98
Views
3
CrossRef citations to date
0
Altmetric
Review

Rheumatoid Arthritis Relapse and Remission – Advancing Our Predictive Capability Using Modern Imaging

&
Pages 2547-2555 | Published online: 16 Jun 2021

References

  • Smolen JS, Aletaha D, Bijlsma JW, et al. Treating rheumatoid arthritis to target: recommendations of an international task force. Ann Rheum Dis. 2010;69(4):631–637. doi:10.1136/ard.2009.123919
  • Schipper LG, Vermeer M, Kuper HH, et al. A tight control treatment strategy aiming for remission in early rheumatoid arthritis is more effective than usual care treatment in daily clinical practice: a study of two cohorts in the Dutch Rheumatoid Arthritis Monitoring registry. Ann Rheum Dis. 2012;71:845–850. doi:10.1136/annrheumdis-2011-200274
  • Gullick NJ, Oakley SP, Zain A, et al. Goal-directed therapy for RA in routine practice is associated with improved function in patients with disease duration up to 15 years. Rheumatology (Oxford). 2012;51:759–761. doi:10.1093/rheumatology/ker399
  • Smolen JS, Breedveld FC, Burmester GR, et al. Treating rheumatoid arthritis to target: 2014 update of the recommendations of an international task force. Ann Rheum Dis. 2016;75:3–15. doi:10.1136/annrheumdis-2015-207524
  • Smolen JS, Landewé RBM, Bijlsma JWJ, et al. EULAR recommendations for the management of RA with synthetic and biological disease-modifying antirheumatic drugs: 2019 update. Ann Rheum Dis. 2020;79:685–699. doi:10.1136/annrheumdis-2019-216655
  • Hammer HB, Uhlig T, Kvien TK, Lampa J. Pain catastrophizing, subjective outcomes, and inflammatory assessments including ultrasound: results from a longitudinal study of rheumatoid arthritis patients. Arthritis Care Res (Hoboken). 2018;70(5):703–712. doi:10.1002/acr.23339
  • Nguyen H, Ruyssen-Witrand A, Gandjbakhch F, Constantin A, Foltz V, Cantagrel A. Prevalence of ultrasound-detected residual synovitis and risk of relapse and structural progression in rheumatoid arthritis patients in clinical remission: a systematic review and meta-analysis. Rheumatology (Oxford). 2014;53(11):2110–2118. doi:10.1093/rheumatology/keu217
  • Lillegraven S, Prince FH, Shadick NA, et al. Remission and radiographic outcome in rheumatoid arthritis: application of the 2011 ACR/EULAR remission criteria in an observational cohort. Ann Rheum Dis. 2012;71(5):681–686. doi:10.1136/ard.2011.154625
  • Paulshus Sundlisæter N, Olsen IC, Aga A-B, et al. Predictors of sustained remission in patients with early rheumatoid arthritis treated according to an aggressive treat-to-target protocol. Rheumatology. 2018;57:2022–2031. doi:10.1093/rheumatology/key202
  • Felson DT, Smolen JS, Wells G, et al. American College of Rheumatology/European League against rheumatism provisional definition of remission in rheumatoid arthritis for clinical trials. Ann Rheum Dis. 2011;70:404–413. doi:10.1136/ard.2011.149765
  • Sewerin P, Vordenbaeumen S, Hoyer A, et al. Silent progression in patients with rheumatoid arthritis: is DAS28 remission an insufficient goal in RA? Results from the German Remission-plus cohort. BMC Musculoskelet Disord. 2017;18(1):163. doi:10.1186/s12891-017-1528-y
  • Olmez MO, Gunal EK, Ureyen SB, et al. Comparison of composite indices with global synovitis score on ultrasound for detecting remission. Clin Rheumatol. 2018;37:1111–1114. doi:10.1007/s10067-017-3925-x
  • Brown AK, Quinn MA, Karim Z, et al. 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(12):3761–3773. doi:10.1002/art.22190
  • Brown AK, Conaghan PG, Karim Z, et al. An explanation for the apparent dissociation between clinical remission and continued structural deterioration in rheumatoid arthritis. Arthritis Rheum. 2008;58(10):2958–2967. doi:10.1002/art.23945
  • Wakefield RJ, Freeston JE, Hensor EM, Bryer D, Quinn MA, Emery P. Delay in imaging versus clinical response: a rationale for prolonged treatment with anti-tumor necrosis factor medication in early rheumatoid arthritis. Arthritis Rheum. 2007;57(8):1564–1567. doi:10.1002/art.23097
  • Zhang H, Xu H, Chen S, Mao X. The application value of MRI in the diagnosis of subclinical inflammation in patients with rheumatoid arthritis in remission. J Orthop Surg Res. 2018;13(1):164. doi:10.1186/s13018-018-0866-2
  • Gandjbakhch F, Haavardsholm EA, Conaghan PG, et al. Determining a magnetic resonance imaging inflammatory activity acceptable state without subsequent radiographic progression in rheumatoid arthritis: results from a follow-up MRI study of 254 patients in clinical remission or low disease activity. J Rheumatol. 2014;41(2):398–406. doi:10.3899/jrheum.131088
  • Zufferey P, Möller B, Brulhart L, et al. Persistence of ultrasound synovitis in patients with rheumatoid arthritis fulfilling the DAS28 and/or the new ACR/EULAR RA remission definitions: results of an observational cohort study. Joint Bone Spine. 2014;81(5):426–432. doi:10.1016/j.jbspin.2014.04.014
  • Terslev L, Brahe CH, Østergaard M, et al. Using a DAS28-CRP-steered treat-to-target strategy does not eliminate subclinical inflammation as assessed by ultrasonography in rheumatoid arthritis patients in longstanding clinical remission. Arthritis Res Ther. 2021;23(1):48. doi:10.1186/s13075-021-02426-w
  • Bellis E, Scirè CA, Carrara G, et al. Ultrasound-detected tenosynovitis independently associates with patient-reported flare in patients with rheumatoid arthritis in clinical remission: results from the observational study STARTER of the Italian Society for Rheumatology. Rheumatology (Oxford). 2016;55:1826–1836. doi:10.1093/rheumatology/kew258
  • Filippou G, Sakellariou G, Scirè CA, et al. The predictive role of ultrasound-detected tenosynovitis and joint synovitis for flare in patients with rheumatoid arthritis in stable remission. Results of an Italian multicentre study of the Italian Society for Rheumatology Group for Ultrasound: the STARTER study. Ann Rheum Dis. 2018;77(9):1283–1289. doi:10.1136/annrheumdis-2018-213217
  • Wakefield RJ, Green MJ, Marzo-Ortega H, et al. Should oligoarthritis be reclassified? Ultrasound reveals a high prevalence of subclinical disease. Ann Rheum Dis. 2004;63(4):382–385. doi:10.1136/ard.2003.007062
  • Terslev L, Brahe CH, Hetland ML, et al. Doppler ultrasound predicts successful discontinuation of biological DMARDs in rheumatoid arthritis patients in clinical remission. Rheumatology (Oxford). 2021;keab276. doi:10.1093/rheumatology/keab276
  • Hammer HB, Kvien TK, Terslev L. Ultrasound of the hand is sufficient to detect subclinical inflammation in rheumatoid arthritis remission: a post hoc longitudinal study. Arthritis Res Ther. 2017;19(1):221. doi:10.1186/s13075-017-1428-4
  • Gandjbakhch F, Conaghan PG, Ejbjerg B, et al. Synovitis and osteitis are very frequent in rheumatoid arthritis clinical remission: results from an MRI study of 294 patients in clinical remission or low disease activity state. J Rheumatol. 2011;38(9):2039–2044. doi:10.3899/jrheum.110421
  • Szkudlarek M, Court-Payen M, Jacobsen S, Klarlund M, Thomsen HS, Østergaard M. Interobserver agreement in ultrasonography of the finger and toe joints in rheumatoid arthritis. Arthritis Rheum. 2003;48(4):955–962. doi:10.1002/art.10877
  • Aletaha D, Neogi T, Silman AJ, et al. 2010 Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum. 2010;62(9):2569–2581. doi:10.1002/art.27584
  • Sundin U, Sundlisater NP, Aga AB, et al. Value of MRI and ultrasound for prediction of therapeutic response and erosive progression in patients with early rheumatoid arthritis managed by an aggressive treat-to-target strategy. RMD Open. 2021;7(1):e001525. doi:10.1136/rmdopen-2020-001525
  • Saleem B, Brown AK, Keen H, et al. Disease remission state in patients treated with the combination of tumor necrosis factor blockade and methotrexate or with disease-modifying antirheumatic drugs: a clinical and imaging comparative study. Arthritis Rheum. 2009;60(7):1915–1922. doi:10.1002/art.24596
  • Spinella A, Sandri G, Carpenito G, Belletti L, Mascia MT. The discrepancy between clinical and ultrasonographic remission in rheumatoid arthritis is not related to therapy or autoantibody status. Rheumatol Int. 2012;32(12):3917–3921. doi:10.1007/s00296-011-2259-2
  • Geng Y, Han J, Deng X, Zhang Z. Presence of power Doppler synovitis in rheumatoid arthritis patients with synthetic and/or biological disease-modifying anti-rheumatic drug-induced clinical remission: experience from a Chinese cohort. Clin Rheumatol. 2014;33(8):1061–1066. doi:10.1007/s10067-014-2634-y
  • Cruces M, Al Snih S, Serra-Bonett N, Rivas JC. Subclinical synovitis measured by ultrasound in rheumatoid arthritis patients with clinical remission induced by synthetic and biological modifying disease drugs. Reumatol Clin. 2019;15(4):218–222. doi:10.1016/j.reuma.2017.08.004
  • Padovano I, Costantino F, Breban M, D’Agostino MA. Prevalence of ultrasound synovial inflammatory findings in healthy subjects. Ann Rheum Dis. 2016;75:1819–1823. doi:10.1136/annrheumdis-2015-208103
  • Witt M, Mueller F, Nigg A, et al. Relevance of grade 1 gray-scale ultrasound findings in wrists and small joints to the assessment of subclinical synovitis in rheumatoid arthritis. Arthritis Rheum. 2013;65:1694–1701. doi:10.1002/art.37954
  • Terslev L, Østergaard M, Sexton J, Hammer HB. Is synovial hypertrophy without Doppler activity sensitive to change? Post-hoc analysis from a rheumatoid arthritis ultrasound study. Arthritis Res Ther. 2018;20(1):224. doi:10.1186/s13075-018-1709-6
  • Torp-Pedersen S, Christensen R, Szkudlarek M, et al. Power and color Doppler ultrasound settings for inflammatory flow: impact on scoring of disease activity in patients with rheumatoid arthritis. Arthritis Rheumatol. 2015;67(2):386–395. doi:10.1002/art.38940
  • Østergaard M, Peterfy C, Conaghan P, et al. OMERACT rheumatoid arthritis magnetic resonance imaging studies. Core set of MRI acquisitions, joint pathology definitions, and the OMERACT RA-MRI scoring system. J Rheum. 2003;30:1385–1386.
  • Østergaard M, Peterfy CG, Bird P, et al. The OMERACT rheumatoid arthritis Magnetic Resonance Imaging (MRI) scoring system: updated recommendations by the OMERACT MRI in arthritis working group. J Rheumatol. 2017;44(11):1706–1712. doi:10.3899/jrheum.161433
  • Ejbjerg E, Narvestad E, Rostrup E, et al. Magnetic resonance imaging of wrist and finger joints in healthy subjects occasionally shows changes resembling erosions and synovitis as seen in rheumatoid arthritis. Arthritis Rheumatism. 2004;50:1097–1106. doi:10.1002/art.20135
  • Mangnus L, van Steenbergen HW, Reijnierse M, van der Helm-van Mil AHM. Magnetic resonance imaging–detected features of inflammation and erosions in symptom-free persons from the general population. Arthritis Rheumatol. 2016;68(11):2593–2602. doi:10.1002/art.39749
  • Østergaard M, Haavardsholm E. MRI in healthy volunteers — important to do, and do correctly. Nat Rev Rheum. 2016;12(10):563–564. doi:10.1038/nrrheum.2016.142
  • Paulshus Sundlisæter N, Aga AB, Olsen IC, et al. Clinical and ultrasound remission after 6 months of treat-to-target therapy in early rheumatoid arthritis: associations to future good radiographic and physical outcomes. Ann Rheum Dis. 2018;77(10):1421–1425. doi:10.1136/annrheumdis-2017-212830
  • 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 (Oxford). 2009;48(9):1092–1097. doi:10.1093/rheumatology/kep171
  • Saleem B, Brown AK, Quinn M, et al. Can flare be predicted in DMARD treated RA patients in remission, and is it important? A cohort study. Ann Rheum Dis. 2012;71(8):1316–1321. doi:10.1136/annrheumdis-2011-200548
  • Foltz V, Gandjbakhch F, Etchepare F, et al. Power Doppler ultrasound, but not low-field magnetic resonance imaging, predicts relapse and radiographic disease progression in rheumatoid arthritis patients with low levels of disease activity. Arthritis Rheum. 2012;64(1):67–76. doi:10.1002/art.33312
  • Naredo E, Valor L, De la Torre I, et al. Predictive value of doppler ultrasound-detected synovitis in relation to failed tapering of biologic therapy in patients with rheumatoid. Arthritis Rheumatol (Oxford). 2015;54(8):1408–1414. doi:10.1093/rheumatology/kev006
  • Alivernini S, Peluso G, Fedele AL, Tolusso B, Gremese E, Ferraccioli G. Tapering and discontinuation of TNF-α blockers without disease relapse using ultrasonography as a tool to identify patients with rheumatoid arthritis in clinical and histological remission. Arthritis Res Ther. 2016;18:3. doi:10.1186/s13075-016-0927-z
  • Møller-Bisgaard S, Georgiadis S, Hørslev-Petersen K, et al. Predictors of joint damage progression and stringent remission in patients with established rheumatoid arthritis in clinical remission. Rheumatology (Oxford). 2021;60(1):380–391. doi:10.1093/rheumatology/keaa496
  • Haavardsholm EA, Aga A-B, Olsen IC, et al. Ultrasound in management of rheumatoid arthritis: arctic randomised controlled strategy trial. BMJ. 2016;354:i4205. doi:10.1136/bmj.i4205
  • Møller-Bisgaard S, Hørslev-Petersen K, Ejbjerg B, et al. Effect of magnetic resonance imaging vs conventional treat-to-target strategies on disease activity remission and radiographic progression in rheumatoid arthritis: the IMAGINE-RA randomized clinical trial. JAMA. 2019;321(5):461–472. doi:10.1001/jama.2018.21362
  • Baker JF, Østergaard M, Emery P, Baker DG, Conaghan P. Development and validation of rheumatoid arthritis magnetic resonance imaging inflammation thresholds associated with lack of damage progression. Clin Exp Rheumatol. 2017;35(4):607–613.
  • Ahmad HA, Baker JF, Østergaard M, Ye J, Emery P, Conaghan PG. Determining MRI inflammation targets when considering a rheumatoid arthritis treat-to-target strategy: results of a randomized, placebo-controlled trial. Adv Ther. 2019;36:2384–2393. doi:10.1007/s12325-019-01020-6
  • Brahe CH, Krabbe S, Østergaard M, et al. Dose tapering and discontinuation of biological therapy in rheumatoid arthritis patients in routine care - 2-year outcomes and predictors. Rheumatology (Oxford). 2019;58(1):110–119. doi:10.1093/rheumatology/key244
  • Østergaard M, Møller-Bisgaard S. Optimal use of MRI in clinical trials, clinical care and clinical registries of patients with rheumatoid arthritis. Clin Exp Rheumatol. 2014;32(Suppl 85):S17–S22.
  • Okano T, Inui K, Tada M, et al. Additional intensive treatment for rheumatoid arthritis patients with positive power doppler signals reduce the radiological joint damage even after achieving clinical remission -SCRUM study- [abstract]. Arthritis Rheumatol. 2015;67(suppl 10).
  • Møller-Bisgaard S, Østergaard M. Treat-to-target strategies in rheumatoid arthritis. Reply to comment by van der Helm-van Mil et al. JAMA. 2019;322:83–84. doi:10.1001/jama.2019.5856
  • Kavanaugh A, Fleischmann RM, Emery P, et al. Clinical, functional and radiographic consequences of achieving stable low disease activity and remission with adalimumab plus methotrexate or methotrexate alone in early rheumatoid arthritis: 26-week results from the randomised, controlled OPTIMA study. Ann Rheum Dis. 2013;72:64–71. doi:10.1136/annrheumdis-2011-201247
  • Linde L, Sørensen J, Østergaard M, Hørslev-Petersen K, Hetland ML. Does clinical remission lead to normalization of EQ-5D in patients with rheumatoid arthritis and is selection of remission criteria important? J Rheumatol. 2010;37:285–290. doi:10.3899/jrheum.090898
  • Radner H, Alasti F, Smolen JS, Aletaha D. Physical function continues to improve when clinical remission is sustained in rheumatoid arthritis patients. Arthritis Res Ther. 2015;17:203. doi:10.1186/s13075-015-0719-x
  • Molenaar ET, Voskuyl AE, Dinant HJ, Bezemer PD, Boers M, Dijkmans BA. Progression of radiologic damage in patients with rheumatoid arthritis in clinical remission. Arthritis Rheum. 2004;50:36–42. doi:10.1002/art.11481
  • Markusse IM, Dirven L, Gerards AH, et al. Disease flares in rheumatoid arthritis are associated with joint damage progression and disability: 10-year results from the BeSt study. Arthritis Res Ther. 2015;17:232.
  • Bartlett SJ, Hewlett S, Bingham CO, et al. Identifying core domains to assess flare in rheumatoid arthritis: an OMERACT international patient and provider combined Delphi consensus. Ann Rheum Dis. 2012;71:1855–1860. doi:10.1136/annrheumdis-2011-201201
  • Lie E, Woodworth TG, Christensen R, et al. Validation of OMERACT preliminary rheumatoid arthritis flare domains in the NOR-DMARD study. Ann Rheum Dis. 2014;73:1781–1787. doi:10.1136/annrheumdis-2013-203496
  • Smolen JS, Pedersen R, Jones H, Mahgoub E, Marshall L. Impact of flare on radiographic progression after eternacpet continuation, tapering or withdrawal in patients with rheumatoid arthritis. Rheumatology(Oxford). 2020;59:153–164. doi:10.1093/rheumatology/kez224
  • 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(9):2625–2636. doi:10.1002/art.21235
  • Kuettel D, Terslev L, Weber U, et al. Flares in rheumatoid arthritis: do patient-reported swollen and tender joints match clinical and ultrasonography findings? Rheumatology (Oxford). 2020;59(1):129–136. doi:10.1093/rheumatology/kez231
  • Kuettel D, Glinatsi D, Østergaard M, et al. Serial magnetic resonance imaging and ultrasound examinations demonstrate differential inflammatory lesion patterns in soft tissue and bone upon patient-reported flares in rheumatoid arthritis. Arthritis Res Ther. 2020;22(1):19. doi:10.1186/s13075-020-2105-6
  • Peluso G, Michelutti A, Bosello S, Gremese E, Tolusso B, Ferraccioli G. Clinical and ultrasonographic remission determines different chances of relapse in early and long standing rheumatoid arthritis. Ann Rheum Dis. 2011;70(1):172–175. doi:10.1136/ard.2010.129924
  • Ten Wolde S, Breedveld FC, Hermans J, et al. Randomised placebo-controlled study of stopping second-line drugs in rheumatoid arthritis. Lancet. 1996;347:347–352. doi:10.1016/S0140-6736(96)90535-8
  • Ten Wolde S, Hermans J, Breedveld FC, Dijkmans BA. Effect of resumption of second line drugs in patients with rheumatoid arthritis that flared up after treatment discontinuation. Ann Rheum Dis. 1997;56:235–239. doi:10.1136/ard.56.4.235
  • Ollendorf DA, Klingman D, Hazard E, et al. Differences in annual medication costs and rates of dosage increase between tumor necrosis factor-antagonist therapies for rheumatoid arthritis in a managed care population. Clin Ther. 2009;31:825–835. doi:10.1016/j.clinthera.2009.04.002
  • Bongartz T, Sutton AJ, Sweeting MJ, et al. Anti-TNF antibody therapy rheumatoid arthritis and the risk of serious infections and malignancies: systematic review and meta-analysis of rare harmful effects in randomized controlled trials. JAMA. 2006;295:2275–2285. doi:10.1001/jama.295.19.2275
  • Smolen JS, Nash P, Durez P, et al. Maintenance, reduction, or withdrawal of etanercept after treatment with etanercept and methotrexate in patients with moderate rheumatoid arthritis (PRESERVE): a randomised controlled trial. Lancet. 2013;381:918–929. doi:10.1016/S0140-6736(12)61811-X
  • Van Vollenhoven RF, Østergaard M, Leirisalo-Repo M, et al. Full dose, reduced dose or discontinuation of etanercept in rheumatoid arthritis. Ann Rheum Dis. 2016;75:52–58. doi:10.1136/annrheumdis-2014-205726
  • Van den Broek M, Klarenbeek NB, Dirven L, et al. Discontinuation of infliximab and potential predictors of persistent low disease activity in patients with early rheumatoid arthritis and disease activity score-steered therapy: subanalysis of the BeSt study. Ann Rheum Dis. 2011;70:1389–1394. doi:10.1136/ard.2010.147751
  • Smolen JS, Emery P, Fleischmann R, et al. Adjustment of therapy in rheumatoid arthritis on the basis of achievement of stable low disease activity with adalimumab plus methotrexate or methotrexate alone: the randomized controlled OPTIMA trial. Lancet. 2014;383:321–332. doi:10.1016/S0140-6736(13)61751-1
  • Den Broeder AA, van Herwaarden N, van der Maas A, et al. Dose REduction strategy of subcutaneous TNF inhibitors in rheumatoid arthritis: design of a pragmatic randomised non inferiority trial, the DRESS study. BMC Musculoskelet Disord. 2013;14:299. doi:10.1186/1471-2474-14-299
  • Haschka J, Englbrecht M, Hueber AJ, et al. Relaps rates in patients with rheumatoid arthritis in stable remission tapering or stopping antirheumatic therapy: interim results from the prospective randomised controlled RETRO study. Ann Rheum Dis. 2016;75:45–51. doi:10.1136/annrheumdis-2014-206439
  • Tanaka Y, Takeuchi T, Mimori T, et al. Discontinuation of infliximab after attaining low disease activity in patients with rheumatoid arthritis: RRR (remission induction by Remicade in RA) study. Ann Rheum Dis. 2010;69:1286–1291. doi:10.1136/ard.2009.121491
  • Henaux S, Ruyssen-Witrand A, Cantagrel A, et al. Risk of losing remission, low disease activity or radiographic progression in case of bDMARD discontinuation or tapering in rheumatoid arthritis: systematic analysis of the literature and meta-analysis.Ann. Rheum Dis. 2018;77(4):515–522. doi:10.1136/annrheumdis-2017-212423
  • Østergaard M, Leirisalo-Repo M, Uhlig T, et al. In rheumatoid arthritis patients with stable low disease activity on methotrexate plus etanercept, continuation of etanercept is superior both clinically and radiographically to discontinuation: results from a randomized, 3-armed, double-blind clinical trial. Arthritis Rheum. 2013;65(10):S1017–8.
  • Iwamoto T, Ikeda K, Hosokawa J, et al. Prediction of relapse after discontinuation of biologic agents by ultrasonographic assessment in patients with rheumatoid arthritis in clinical remission: high predictive values of total gray-scale and power Doppler scores that represent residual synovial inflammation before discontinuation. Arthritis Care Res (Hoboken). 2014;66(10):1576–1581. doi:10.1002/acr.22303
  • Saleem B, Keen H, Goeb V, et al. Patients with RA in remission on TNF blockers: when and in whom can TNF blocker therapy be stopped? Ann Rheum Dis. 2010;69(9):1636–1642. doi:10.1136/ard.2009.117341
  • Lamers-Karnebeek FB, Luime JJ, Ten Cate DF, et al. Limited value for ultrasonography in predicting flare in rheumatoid arthritis patients with low disease activity stopping TNF inhibitors. Rheumatology (Oxford). 2017;56(9):1560–1565. doi:10.1093/rheumatology/kex184