Efficacy and safety of rituximab treatment in early primary Sjögren's syndrome: A prospective, multi-center, follow-up study

Arthritis Research and Therapy

Volumn 15, Issue 5, 2013, Pages

  Carubbi, Francesco ^a   Cipriani, Paola ^a   Marrelli, Alessandra ^a   Benedetto, Paola D ^a   Ruscitti, Piero ^a   Berardicurti, Onorina ^a   Pantano, Ilenia ^a   Liakouli, Vasiliki ^a   Alvaro, Saverio ^a   Alunno, Alessia ^b   Manzo, Antonio ^c   Ciccia, Francesco ^d   Gerli, Roberto ^b   Triolo, Giovanni ^d   Giacomelli, Roberto ^a  

^a UNIVERSITY OF L'AQUILA   (Italy)

^b UNIVERSITY OF PERUGIA   (Italy)

^c UNIVERSITY OF PAVIA   (Italy)

^d UNIVERSITY OF PALERMO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINUCLEAR ANTIBODY; B CELL ACTIVATING FACTOR; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR5; CHLORPHENIRAMINE; CXCL13 CHEMOKINE; CYCLOSPORIN; HYDROXYCHLOROQUINE; IMMUNOGLOBULIN G; LA ANTIBODY; METHOTREXATE; METHYLPREDNISOLONE; PARACETAMOL; PREDNISONE; RHEUMATOID FACTOR; RITUXIMAB; RO ANTIBODY; ANTIRHEUMATIC AGENT; CXCL12 PROTEIN, HUMAN; CXCR4 PROTEIN, HUMAN; CXCR5 PROTEIN, HUMAN; MONOCLONAL ANTIBODY; STROMAL CELL DERIVED FACTOR 1;

ADULT; ARTICLE; B LYMPHOCYTE; CELL COMPARTMENTALIZATION; CLINICAL ARTICLE; CLINICAL ASSESSMENT; CLINICAL FEATURE; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE DURATION; DRUG EFFICACY; DRUG SAFETY; DRUG TOLERABILITY; FATIGUE; FEMALE; FOLLOW UP; GERMINAL CENTER; HISTOPATHOLOGY; HUMAN; IMMUNOTHERAPY; INFUSION RELATED REACTION; LABORATORY TEST; MALE; MINOR SALIVA GLAND; MULTICENTER STUDY; MULTIPLE CYCLE TREATMENT; OUTCOME ASSESSMENT; PRIMARY SJOGREN SYNDROME; PROSPECTIVE STUDY; PROTEIN EXPRESSION; REPEATED DRUG DOSE; SALIVARY GLAND BIOPSY; SCHIRMER TEST; SELF REPORT; SJOEGREN SYNDROME; SYMPTOM ASSESSMENT; T LYMPHOCYTE; TREATMENT RESPONSE; VISUAL ANALOG SCALE; BIOPSY; CHEMICALLY INDUCED DISORDER; DRUG EFFECT; GENE EXPRESSION; GENETICS; IMMUNOLOGY; METABOLISM; MIDDLE AGED; PAIN ASSESSMENT; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALIVARY GLAND; TIME; TREATMENT OUTCOME;

ADULT; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; ANTIRHEUMATIC AGENTS; BIOPSY; CHEMOKINE CXCL12; CHEMOKINE CXCL13; FATIGUE; FEMALE; FOLLOW-UP STUDIES; GENE EXPRESSION; HUMANS; MALE; MIDDLE AGED; PAIN MEASUREMENT; PROSPECTIVE STUDIES; RECEPTORS, CXCR4; RECEPTORS, CXCR5; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SALIVARY GLANDS; SELF REPORT; SJOGREN'S SYNDROME; TIME FACTORS; TREATMENT OUTCOME;

EID: 84886552636     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar4359     Document Type: Article

References (57)

1. Tzioufas AG, Vlachoyiannopoulos PG. Sjogren's syndrome: an update on clinical, basic and diagnostic therapeutic aspects. J Autoimmun 2012, 39:1-3. 10.1016/j.jaut.2012.01.006, 22361268.
2. Garcia-Carrasco M, Ramos-Casals M, Rosas J. Primary Sjogren syndrome: clinical and immunologic disease patterns in a cohort of 400 patients. Medicine 2002, 81:270. 10.1097/00005792-200207000-00003, 12169882.
3. Fox RI. Sjogren's syndrome. Lancet 2005, 366:321-331. 10.1016/S0140-6736(05)66990-5, 16039337.
4. Meijer JM, Meiners PM, Slater JJRH. Health-related quality of life, employment and disability in patients with Sjogren's syndrome. Rheumatology 2009, 48:1077-1082. 10.1093/rheumatology/kep141, 19553376.
5. Barone F, Bombardieri M, Manzo A, Blades MC, Morgan PR, Challacombe SJ, Valesini G, Pitzalis C. Association of CXCL13 and CCL21 expression with the progressive organization of lymphoid-like structures in Sjogren's syndrome. Arthritis Rheum 2005, 52:1773-1784. 10.1002/art.21062, 15934082.
6. Bombardieri M, Barone F, Humby F, Kelly S, McGurk M, Morgan P, Challacombe S, De Vita S, Valesini G, Spencer J, Pitzalis C. Activation induced cytidine deaminase expression in follicular dendritic cell networks and interfollicular large B cells supports functionality of ectopic lymphoid neogenesis in autoimmune sialoadenitis and MALT lymphoma in Sjogren's syndrome. J Immunol 2007, 179:4929-4938.
7. Anolik JH, Looney RJ, Lund FE. Insights into the heterogeneity of human B cells: diverse functions, roles in autoimmunity, and use as therapeutic targets. Immunol Res 2009, 45:144-158. 10.1007/s12026-009-8096-7, 2891332, 19350211.
8. Tatouli IP, Tzioufas AG. Pathogenetic aspects of humoral autoimmunity in Sjögren's syndrome. Lupus 2012, 21:1151-1154. 10.1177/0961203312458717, 22898537.
9. Voulgarelis M, Dafni UG, Isenberg DA, Moutsopoulos HM. Malignant lymphoma in primary Sjögren's syndrome: a multicenter, retrospective, clinical study by the European Concerted Action on Sjögren's Syndrome. Arthritis Rheum 1999, 42:1765-1772. 10.1002/1529-0131(199908)42:8<1765::AID-ANR28>3.0.CO;2-V, 10446879.
10. Theander E, Henriksson G, Ljungberg O, Mandl T, Manthorpe R, Jacobsson LT. Lymphoma and other malignancies in primary Sjogren's syndrome: a cohort study on cancer incidence and lymphoma predictors. Ann Rheum Dis 2006, 65:796-803. 10.1136/ard.2005.041186, 1798187, 16284097.
11. Moisini I, Davidson A. BAFF: a local and systemic target in autoimmune diseases. Clin Exp Immunol 2009, 158:155-163. 10.1111/j.1365-2249.2009.04007.x, 2768805, 19737141.
12. Thien M, Phan TG, Gardam S. Excess BAFF rescues self-reactive B cells from peripheral deletion and allows them to enter forbidden follicular and marginal zone niches. Immunity 2004, 20:785-798. 10.1016/j.immuni.2004.05.010, 15189742.
13. Groom J, Kalled SL, Cutler AH. Association of BAFF/BLyS overexpression and altered B cell differentiation with Sjogren's syndrome. J Clin Invest 2002, 109:59-68. 150825, 11781351.
14. Lavie F, Miceli-Richard C, Quillard J. Expression of BAFF (BLyS) in T cells infiltrating labial salivary glands from patients with Sjogren's syndrome. J Pathol 2004, 202:496-502. 10.1002/path.1533, 15095277.
15. Pers JO, Daridon C, Devauchelle V. BAFF overexpression is associated with autoantibody production in autoimmune diseases. Ann NY Acad Sci 2005, 1050:34-39. 10.1196/annals.1313.004, 16014518.
16. Mariette X, Roux S, Zhang J. The level of BLyS (BAFF) correlates with the titre of autoantibodies in human Sjogren's syndrome. Ann Rheum Dis 2003, 62:168-171. 10.1136/ard.62.2.168, 1754442, 12525388.
17. Szodoray P, Alex P, Jonsson MV. Distinct profiles of Sjogren's syndrome patients with ectopic salivary gland germinal centers revealed by serum cytokines and BAFF. Clin Immunol 2005, 117:168-176. 10.1016/j.clim.2005.06.016, 16126006.
18. Corsiero E, Bombardieri M, Manzo A, Bugatti S, Uguccioni M, Pitzalis C. Role of lymphoid chemokines in the development of functional ectopic lymphoid structures in rheumatic autoimmune diseases. Immunol Lett 2012, 145:62-67. 10.1016/j.imlet.2012.04.013, 22698185.
19. Aloisi F, Pujol-Borrell R. Lymphoid neogenesis in chronic inflammatory diseases. Nat Rev Immunol 2006, 6:205-217. 10.1038/nri1786, 16498451.
20. van de Pavert SA, Mebius RE. New insights into the development of lymphoid tissues. Nat Rev Immunol 2010, 10:664-674. 10.1038/nri2832, 20706277.
21. Amft N, Curnow SJ, Scheel-Toellner D. Ectopic expression of the B cell-attracting chemokine BCA-1 (CXCL13) on endothelial cells and within lymphoid follicles contributes to the establishment of germinal center-like structures in Sjogren's syndrome. Arthritis Rheum 2001, 44:2633-2641. 10.1002/1529-0131(200111)44:11<2633::AID-ART443>3.0.CO;2-9, 11710719.
22. Xanthou G, Polihronis M, Tzioufas AG, Paikos S, Sideras P, Moutsopoulos HM. 'Lymphoid' chemokine messenger RNA expression by epithelial cells in the chronic inflammatory lesion of the salivary glands of Sjögren's syndrome patients. Possible participation in lymphoid structure formation. Arthritis Rheum 2001, 44:408-418. 10.1002/1529-0131(200102)44:2<408::AID-ANR60>3.0.CO;2-0, 11229473.
23. Salomonsson S, Larsson P, Tengnér P, Mellquist E, Hjelmström P, Wahren-Herlenius M. Expression of the B cell-attracting chemokine CXCL13 in the target organ and autoantibody production in ectopic lymphoid tissue in the chronic inflammatory disease Sjögren's syndrome. Scand J Immunol 2002, 55:336-342. 10.1046/j.1365-3083.2002.01058.x, 11967114.
24. Hansen A, Reiter K, Ziprian T, Jacobi A, Hoffmann A, Gosemann M, Scholze J, Lipsky PE, Dörner T. Dysregulation of chemokine receptor expression and function by B cells of patients with primary Sjögren's syndrome. Arthritis Rheum 2005, 52:2109-2119. 10.1002/art.21129, 15986367.
25. Hansen A, Lipsky PE, Dörner T. B cells in Sjögren's syndrome: indications for disturbed selection and differentiation in ectopic lymphoid tissue. Arthritis Res Ther 2007, 9:218. 10.1186/ar2210, 2206371, 17697366.
26. Ramos-Casals M, Tzioufas AG, Stone JH, Sisó A, Bosch X. Treatment of primary Sjögren syndrome, a systematic review. JAMA 2010, 304:452-460. 10.1001/jama.2010.1014, 20664046.
27. Blüml S, McKeever K. B-cell targeted therapeutics in clinical development. Arthritis Res Ther 2013, 15:S4. 10.1186/ar3906, 3624127, 23566679.
28. Meiners PM, Vissink A, Kallenberg CG. Treatment of primary Sjogren's syndrome with anti-CD20 therapy (rituximab): a feasible approach or just a starting point?. Expert Opin Biol Ther 2011, 11:1381-1394. 10.1517/14712598.2011.605352, 21819314.
29. Kuijpers TW, Bende RJ, Baars PA. CD20 deficiency in humans results in impaired T cell-independent antibody responses. J Clin Invest 2010, 120:214-222. 10.1172/JCI40231, 2798692, 20038800.
30. St Clair EW, Levesque MC, Prak ET, Vivino FB. Rituximab therapy for primary Sjögren's syndrome: an open-label clinical trial and mechanistic analysis. Arthritis Rheum 2013, 65:1097-1106. 10.1002/art.37850, 23334994.
31. Gottenberg JE, Cinquetti G, Larroche C, Combe B, Hachulla E, Meyer O. Efficacy of rituximab in systemic manifestations of primary Sjogren's syndrome: results in 78 patients of the AutoImmune and Rituximab registry. Ann Rheum Dis 2013, 72:1026-1031. 10.1136/annrheumdis-2012-202293, 23264337.
32. Pers JO, Devauchelle V, Daridon C. BAFF-modulated repopulation of B lymphocytes in the blood and salivary glands of rituximab-treated patients with Sjogren's syndrome. Arthritis Rheum 2007, 56:1464-1477. 10.1002/art.22603, 17469105.
33. Pollard RPE, Abdulahad WH, Vissink A, Hamza N. Serum levels of BAFF, but not APRIL, are increased after rituximab treatment in patients with primary Sjögren's syndrome: data from a placebo-controlled clinical trial. Ann Rheum Dis 2013, 72:146-148. 10.1136/annrheumdis-2012-202071, 22851468.
34. Rosengren S, Wei N, Kalunian KC. CXCL13: a novel biomarker of B-cell return following rituximab treatment and synovitis in patients with rheumatoid arthritis. Rheumatology 2011, 50:603-610. 10.1093/rheumatology/keq337, 21098574.
35. Pijpe J, van Imhoff GW, Spijkervet FK, Roodenburg JL, Wolbink GJ, Mansour K. Rituximab treatment in patients with primary Sjogren's syndrome: an open-label phase II study. Arthritis Rheum 2005, 52:2740e50.
36. Devauchelle-Pensec V, Pennec Y, Morvan J, Pers JO, Daridon C, Jousse-Joulin S. Improvement of Sjogren's syndrome after two infusions of rituximab (anti-CD20). Arthritis Rheum 2007, 57:310e7.
37. Jousse-Joulin S, Devauchelle-Pensec V, Morvan J. Ultrasound assessment of salivary glands in patients with primary Sjogren's syndrome treated with rituximab: quantitative and Doppler wave form analysis. Biologics 2007, 1:311-319. 2721315, 19707340.
38. Gottenberg JE, Guillevin L, Lambotte O, Combe B, Allanore Y, Cantagrel A. Tolerance and short term efficacy of rituximab in 43 patients with systemic autoimmune diseases. Ann Rheum Dis 2005, 64:913e20.
39. Galarza C, Valencia D, Tobon GJ, Zurita L, Mantilla RD, Pineda-Tamayo R. Should rituximab be considered as the first-choice treatment for severe autoimmune rheumatic diseases?. Clin Rev Allergy Immunol 2008, 34:124e8.
40. Meijer JM, Meiners PM, Vissink A. Effectiveness of rituximab treatment in primary Sjogren's syndrome: a randomized, double-blind, placebo-controlled trial. Arthritis Rheum 2010, 62:960-968.
41. Vitali C, Bombardieri S, Jonsson R, Moutsopoulos HM, Alexander EL, Carsons SE. Classification criteria for Sjogren's syndrome: a revised version of the European criteria proposed by the American-European Consensus Group. Ann Rheum Dis 2002, 61:554-558. 10.1136/ard.61.6.554, 1754137, 12006334.
42. Seror R, Ravaud P, Bowman SJ. EULAR Sjögren's Syndrome Disease Activity Index (ESSDAI): development of a consensus systemic disease activity index for primary Sjögren's syndrome. Ann Rheum Dis 2010, 69:1103-1109. 10.1136/ard.2009.110619, 2937022, 19561361.
43. Giusti L, Baldini C, Bazzichi L, Ciregia F, Tonazzini I. Proteome analysis of whole saliva: a new tool for rheumatic diseases-the example of Sjögren's syndrome. Proteomics 2007, 7:1634-1643. 10.1002/pmic.200600783, 17436266.
44. Hernández-Molina G, Sánchez-Hernández T. Clinimetric methods in Sjögren's syndrome. Semin Arthritis Rheum 2013, 42:627-639. 10.1016/j.semarthrit.2012.09.008, 23352255.
45. Chisholm DM, Mason DK. Labial salivary gland biopsy in Sjogren's disease. J Clin Pathol 1968, 21:656-660. 10.1136/jcp.21.5.656, 473887, 5697370.
46. Daniels TE, Whitcher JP. Association of patterns of labial salivary gland inflammation with keratoconjunctivitissicca: analysis of 618 patients with suspected Sjogren's syndrome. Arthritis Rheum 1994, 37:869-877. 10.1002/art.1780370615, 8003059.
47. Ciccia F, Giardina A, Rizzo A, Guggino G, Cipriani P, Carubbi F, Giacomelli R, Triolo G. Rituximab modulates the expression of IL-22 in the salivary glands of patients with primary Sjogren's syndrome. Ann Rheum Dis 2013, 72:782-783. 10.1136/annrheumdis-2012-202754, 23264342.
48. Leandra MJ. B-cell subpopulations in humans and their differential susceptibility to depletion with anti-CD20 monoclonal antibodies. Arthritis Res Ther 2013, 15:S3. 3624669, 23566754.
49. Duddy ME, Alter A, Bar-Or A. Distinct profiles of human B-cell effector cytokines: a role in immune regulation?. J Immunol 2004, 172:3422e7.
50. Popa C, Leandro MJ, Cambridge G, Edwards JC. Repeated B lymphocyte depletion with rituximab in rheumatoid arthritis over 7 yrs. Rheumatology (Oxford) 2007, 46:626-630.
51. Abdulahad WH, Meijer JM, Kroese FG. B-cell reconstitution and T-helper-cell balance after rituximab treatment of active primary Sjogren's syndrome. Arthritis Rheum 2011, 63:1116-1123. 10.1002/art.30236, 21225693.
52. Caron G, LeGallou S, Lamy T, Tarte K, Thierry Fest T. CXCR4 expression functionally discriminates centroblasts versus centrocytes within human germinal center B cells. J Immunol 2009, 182:7595-7602. 10.4049/jimmunol.0804272, 19494283.
53. Cupedo T, Mebius RE. Role of chemokines in the development of secondary and tertiary lymphoid tissues. Semin Immunol 2003, 15:243-248. 10.1016/j.smim.2003.08.002, 15001173.
54. Barone F, Bombardieri M, Rosado MM, Morgan PR, Challacombe SJ, De Vita S. CXCL13, CCL21, and CXCL12 expression in salivary glands of patients with Sjogren's syndrome and MALT lymphoma: association with reactive and malignant areas of lymphoid organization. J Immunol 2008, 180:5130-5140.
55. Daridon C, Devauchelle V, Hutin P. Aberrant expression of BAFF by B lymphocytes infiltrating the salivary glands of patients with primary Sjogren's syndrome. Arthritis Rheum 2007, 56:1134-1144. 10.1002/art.22458, 17393395.
56. Ittah M, Miceli-Richard C, Gottenberg EJ. B cell-activating factor of the tumor necrosis factor family (BAFF) is expressed under stimulation by interferon in salivary gland epithelial cellsin primary Sjogren's syndrome. Arthritis Res Ther 2006, 8:R51. 10.1186/ar1912, 1526588, 16507175.
57. Ittah M, Miceli-Richard C, Gottenberg JE. Viruses inducehigh expression of BAFF by salivarygland epithelial cells through TLR- and type-I IFN-dependent and -independent pathways. Eur J Immunol 2008, 38:1058-1064. 10.1002/eji.200738013, 18350548.