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Positive rate and prognostic significance of the superb microvascular imaging signal in joints of rheumatoid arthritis patients in remission with normal C-reactive protein levels and erythrocyte sedimentation rates

  • Original Article–Orthopedics
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Abstract

Purpose

This study aimed to evaluate the positive rate and prognostic significance of superb microvascular imaging (SMI) in rheumatoid arthritis (RA) patients in remission with normal C-reactive protein (CRP) levels and erythrocyte sedimentation rates (ESR).

Methods

The study enrolled 112 RA patients, and ultrasound (US) assessment was performed on 28 joints of each patient.

Results

The SMI signal-positive rates for each joint were: metacarpophalangeal (MCP) joints: 20.5%, wrist joints: 43.8%, metatarsophalangeal (MTP) joints: 17.0%, and other foot joints: 25.0%. Investigation of the prognostic significance of the SMI signal in each joint revealed that only in the MTP joints was the total score of the SMI signal in the patients with relapse significantly higher than that in the patients with remission (P = 0.01). Comparison of the receiver operating characteristics curves for predicting relapse showed that the area under the curve (AUC) of the MTP joints was the highest (AUC = 0.66) of the investigated joints. The optimal threshold for the total MTP SMI score was 1 (accuracy = 83.3%). Positive/negative data of the SMI signal in the MTP joints were not significantly associated with the values of conventional disease activity markers.

Conclusion

In RA patients in remission with normal CRP and ESR levels, the percentage of positive SMI signal was highest in the wrist joints. However, the accuracy of the SMI signal for predicting relapse was greatest for the MTP joints, suggesting that US assessment of the MTP joints by SMI is useful for predicting relapse in these patients.

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Abbreviations

SMI:

Superb microvascular imaging

MCP:

Metacarpophalangeal

MTP:

Metatarsophalangeal

ROC:

Receiver operating characteristics

AUC:

Area under the curve

References

  1. Smolen JS, Aletaha D, McInnes IB. Rheumatoid arthritis. Lancet. 2016;388:2023–38.

    Article  CAS  Google Scholar 

  2. Aga AB, Lie E, Uhlig T, et al. Time trends in disease activity, response and remission rates in rheumatoid arthritis during the past decade: results from the NOR-DMARD study 2000–2010. Ann Rheum Dis. 2015;74:381–8.

    Article  CAS  Google Scholar 

  3. Bechman K, Tweehuysen L, Garrood T, et al. Flares in rheumatoid arthritis patients with low disease activity: predictability and association with worse clinical outcomes. J Rheumatol. 2018;45:1515–21.

    Article  CAS  Google Scholar 

  4. Goekoop-Ruiterman YP, Huizinga TW. Rheumatoid arthritis: can we achieve true drug-free remission in patients with RA? Nat Rev Rheumatol. 2010;6:68–70.

    Article  Google Scholar 

  5. Smolen JS, Landewé RBM, Bijlsma JWJ, et al. EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs: 2019 update. Ann Rheum Dis. 2020;79:685–99.

    Article  CAS  Google Scholar 

  6. Vastesaeger N, Xu S, Aletaha D, et al. A pilot risk model for the prediction of rapid radiographic progression in rheumatoid arthritis. Rheumatology (Oxford). 2009;48:1114–21.

    Article  CAS  Google Scholar 

  7. Wells G, Becker JC, Teng J, et al. Validation of the 28-joint Disease Activity Score (DAS28) and European League against rheumatism response criteria based on C-reactive protein against disease progression in patients with rheumatoid arthritis, and comparison with the DAS28 based on erythrocyte sedimentation rate. Ann Rheum Dis. 2009;68:954–60.

    Article  CAS  Google Scholar 

  8. 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;70:404–13.

    Article  Google Scholar 

  9. Ohrndorf S, Backhaus M. Advances in sonographic scoring of rheumatoid arthritis. Ann Rheum Dis. 2013;72:ii69-75.

    Article  Google Scholar 

  10. Scirè CA, Montecucco C, Codullo V, et al. Ultrasonographic evaluation of joint involvement in early rheumatoid arthritis in clinical remission: power Doppler signal predicts short-term relapse. Rheumatology (Oxford). 2009;48:1092–7.

    Article  Google Scholar 

  11. Peluso G, Michelutti A, Bosello S, et al. Clinical and ultrasonographic remission determines different chances of relapse in early and long standing rheumatoid arthritis. Ann Rheum Dis. 2011;70:172–5.

    Article  Google Scholar 

  12. 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;64:67–76.

    Article  Google Scholar 

  13. Yoshimi R, Hama M, Takase K, et al. Ultrasonography is a potent tool for the prediction of progressive joint destruction during clinical remission of rheumatoid arthritis. Mod Rheumatol. 2013;23:456–65.

    Article  CAS  Google Scholar 

  14. 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. 2014;66:1576–81.

    Article  Google Scholar 

  15. Nguyen H, Ruyssen-Witrand A, Gandjbakhch F, et al. 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;53:2110–8.

    Article  Google Scholar 

  16. Han J, Geng Y, Deng X, Zhang Z. Subclinical synovitis assessed by ultrasound predicts flare and progressive bone erosion in rheumatoid arthritis patients with clinical remission: a systematic review and metaanalysis. J Rheumatol. 2016;43:2010–8.

    Article  Google Scholar 

  17. Kawashiri SY, Fujikawa K, Nishino A, et al. Ultrasound-detected bone erosion is a relapse risk factor after discontinuation of biologic disease-modifying antirheumatic drugs in patients with rheumatoid arthritis whose ultrasound power Doppler synovitis activity and clinical disease activity are well controlled. Arthritis Res Ther. 2017;19:108.

    Article  Google Scholar 

  18. Matsuo H, Imamura A, Shimizu M, et al. Prediction of recurrence and remission using superb microvascular imaging in rheumatoid arthritis. J Med Ultrason (2001). 2020;47:131–8.

    Article  Google Scholar 

  19. Naredo E, Valor L, De la Torre I, et al. Ultrasound joint inflammation in rheumatoid arthritis in clinical remission: how many and which joints should be assessed? Arthritis Care Res (Hoboken). 2013;65:512–7.

    Article  Google Scholar 

  20. Backhaus M, Burmester GR, Gerber T, et al. Guidelines for musculoskeletal ultrasound in rheumatology. Ann Rheum Dis. 2001;60:641–9.

    Article  CAS  Google Scholar 

  21. Szkudlarek M, Court-Payen M, Jacobsen S, et al. Interobserver agreement in ultrasonography of the finger and toe joints in rheumatoid arthritis. Arthritis Rheum. 2003;48:955–62.

    Article  Google Scholar 

  22. Sun X, Deng X, Xie W, et al. The agreement between ultrasound-determined joint inflammation and clinical signs in patients with rheumatoid arthritis. Arthritis Res Ther. 2019;21:100.

    Article  Google Scholar 

  23. Terslev L, Torp-Pedersen S, Qvistgaard E, et al. Doppler ultrasound findings in healthy wrists and finger joints. Ann Rheum Dis. 2004;63:644–8.

    Article  CAS  Google Scholar 

  24. Dalal DS, Zhang T, Shireman TI. Medicare expenditures for conventional and biologic disease-modifying agents commonly used for the treatment of rheumatoid arthritis. Semin Arthritis Rheum. 2020;50:822–6.

    Article  CAS  Google Scholar 

  25. Aletaha D, Smolen JS. Diagnosis and management of rheumatoid arthritis: a review. JAMA. 2018;320:1360–72.

    Article  Google Scholar 

  26. Kawahara R, Nakabo S, Shimizu M, et al. Feasibility of patient-oriented ultrasound joint selection: Cross-sectional observational study on rheumatoid arthritis. Mod Rheumatol. 2020;30:975–81.

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by JSPS KAKENHI (18K12103).

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Correspondence to Hidemasa Matsuo.

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Conflict of interest

Y. Tabuchi receives instructor fees from Asahi Kasei Pharma, Astellas Pharma, GlaxoSmithKline, Mitsubishi Tanabe Pharma, and Nippon Shinyaku, and speaker fees from AbbVie, Chugai Pharmaceutical, Eli Lilly, Janssen Pharmaceutical, Mitsubishi Tanabe Pharma, Nippon Shinyaku, and Novartis Pharma. M.H. and H.I. work in a department that received financial support from Nagahama City, Toyooka City, and five pharmaceutical companies (Mitsubishi Tanabe Pharma, Chugai Pharmaceutical, UCB Japan, Ayumi, and Asahi Kasei Pharma). M.H. receives research grants and/or speaker fees from Bristol-Myers, Eisai, Eli Lilly, and Mitsubishi Tanabe Pharma. H.I. receives research grants from Bristol-Myers, Eisai, Mochida, and Taisho. The KURAMA cohort study is supported by a grant from Daiichi-Sankyo. The present study was an investigator-initiated study. These companies played no role in study design, data collection or analysis, writing of the manuscript, or the decision to submit for publication. H.M., R.Y., A.I., M.S., M.I., Y. Tsuji, S.N., H.T,. T.N., A.M., and Y.F. declare no competing financial interests.

Ethical statements

This study was conducted in accordance with the principles set down in the Declaration of Helsinki and was approved by the ethics committee of Kyoto University (R0357). All patients provided written informed consent.

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Matsuo, H., Tabuchi, Y., Yukimatsu, R. et al. Positive rate and prognostic significance of the superb microvascular imaging signal in joints of rheumatoid arthritis patients in remission with normal C-reactive protein levels and erythrocyte sedimentation rates. J Med Ultrasonics 48, 353–359 (2021). https://doi.org/10.1007/s10396-021-01102-5

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