Serum levels of CXCL13 are associated with ultrasonographic synovitis and predict power Doppler persistence in early rheumatoid arthritis treated with non-biological disease-modifying anti-rheumatic drugs

Arthritis Research and Therapy

Volumn 14, Issue 1, 2012, Pages

  Bugatti, Serena ^a   Manzo, Antonio ^a   Benaglio, Francesca ^a   Klersy, Catherine ^b   Vitolo, Barbara ^a   Todoerti, Monica ^a   Sakellariou, Garifallia ^a   Montecucco, Carlomaurizio ^a   Caporali, Roberto ^a  

^a UNIVERSITY OF PAVIA   (Italy)

^b FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

Author keywords

Biomarkers; CXCL13; Rheumatoid arthritis; Synovitis; Ultrasonography

Indexed keywords

C REACTIVE PROTEIN; CXCL13 CHEMOKINE; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; METHOTREXATE; RHEUMATOID FACTOR; ANTIRHEUMATIC AGENT; BIOLOGICAL MARKER; CXCL13 PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; CONTROLLED STUDY; DISEASE ACTIVITY; DOPPLER ECHOGRAPHY; DRUG DOSE INCREASE; ENZYME LINKED IMMUNOSORBENT ASSAY; ERYTHROCYTE SEDIMENTATION RATE; FEMALE; FOLLOW UP; GRAY SCALE ECHOGRAPHY; HAND; HUMAN; JOINT SWELLING; MAJOR CLINICAL STUDY; MALE; OUTCOME ASSESSMENT; PREDICTION; PROTEIN BLOOD LEVEL; RHEUMATOID ARTHRITIS; SYNOVITIS; BLOOD; COLOR ULTRASOUND FLOWMETRY; DRUG EFFECT; ECHOGRAPHY; JOINT; MIDDLE AGED; PATHOLOGY; SENSITIVITY AND SPECIFICITY; TIME; TREATMENT OUTCOME;

AGED; ANTIRHEUMATIC AGENTS; ARTHRITIS, RHEUMATOID; BIOLOGICAL MARKERS; CHEMOKINE CXCL13; FEMALE; HUMANS; JOINTS; MALE; MIDDLE AGED; SENSITIVITY AND SPECIFICITY; SYNOVITIS; TIME FACTORS; TREATMENT OUTCOME; ULTRASONOGRAPHY, DOPPLER, COLOR;

EID: 84856979170     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar3742     Document Type: Article

References (41)

1. Knevel R, Schoels M, Huizinga TW, Aletaha D, Burmester GR, Combe B, Landewé RB, Smolen JS, Sokka T, van der Heijde DM. Current evidence for a strategic approach to the management of rheumatoid arthritis with disease-modifying antirheumatic drugs: a systematic literature review informing the EULAR recommendations for the management of rheumatoid arthritis. Ann Rheum Dis 2010, 69:987-994. 10.1136/ard.2009.126748, 20448280.
2. Smolen JS, Aletaha D, Bijlsma JW, Breedveld FC, Boumpas D, Burmester G, Combe B, Cutolo M, de Wit M, Dougados M, Emery P, Gibofsky A, Gomez-Reino JJ, Haraoui B, Kalden J, Keystone EC, Kvien TK, McInnes I, Martin-Mola E, Montecucco C, Schoels M, van der Heijde D, . T2T Expert Committee Treating rheumatoid arthritis to target: recommendations of an international task force. Ann Rheum Dis 2010, 69:631-637. 10.1136/ard.2009.123919, 3015099, 20215140, T2T Expert Committee.
3. Bykerk V. Unmet needs in rheumatoid arthritis. J Rheumatol Suppl 2009, 82:42-46. 10.3899/jrheum.090131, 19509330.
4. Brown AK, Quinn MA, Karim Z, Conaghan PG, Peterfy CG, Hensor E, Wakefield RJ, O'Connor PJ, Emery P. Presence of significant synovitis in rheumatoid arthritis patients with disease-modifying antirheumatic drug-induced clinical remission: evidence from an imaging study may explain structural progression. Arthritis Rheum 2006, 54:3761-3773. 10.1002/art.22190, 17133543.
5. Brown AK, Conaghan PG, Karim Z, Quinn MA, Ikeda K, Peterfy CG, Hensor E, Wakefield RJ, O'Connor PJ, Emery P. An explanation for the apparent dissociation between clinical remission and continued structural deterioration in rheumatoid arthritis. Arthritis Rheum 2008, 58:2958-2967. 10.1002/art.23945, 18821687.
6. Scirè CA, Montecucco C, Codullo V, Epis O, Todoerti M, Caporali R. Ultrasonographic evaluation of joint involvement in early rheumatoid arthritis in clinical remission: power Doppler signal predicts short-term relapse. Rheumatology 2009, 48:1092-1097. 10.1093/rheumatology/kep171, 19561156.
7. de Vries-Bouwstra J, Le Cessie S, Allaart C, Breedveld F, Huizinga T. Using predicted disease outcome to provide differentiated treatment of early rheumatoid arthritis. J Rheumatol 2006, 33:1747-1753.
8. Hider SL, Silman AJ, Thomson W, Lunt M, Bunn D, Symmons DP. Can clinical factors at presentation be used to predict outcome of treatment with methotrexate in patients with early inflammatory polyarthritis?. Ann Rheum Dis 2009, 68:57-62. 2596302, 18292102.
9. de Rooy DP, van der Linden MP, Knevel R, Huizinga TW, van der Helm-van Mil AH. Predicting arthritis outcomes-what can be learned from the Leiden Early Arthritis Clinic?. Rheumatology 2011, 50:93-100. 10.1093/rheumatology/keq230, 20639266.
10. Manzo A, Caporali R, Montecucco C, Pitzalis C. Role of chemokines and chemokine receptors in regulating specific leukocyte trafficking in the immune/inflammatory response. Clin Exp Rheumatol 2003, 21:501-508.
11. Chevalier N, Jarrossay D, Ho E, Avery DT, Ma CS, Yu D, Sallusto F, Tangye SG, Mackay CR. CXCR5 expressing human central memory CD4 T cells and their relevance for humoral immune responses. J Immunol 2011, 186:5556-5568. 10.4049/jimmunol.1002828, 21471443.
12. Sáez de Guinoa J, Barrio L, Mellado M, Carrasco YR. CXCL13/CXCR5 signaling enhances B-cell receptor-triggered B-cell activation by shaping cell dynamics. Blood 2011, 118:1560-1569. 10.1182/blood-2011-01-332106, 21659539.
13. Manzo A, Bombardieri M, Humby F, Pitzalis C. Secondary and ectopic lymphoid tissue responses in rheumatoid arthritis: from inflammation to autoimmunity and tissue damage/remodeling. Immunol Rev 2010, 233:267-285. 10.1111/j.0105-2896.2009.00861.x, 20193005.
14. Zheng B, Ozen Z, Zhang X, De Silva S, Marinova E, Guo L, Wansley D, Huston DP, West MR, Han S. CXCL13 neutralization reduces the severity of collagen-induced arthritis. Arthritis Rheum 2005, 52:620-626. 10.1002/art.20768, 15692971.
15. Rosengren S, Wei N, Kalunian KC, Kavanaugh A, Boyle DL. 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.
16. Manzo A, Vitolo B, Humby F, Caporali R, Jarrossay D, Dell'accio F, Ciardelli L, Uguccioni M, Montecucco C, Pitzalis C. Mature antigen-experienced T helper cells synthesize and secrete the B cell chemoattractant CXCL13 in the inflammatory environment of the rheumatoid joint. Arthritis Rheum 2008, 58:3377-3387. 10.1002/art.23966, 18975336.
17. Rioja I, Hughes FJ, Sharp CH, Warnock LC, Montgomery DS, Akil M, Wilson AG, Binks MH, Dickson MC. Potential novel biomarkers of disease activity in rheumatoid arthritis patients: CXCL13, CCL23, transforming growth factor alpha, tumor necrosis factor receptor superfamily member 9, and macrophage colony-stimulating factor. Arthritis Rheum 2008, 58:2257-2267. 10.1002/art.23667, 18668547.
18. Meeuwisse CM, van der Linden MP, Rullmann TA, Allaart CF, Nelissen R, Huizinga TW, Garritsen A, Toes RE, van Schaik R, van der Helm-van Mil AH. Identification of CXCL13 as a marker for rheumatoid arthritis outcome using an in silico model of the rheumatic joint. Arthritis Rheum 2011, 63:1265-1273. 10.1002/art.30273, 21305530.
19. Todoerti M, Scirè CA, Boffini N, Bugatti S, Montecucco C, Caporali R. Early disease control by low-dose prednisone comedication may affect the quality of remission in patients with early rheumatoid arthritis. Ann N Y Acad Sci 2010, 1193:139-145. 10.1111/j.1749-6632.2009.05367.x, 20398020.
20. van der Heijde DM, van't Hof M, van Riel PL, van de Putte LB. Development of a disease activity score based on judgment in clinical practice by rheumatologists. J Rheumatol 1993, 20:579-581.
21. Aletaha D, Ward MM, Machold KP, Nell VP, Stamm T, Smolen JS. Remission and active disease in rheumatoid arthritis: defining criteria for disease activity states. Arthritis Rheum 2005, 52:2625-2636. 10.1002/art.21235, 16142705.
22. Backhaus M, Burmester GR, Gerber T, Grassi W, Machold KP, Swen WA, Wakefield RJ, Manger B, . Working Group for Musculoskeletal Ultrasound in the EULAR Standing Committee on International Clinical Studies including Therapeutic Trials Guidelines for musculoskeletal ultrasound in rheumatology. Ann Rheum Dis 2001, 60:641-649. 10.1136/ard.60.7.641, 1753749, 11406516, Working Group for Musculoskeletal Ultrasound in the EULAR Standing Committee on International Clinical Studies including Therapeutic Trials.
23. Meenagh G, Filippucci E, Delle Sedie A, Riente L, Iagnocco A, Epis O, Scirè CA, Montecucco C, Bombardieri S, Valesini G, Grassi W. Ultrasound imaging for the rheumatologist. XVIII. Ultrasound measurements. Clin Exp Rheumatol 2008, 26:982-985.
24. Saleem B, Brown AK, Keen H, Nizam S, Freeston J, Wakefield R, Karim Z, Quinn M, Hensor E, Conaghan PG, Emery P. Should imaging be a component of rheumatoid arthritis remission criteria? A comparison between traditional and modified composite remission scores and imaging assessments. Ann Rheum Dis 2011, 70:792-798. 10.1136/ard.2010.134445, 21242236.
25. Naredo E, Bonilla G, Gamero F, Uson J, Carmona L, Laffon A. Assessment of inflammatory activity in rheumatoid arthritis: a comparative study of clinical evaluation with Grey Scale and Power Doppler ultrasonography. Ann Rheum Dis 2005, 64:375-381. 1755396, 15708891.
26. Hameed B, Pilcher J, Heron C, Kiely PD. The relation between composite ultrasound measures and the DAS28 score, its components and acute phase markers in adult RA. Rheumatology 2008, 47:476-480.
27. Takemura S, Braun A, Crowson C, Kurtin PJ, Cofield RH, O'Fallon WM, Goronzy JJ, Weyand CM. Lymphoid neogenesis in rheumatoid synovitis. J Immunol 2001, 167:1072-1080.
28. Shi K, Hayashida K, Kaneko M, Hashimoto J, Tomita T, Lipsky PE, Yoshikawa H, Ochi T. Lymphoid chemokine B cell-attracting chemokine-1 (CXCL13) is expressed in germinal center of ectopic lymphoid follicles within the synovium of chronic arthritis patients. J Immunol 2001, 166:650-655.
29. Manzo A, Caporali R, Vitolo B, Alessi S, Benaglio F, Todoerti M, Bugatti S, Calliada F, Montecucco C. Subclinical remodelling of draining lymph node structure in early and established rheumatoid arthritis assessed by power Doppler ultrasonography. Rheumatology 2011, 50:1395-400. 10.1093/rheumatology/ker076, 21378108.
30. Gabay C, Kushner I. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med 1999, 340:448-454. 10.1056/NEJM199902113400607, 9971870.
31. Naredo E, Collado P, Cruz A, Palop MJ, Cabero F, Richi P, Carmona L, Crespo M. Longitudinal power Doppler ultrasonographic assessment of joint inflammatory activity in early rheumatoid arthritis: predictive value in disease activity and radiologic progression. Arthritis Rheum 2007, 57:116-124. 10.1002/art.22461, 17266071.
32. Emery P, Gabay C, Kraan M, Gomez-Reino J. Evidence-based review of biologic markers as indicators of disease progression and remission in rheumatoid arthritis. Rheumatol Int 2007, 27:793-806. 10.1007/s00296-007-0357-y, 17505829.
33. Klareskog L, Widhe M, Hermansson M, Rönnelid J. Antibodies to citrullinated proteins in arthritis: pathology and promise. Curr Opin Rheumatol 2008, 20:300-305. 10.1097/BOR.0b013e3282fbd22a, 18388522.
34. Taylor PC, Steuer A, Gruber J, Cosgrove DO, Blomley MJ, Marsters PA, Wagner CL, McClinton C, Maini RN. Comparison of ultrasonographic assessment of synovitis and joint vascularity with radiographic evaluation in a randomized, placebo-controlled study of infliximab therapy in early rheumatoid arthritis. Arthritis Rheum 2004, 50:1107-1116. 10.1002/art.20123, 15077292.
35. Naredo E, Möller I, Cruz A, Carmona L, Garrido J. Power Doppler ultrasonographic monitoring of response to anti-tumor necrosis factor therapy in patients with rheumatoid arthritis. Arthritis Rheum 2008, 58:2248-2256. 10.1002/art.23682, 18668537.
36. Aletaha D, Funovits J, Keystone EC, Smolen JS. Disease activity early in the course of treatment predicts response to therapy after one year in rheumatoid arthritis patients. Arthritis Rheum 2007, 56:3226-3235. 10.1002/art.22943, 17907167.
37. Schipper LG, Fransen J, den Broeder AA, Van Riel PL. Time to achieve remission determines time to be in remission. Arthritis Res Ther 2010, 12:R97. 10.1186/ar3027, 2911884, 20487520.
38. Manzo A, Paoletti S, Carulli M, Blades MC, Barone F, Yanni G, Fitzgerald O, Bresnihan B, Caporali R, Montecucco C, Uguccioni M, Pitzalis C. Systematic microanatomical analysis of CXCL13 and CCL21 in situ production and progressive lymphoid organization in rheumatoid synovitis. Eur J Immunol 2005, 35:1347-1359. 10.1002/eji.200425830, 15832291.
39. Manzo A, Pitzalis C. Lymphoid tissue reactions in rheumatoid arthritis. Autoimmun Rev 2007, 7:30-34. 10.1016/j.autrev.2007.03.006, 17967722.
40. Bugatti S, Manzo A, Bombardieri M, Vitolo B, Humby F, Kelly S, Montecucco C, Pitzalis C. Synovial tissue heterogeneity and peripheral blood biomarkers. Curr Rheumatol Rep 2011, 13:440-448. 10.1007/s11926-011-0201-y, 21847543.
41. Maksymowych WP, Fitzgerald O, Wells GA, Gladman DD, Landewé R, Ostergaard M, Taylor WJ, Christensen R, Tak PP, Boers M, Syversen SW, Bathon JM, Ritchlin CJ, Mease PJ, Bykerk VP, Garnero P, Geusens P, El-Gabalawy H, Aletaha D, Inman RD, Kraus VB, Kvien TK, van der Heijde D. Proposal for levels of evidence schema for validation of a soluble biomarker reflecting damage endpoints in rheumatoid arthritis, psoriatic arthritis, and ankylosing spondylitis, and recommendations for study design. J Rheumatol 2009, 36:1792-1799. 10.3899/jrheum090347, 19671814.