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Performance of ultrasound to monitor Achilles enthesitis in patients with ankylosing spondylitis during TNF-a antagonist therapy

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Abstract

Enthesitis is considered as the primary anatomical lesion in ankylosing spondylitis (AS). We aimed to investigate the potential of ultrasound to detect early changes after TNF-a antagonist therapy of Achilles enthesitis of AS patients. One hundred AS patients with active disease, requiring TNF-a antagonist therapy, were included (etanercept n = 25, infliximab n = 25, adalimumab n = 25, non-biologic disease-modifying antirheumatic drugs (DMARDs) n = 25). Physical examination was performed to evaluate disease activity and detect Achilles enthesitis and/or retrocalcaneal bursitis. Ultrasound of the Achilles enthesitis was performed bilaterally. Follow-up examinations were performed 3 months after the initiation of therapy. Gray scale (GS) scores, Power Doppler (PD) scores, and total additive scores (TS) decreased significantly during TNF-a antagonist therapy but not in traditional non-biologic traditional DMARDs group. The bath ankylosing spondylitis disease activity index (BASDAI), bath ankylosing spondylitis metrology index (BASMI), bath ankylosing spondylitis functional index (BASFI), and Maastricht ankylosing spondylitis enthesitis score (MASES) all showed significant improvements. When three different TNF-a antagonists were analyzed separately, no significant difference was observed in GS, PD, and total scores. Subclinical Achilles enthesitis, detected only with GS ultrasound, is present in a subset of AS patients and a significant improvement can be demonstrated after 3 months of TNF-a antagonist therapy. Doppler ultrasound provides a reliable estimation to monitor the therapeutic response to TNF antagonists in AS patients with Achilles enthesitis. TNF-a antagonists have been shown to be effective in decreasing ultrasound signs of enthesitis after 3 months of therapy in AS patients.

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References

  1. Zochling J (2008) Assessment and treatment of ankylosing spondylitis: current status and future directions. Curr Opin Rheumatol 20(4):398–403

    Article  PubMed  Google Scholar 

  2. Heuft-Dorenbosch L, Spoorenberg A, van Tubergen A et al (2003) Assessment of enthesitis in ankylosing spondylitis. Ann Rheum Dis 62(2):127–132

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  3. Sengupta R, Stone MA (2007) The assessment of ankylosing spondylitis in clinical practice. Nat Clin Pract Rheumatol 3(9):496–503

    Article  CAS  PubMed  Google Scholar 

  4. Backhaus M, Burmester GR, Gerber T et al (2001) Guidelines for musculoskeletal ultrasound in rheumatology. Ann Rheum Dis 60(7):641–649

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  5. Hamdi W, Bouaziz Chelli M, Ghannouchi MM, Hawel M, Ladeb MF, Kchir MM (2013) Performance of ultrasounds compared with radiographs to detect chronic enthesitis signs in patients with ankylosing spondylitis. Rheumatol Int 33(2):497–499

    Article  PubMed  Google Scholar 

  6. Marzo-Ortega H, McGonagle D, O’Connor P, Emery P (2001) Efficacy of etanercept in the treatment of the entheseal pathology in resistant spondylarthropathy: a clinical and magnetic resonance imaging study. Arthritis Rheum 44(9):2112–2117

    Article  CAS  PubMed  Google Scholar 

  7. Naredo E, Batlle-Gualda E, Garcia-Vivar ML et al (2010) Power Doppler ultrasonography assessment of entheses in spondyloarthropathies: response to therapy of entheseal abnormalities. J Rheumatol 37(10):2110–2117

    Article  PubMed  Google Scholar 

  8. Filippucci E, Aydin SZ, Karadag O et al (2009) Reliability of high-resolution ultrasonography in the assessment of Achilles tendon enthesopathy in seronegative spondyloarthropathies. Ann Rheum Dis 68(12):1850–1855

    Article  CAS  PubMed  Google Scholar 

  9. Torp-Pedersen ST, Terslev L (2008) Settings and artefacts relevant in colour/power Doppler ultrasound in rheumatology. Ann Rheum Dis 67(2):143–149

    Article  CAS  PubMed  Google Scholar 

  10. Braun J, Davis J, Dougados M, Sieper J, van der Linden S, van der Heijde D (2006) First update of the international ASAS consensus statement for the use of anti-TNF agents in patients with ankylosing spondylitis. Ann Rheum Dis 65(3):316–320

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  11. Braun J, Brandt J, Listing J et al (2002) Treatment of active ankylosing spondylitis with infliximab: a randomised controlled multicentre trial. Lancet 359(9313):1187–1193

    Article  CAS  PubMed  Google Scholar 

  12. Aydin SZ, Karadag O, Filippucci E et al (2010) Monitoring Achilles enthesitis in ankylosing spondylitis during TNF-alpha antagonist therapy: an ultrasound study. Rheumatology (Oxford) 49(3):578–582

    Article  CAS  Google Scholar 

  13. Gorman JD, Sack KE, Davis JC Jr (2002) Treatment of ankylosing spondylitis by inhibition of tumor necrosis factor alpha. N Engl J Med 346(18):1349–1356

    Article  CAS  PubMed  Google Scholar 

  14. van der Linden S, Valkenburg HA, Cats A (1984) Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria. Arthritis Rheum 27(4):361–368

    Article  PubMed  Google Scholar 

  15. Wakefield RJ, Balint PV, Szkudlarek M et al (2005) Musculoskeletal ultrasound including definitions for ultrasonographic pathology. J Rheumatol 32(12):2485–2487

    PubMed  Google Scholar 

  16. D’Agostino MA, Said-Nahal R, Hacquard-Bouder C, Brasseur JL, Dougados M, Breban M (2003) Assessment of peripheral enthesitis in the spondylarthropathies by ultrasonography combined with power Doppler: a cross-sectional study. Arthritis Rheum 48(2):523–533

    Article  PubMed  Google Scholar 

  17. van der Linden S, van der Heijde D (2000) Clinical aspects, outcome assessment, and management of ankylosing spondylitis and postenteric reactive arthritis. Curr Opin Rheumatol 12(4):263–268

    Article  PubMed  Google Scholar 

  18. Maksymowych WP (2009) Progress in spondylarthritis. Spondyloarthritis: lessons from imaging. Arthritis Res ther 11(3):222

    Article  PubMed Central  PubMed  Google Scholar 

  19. Wakefield RJ, O’Connor PJ, Conaghan PG et al (2007) Finger tendon disease in untreated early rheumatoid arthritis: a comparison of ultrasound and magnetic resonance imaging. Arthritis Rheum 57(7):1158–1164

    Article  CAS  PubMed  Google Scholar 

  20. Kamel M, Eid H, Mansour R (2003) Ultrasound detection of heel enthesitis: a comparison with magnetic resonance imaging. J Rheumatol 30(4):774–778

    PubMed  Google Scholar 

  21. Laatiris A, Amine B, Ibn Yacoub Y, Hajjaj-Hassouni N (2012) Enthesitis and its relationships with disease parameters in Moroccan patients with ankylosing spondylitis. Rheumatol Int 32(3):723–727

    Article  PubMed  Google Scholar 

  22. Braun J, Pham T, Sieper J et al (2003) International ASAS consensus statement for the use of anti-tumour necrosis factor agents in patients with ankylosing spondylitis. Ann Rheum Dis 62(9):817–824

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Zochling J (2011) Measures of symptoms and disease status in ankylosing spondylitis: Ankylosing Spondylitis Disease Activity Score (ASDAS), Ankylosing Spondylitis Quality of Life Scale (ASQoL), Bath Ankylosing Spondylitis Disease Activity Index (BASDAI), Bath Ankylosing Spondylitis Functional Index (BASFI), Bath Ankylosing Spondylitis Global Score (BAS-G), Bath Ankylosing Spondylitis Metrology Index (BASMI), Dougados Functional Index (DFI), and Health Assessment Questionnaire for the Spondylarthropathies (HAQ-S). Arthritis Care Res (Hoboken) 63(Suppl 11):S47–S58

    Article  Google Scholar 

  24. van der Heijde D, Landewe R, Einstein S et al (2008) Radiographic progression of ankylosing spondylitis after up to two years of treatment with etanercept. Arthritis Rheum 58(5):1324–1331

    Article  PubMed  Google Scholar 

  25. van der Heijde D, Landewe R, Baraliakos X et al (2008) Radiographic findings following two years of infliximab therapy in patients with ankylosing spondylitis. Arthritis Rheum 58(10):3063–3070

    Article  PubMed  Google Scholar 

  26. van der Heijde D, Salonen D, Weissman BN et al (2009) Assessment of radiographic progression in the spines of patients with ankylosing spondylitis treated with adalimumab for up to 2 years. Arthritis Res Ther 11(4):R127

    Article  PubMed Central  PubMed  Google Scholar 

  27. Sieper J, Baraliakos X, Listing J et al (2005) Persistent reduction of spinal inflammation as assessed by magnetic resonance imaging in patients with ankylosing spondylitis after 2 yrs of treatment with the anti-tumour necrosis factor agent infliximab. Rheumatology (Oxford) 44(12):1525–1530

    Article  CAS  Google Scholar 

  28. Zayat AS, Conaghan PG, Sharif M, Freeston JE, Wenham C, Hensor EM et al (2011) Do non-steroidal anti-inflammatory drugs have a significant effect on detection and grading of ultrasound-detected synovitis in patients with rheumatoid arthritis? Results from a randomised study. Ann Rheum Dis 70(10):1746–1751

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank experienced technician Yan-hong Wang and Chun-mei Fan for their excellent technical assistance.

Disclosure

None.

Funding

This work was supported by grants from the National Natural Science Foundation of China (No.81202299), Xijing Hospital Foundation (No.XJGX13LC21), and Pfizer 2010 China RA Grant (No.WS1595293).

Ethics approval

The approval was granted from the Ethics Committee of Fourth Military Medical University. All patients and controls gave their informed consent to participate in the study.

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Correspondence to Cong-hua Wang, Xue-yi Li or Zhen-biao Wu.

Additional information

Cong-hua Wang, Yuan Feng, Zhen Ren and Xichao Yang contributed equally to this work.

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Wang, Ch., Feng, Y., Ren, Z. et al. Performance of ultrasound to monitor Achilles enthesitis in patients with ankylosing spondylitis during TNF-a antagonist therapy. Clin Rheumatol 34, 1073–1078 (2015). https://doi.org/10.1007/s10067-015-2939-5

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  • DOI: https://doi.org/10.1007/s10067-015-2939-5

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