mysler EF, Spindler AJ, Guzman R, Bijl M, Jayne D, Furie RA, Maciuca R, Shahdad S, Close D, Brunetta P, Drappa P. Efficacy and safety of ocrelizumab, a humanized antiCD20 antibody, in patients with active proliferative lupus nephritis (LN): results from the randomized, double-blind phase III BELONG study. Arthritis Rheum 2010, 62(Suppl 10):1455.
41. Kappos L, Li D, Calabresi PA, O'Connor P, Bar-Or A, Barkhof F, Yin M, Leppert D, Glanzman R, Tinbergen J, Hauser SL. Ocrelizumab in relapsing-remitting multiple sclerosis: a phase 2, randomised, placebo-controlled, multicentre trial. Lancet 2011, 378:1779-1787. 10.1016/S0140-6736(11)61649-8, 22047971.
42. Navarra SV, Guzman RM, Gallacher AE, Hall S, Levy RA, Jimenez RE, Li EK, Thomas M, Kim HY, Leon MG, Tanasescu C, Nasonov E, Lan JL, Pineda L, Zhong ZJ, Freimuth W, Petri MA, . BLISS-52 Study Group Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomised, placebo-controlled, phase 3 trial. Lancet 2011, 377:721-731. 10.1016/S0140-6736(10)61354-2, 21296403, BLISS-52 Study Group.
43. Furie R, Petri M, Zamani O, Cervera R, Wallace DJ, Tegzova D, Sanchez-Guerrero J, Schwarting A, Merrill JT, Chatham WW, Stohl W, Ginzler EM, Hough DR, Zhong ZJ, Freimuth W, van Vollenhoven RF, . BLISS-76 Study Group A phase III, randomized, placebo-controlled study of belimumab, a monoclonal antibody that inhibits B lymphocyte stimulator, in patients with systemic lupus erythematosus. Arthritis Rheum 2011, 63:3918-3930. 10.1002/art.30613, 22127708, BLISS-76 Study Group.
44. Bertsias GK, Ioannidis JP, Boletis J, Bombardieri S, Cervera R, Dostal C, Font J, Gilboe IM, Houssiau F, Huizinga T, Isenberg D, Kallenberg CG, Khamashta M, Piette JC, Schneider M, Smolen J, Sturfelt G, Tincani A, van Vollenhoven R, Boumpas DT, Gordon C. EULAR points to consider for conducting clinical trials in systemic lupus erythematosus: literature based evidence for the selection of endpoints. Ann Rheum Dis 2009, 68:477-483. 10.1136/ard.2007.083030, 18434449.
45. Reynolds JA, Toescu V, Yee CS, Prabu A, Situnayake D, Gordon C. Effects of rituximab on resistant SLE disease including lung involvement. Lupus 2009, 18:67-73. 10.1177/0961203308094653, 19074171.
46. Alishiri GH, Saburi A, Bayat N, Saadat AR, Saburi E. The initial presentation of systemic lupus erythematosis with aplastic anemia successfully treated with rituximab. Clin Rheumatol 2012, 31:381-384. 10.1007/s10067-011-1878-z, 22015937.
47. Chen H, Zheng W, Su J, Xu D, Wang Q, Leng X, Zhang W, Li M, Tang F, Zhang X, Zeng X, Zhao Y, Zhang F. Low-dose rituximab therapy for refractory thrombocytopenia in patients with systemic lupus erythematosus - a prospective pilot study. Rheumatology (Oxford) 2011, 50:1640-1644.
48. Cambridge G, Isenberg DA, Edwards JC, Leandro MJ, Migone TS, Teodorescu M, Stohl W. B cell depletion therapy in systemic lupus erythematosus: relationships among serum B lymphocyte stimulator levels, autoantibody profile and clinical response. Ann Rheum Dis 2008, 67:1011-1016.
49. Ramos-Casals M, Brito-Zeron P, Munoz S, So to MJ. A systematic review of the off-label use of biological therapies in systemic autoimmune diseases. Medicine 2008, 87:345-364. 10.1097/MD.0b013e318190f170, 19011506.
50. Vital EM, Rawstron AC, Dass S, Henshaw K, Madden J, Emery P, McGonagle D. Reduced-dose rituximab in rheumatoid arthritis: efficacy depends on degree of B cell depletion. Arthritis Rheum 2011, 63:603-608. 10.1002/art.30152, 21360489.
51. Anolik JH, Campbell D, Felgar RE, Young F, Sanz I, Rosenblatt J, Looney RJ. The relationship of FcγRIIIa genotype to degree of B cell depletion by rituximab in the treatment of systemic lupus erythematosus. Arthritis Rheum 2003, 48:455-459. 10.1002/art.10764, 12571855.
52. Emery P, Mease PJ, Rubbert-Roth A, Curtis JR, Muller-Ladner U, Gaylis NB, Williams S, Reynard M, Tyrrell H. Retreatment with rituximab based on a treatment-to-target approach provides better disease control than treatment as needed in patients with rheumatoid arthritis: a retrospective pooled analysis. Rheumatology (Oxford) 2011, 50:2223-2232.
53. Reddy V, Croca S, Gerona D, Ortega IDLT, Isenberg D, Leandro M, Cambridge G. Serum rituximab levels and efficiency of b-cell depletion: differences between patients with systemic lupus erythematosus and rheumatoid arthritis. Ann Rheum Dis 2012, 71(Suppl 3):532.
54. Terrier B, Amoura Z, Ravaud P, Hachulla E, Jouenne R, Combe B, Bonnet C, Cacoub P, Cantagrel A, de Bandt M, Fain O, Fautrel B, Gaudin P, Godeau B, Harlé JR, Hot A, Kahn JE, Lambotte O, Larroche C, Léone J, Meyer O, Pallot-Prades B, Pertuiset E, Quartier P, Schaerverbeke T, Sibilia J, Somogyi A, Soubrier M, Vignon E, Bader-Meunier B, Mariette X, Gottenberg JE, . Club Rhumatismeset Inflammation Safety and efficacy of rituximab in systemic lupus erythematosus: results from 136 patients from the French AutoImmunity and Rituximab registry. Arthritis Rheum 2010, 62:2458-2466. 10.1002/art.27541, 20506527, Club Rhumatismeset Inflammation.
55. 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, 51:833-840.
56. Pepper R, Griffith M, Kirwan C, Levy J, Taube D, Pusey C, Lightstone L, Cairns T. Rituximab is an effective treatment for lupus nephritis and allows a reduction in maintenance steroids. Nephrol Dial Transplant 2009, 24:3717-3723. 10.1093/ndt/gfp336, 19617257.
57. Boumpas DT, Austin HA, Vaughn EM, Klippel JH, Steinberg AD, Yarboro CH, Balow JE. Controlled trial of pulse methylprednisolone versus two regimens of pulse cyclophosphamide in severe lupus nephritis. Lancet 1992, 340:741-745. 10.1016/0140-6736(92)92292-N, 1356175.
58. Levey AS, Lan SP, Corwin HL, Kasinath BS, Lachin J, Neilson EG, Hunsicker LG, Lewis EJ. Progression and remission of renal disease in the Lupus Nephritis Collaborative Study. Results of treatment with prednisone and short-term oral cyclophosphamide. Ann Internal Med 1992, 116:114-123.
59. Fraenkel L, MacKenzie T, Joseph L, Kashgarian M, Hayslett JP, Esdaile JM. Response to treatment as a predictor of longterm outcome in patients with lupus nephritis. J Rheumatol 1994, 21:2052-2057.
60. Houssiau FA, Vasconcelos C, D'Cruz D, Sebastiani GD, de Ramon Garrido E, Danieli MG, Abramovicz D, Blockmans D, Mathieu A, Direskeneli H, Galeazzi M, Gül A, Levy Y, Petera P, Popovic R, Petrovic R, Sinico RA, Cattaneo R, Font J, Depresseux G, Cosyns JP, Cervera R. Early response to immunosuppressive therapy predicts good renal outcome in lupus nephritis: lessons from long-term followup of patients in the Euro-Lupus Nephritis Trial. Arthritis Rheum 2004, 50:3934-3940. 10.1002/art.20666, 15593207.
61. Luijten KM, Tekstra J, Bijlsma JW, Bijl M. The Systemic Lupus Erythematosus Responder Index (SRI); a new SLE disease activity assessment. Autoimmunity Rev 2012, 11:326-329.
62. Touma Z, Gladman DD, Ibanez D, Taghavi-Zadeh S, Urowitz MB. Systemic Lupus Erythematosus Disease Activity Index 2000 Responder Index-50 enhances the ability of SLE Responder Index to identify responders in clinical trials. J Rheumatol 2011, 38:2395-2399. 10.3899/jrheum.110550, 21885488.
63. Woodworth T, Furst DE, Alten R, Bingham C, Yocum D, Sloan V, Tsuji W, Stevens R, Fries J, Witter J, Johnson K, Lassere M, Brooks P. Standardizing assessment and reporting of adverse effects in rheumatology clinical trial II: the Rheumatology Common Toxicity Criteria v.2.0. J Rheumatol 2007, 34:1401-1414.
64. Anolik JH, Barnard J, Cappione A, Pugh-Bernard AE, Felgar RE, Looney RJ, Sanz I. Rituximab improves peripheral B cell abnormalities in human systemic lupus erythematosus. Arthritis Rheum 2004, 50:3580-3590. 10.1002/art.20592, 15529346.
65. Vigna-Perez M, Hernandez-Castro B, Paredes-Saharopulos O, Portales-Perez D, Baranda L, Abud-Mendoza C, Gonzalez-Amaro R. Clinical and immunological effects of Rituximab in patients with lupus nephritis refractory to conventional therapy: a pilot study. Arthritis Res Ther 2006, 8:R83. 10.1186/ar1954, 1526618, 16677395.
66. Tamimoto Y, Horiuchi T, Tsukamoto H, Otsuka J, Mitoma H, Kimoto Y, Nakashima H, Muta K, Abe Y, Kiyohara C, Ueda A, Nagasawa K, Yoshizawa S, Shimoda T, Harada M. A dose-escalation study of rituximab for treatment of systemic lupus erythematosus and Evans' syndrome: immunological analysis of B cells, T cells and cytokines. Rheumatology (Oxford) 2008, 47:821-827.
67. Tanaka Y, Yamamoto K, Takeuchi T, Nishimoto N, Miyasaka N, Sumida T, Shima Y, Takada K, Matsumoto I, Saito K, Koike T. A multicenter phase I/II trial of rituximab for refractory systemic lupus erythematosus. Mod Rheumatol 2007, 17:191-197. 10.1007/s10165-007-0565-z, 17564773.
68. Li EK, Tam LS, Zhu TY, Li M, Kwok CL, Li TK, Leung YY, Wong KC, Szeto CC. Is combination rituximab with cyclophosphamide better than rituximab alone in the treatment of lupus nephritis?. Rheumatology (Oxford) 2009, 48:892-898.
69. Lu TY, Ng KP, Cambridge G, Leandro MJ, Edwards JC, Ehrenstein M, Isenberg DA. A retrospective seven-year analysis of the use of B cell depletion therapy in systemic lupus erythematosus at University College London Hospital: the first fifty patients. Arthritis Rheum 2009, 61:482-487. 10.1002/art.24341, 19333973.
70. Sfikakis PP, Boletis JN, Lionaki S, Vigklis V, Fragiadaki KG, Iniotaki A, Moutsopoulos HM. Remission of proliferative lupus nephritis following B cell depletion therapy is preceded by down-regulation of the T cell costimulatory molecule CD40 ligand: an open-label trial. Arthritis Rheum 2005, 52:501-513. 10.1002/art.20858, 15693003.
71. Gottenberg JE, Guillevin L, Lambotte O, Combe B, Allanore Y, Cantagrel A, Larroche C, Soubrier M, Bouillet L, Dougados M, Fain O, Farge D, Kyndt X, Lortholary O, Masson C, Moura B, Remy P, Thomas T, Wendling D, Anaya JM, Sibilia J, Mariette X, . Club Rheumatismes et Inflammation Tolerance and short term efficacy of rituximab in 43 patients with systemic autoimmune diseases. Ann Rheum Dis 2005, 64:913-920. 10.1136/ard.2004.029694, 1755517, 15550531, Club Rheumatismes et Inflammation.
72. Gunnarsson I, Sundelin B, Jonsdottir T, Jacobson SH, Henriksson EW, van Vollenhoven RF. Histopathologic and clinical outcome of rituximab treatment in patients with cyclophosphamide-resistant proliferative lupus nephritis. Arthritis Rheum 2007, 56:1263-1272. 10.1002/art.22505, 17393458.
73. Galarza C, Valencia D, Tobon GJ, Zurita L, Mantilla RD, Pineda-Tamayo R, Rojas-Villarraga A, Rueda JC, Anaya JM. Should rituximab be considered as the first-choice treatment for severe autoimmune rheumatic diseases?. Clin Rev Allergy Immunol 2008, 34:124-128. 10.1007/s12016-007-8028-z, 18270866.
74. Jonsdottir T, Gunnarsson I, Risselada A, Henriksson EW, Klareskog L, van Vollenhoven RF. Treatment of refractory SLE with rituximab plus cyclophosphamide: clinical effects, serological changes, and predictors of response. Ann Rheum Dis 2008, 67:330-334.
75. Lindholm C, Borjesson-Asp K, Zendjanchi K, Sundqvist AC, Tarkowski A, Bokarewa M. Longterm clinical and immunological effects of anti-CD20 treatment in patients with refractory systemic lupus erythematosus. J Rheumatol 2008, 35:826-833.
76. Sutter JA, Kwan-Morley J, Dunham J, Du YZ, Kamoun M, Albert D, Eisenberg RA, Luning Prak ET. A longitudinal analysis of SLE patients treated with rituximab (anti-CD20): factors associated with B lymphocyte recovery. Clin Immunol 2008, 126:282-290. 10.1016/j.clim.2007.11.012, 18226586.
77. Boletis JN, Marinaki S, Skalioti C, Lionaki SS, Iniotaki A, Sfikakis PP. Rituximab and mycophenolate mofetil for relapsing proliferative lupus nephritis: a long-term prospective study. Nephrol Dial Transplant 2009, 24:2157-2160. 10.1093/ndt/gfp002, 19179411.
78. Melander C, Sallee M, Trolliet P, Candon S, Belenfant X, Daugas E, Remy P, Zarrouk V, Pillebout E, Jacquot C, Boffa JJ, Karras A, Masse V, Lesavre P, Elie C, Brocheriou I, Knebelmann B, Nöel LH, Fakhouri F. Rituximab in severe lupus nephritis: early B-cell depletion affects long-term renal outcome. Clin J Am Soc Nephrol 2009, 4:579-587. 10.2215/CJN.04030808, 2653670, 19261822.