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Egyptian Rheumatology and Rehabilitation
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Musculoskeletal ultrasonographic evaluation of lower limb enthesopathy in ankylosing spondylitis and Behçet’s disease: Relation to clinical status and disease activity

Egyptian Rheumatology and Rehabilitation volume 43, pages 108–116 (2016)Cite this article

Abstract

Aim of the work

Using clinical and musculoskeletal ultrasonographic (MSUS) examination, we aimed to compare the frequency, pattern, and main sites of peripheral enthesopathies in the lower limbs of ankylosing spondylitis (AS) and Behçet’s disease (BD) patients, and to evaluate their relation with different clinical, laboratory, and functional parameters of both diseases.

Patients and methods

Fifteen AS patients (group I) and 22 BD patients (group II) were examined clinically and by carrying out MSUS for enthesopathy at five entheseal sites of the lower limbs. A control group of 20 apparently healthy male volunteers was also included. An enthesopathy score was calculated for each patient according to the Glasgow ultrasound enthesitis scoring system (GUESS). Disease activity was assessed using the Bath Ankylosing Spondylitis Disease Activity Index and the Behçet’s disease current activity form in both groups, respectively.

Results

The GUESS score was significantly higher (P < 0.05) in group I than in group II (7.27 ± 3.88 vs. 4.68 ± 3.67). In the two patients’ groups, tendon thickening was the most frequent finding detected. Bone erosions and enthesophytes were significantly (P < 0.05) more frequent in group I than in group II. The most commonly affected entheseal sites were the distal Achilles tendon, followed by the proximal plantar fascia. In group I, the GUESS scores significantly correlated with the fatigue scores (P < 0.05), peripheral joint pain scores (P < 0.05), and Bath Ankylosing Spondylitis Functional Index scores (P < 0.05), whereas it showed insignificant correlations with patients’ ages (P > 0.05), disease duration (P > 0.05), spinal pain scores (P > 0.05), local tenderness scores (P > 0.05), morning stiffness score (P > 0.05), total Bath Ankylosing Spondylitis Disease Activity Index (P > 0.05), Bath AS metrology indices (P > 0.05), AS quality of life scores (P > 0.05), radiographic scores (P > 0.05), erythrocyte sedimentation rate (P > 0.05), and C-reactive protein levels (P > 0.05). In group II, the mean GUESS score was significantly higher (P < 0.05) for BD patients with arthritis than for BD patients without arthritis, but it showed insignificant correlation (P > 0.05) with disease activity.

Conclusion

Ultrasonographic changes at the entheseal sites of the lower limbs are prevalent in both AS and BD. These changes are more frequently related to functional and articular involvement. MSUS is more sensitive than clinical examination in detecting enthesopathies of the lower limbs in both AS and BD patients.

References

  1. Iagnocco A, Filippucci E, Meenagh G, Delle Sedie A, Riente L, Bombardieri S, et al. Clin Exp Rheumatol 2006; 24:229–32.

    CAS  PubMed  Google Scholar 

  2. Breban M. Genetics of spondyloarthritis. Best Pract Res Clin Rheumatol 2006; 20:593–599.

    Article  CAS  PubMed  Google Scholar 

  3. Hatemi G, Fresko I, Tascilar K, Yazici H. Increased enthesopathy among Behçet’s syndrome patients with acne and arthritis: an ultrasonography study. Arthritis Rheum 2008; 58(5):1539–1545.

    Article  PubMed  Google Scholar 

  4. Diri E, Mat C, Hamuryudan V, Yurdakul S, Hizli N, Yazici H. Papulopustular skin lesions are seen more frequently in patients with Behçet’s syndrome who have arthritis: a controlled and masked study. Ann Rheum Dis 2001; 60(11):1074–1076.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. D’Agostino MA, Olivieri I. Enthesitis. Best Pract Res Clin Rheumatol 2006; 20(3):473–486.

    Article  PubMed  Google Scholar 

  6. McGonagle D, Gibbon W, Emery P. Classification of inflammatory arthritis by enthesitis. Lancet 1998; 352(9134):1137–1140.

    Article  CAS  PubMed  Google Scholar 

  7. Olivieri I, Padula A, Lisanti ME, Braccini G. Longstanding HLA-B27 associated Achilles tendinitis. Ann Rheum Dis 1992; 51(11):1265.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Smolen JS, Braun J, Dougados M, Emery P, Fitzgerald O, Helliwell P, et al. Treating spondyloarthritis, including ankylosing spondylitis and psoriatic arthritis, to target: recommendations of an international task force. Ann Rheum Dis 2014; 73(1):6–16.

    Article  PubMed  Google Scholar 

  9. D’ Agostino MA, Palazzi C, Olivier I. Entheseal involvement. Clin Exp Rheumatol 2009; 27:S50–S55.

    PubMed  Google Scholar 

  10. Balint PV, Kane D, Wilson H, McInnes IB, Sturrock RD. Ultrasonography of entheseal insertions in the lower limb in spondyloarthropathy. Ann Rheum Dis 2002; 61(10):905–910.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Kane D, Grassi W, Sturrock R, Balint PV. Musculoskeletal ultrasound – a state of the art review in rheumatology. Part 2: clinical indications for musculoskeletal ultrasound in rheumatology. Rheumatology (Oxford) 2004; 43(7):829–838.

    CAS  Google Scholar 

  12. Wakefield RJ, Balint PV, Szkudlarek M, Filippucci E, Backhaus M, D’Agostino MA, et al. OMERACT 7 Special Interest Group Musculoskeletal ultrasound including definitions for ultrasonographic pathology. J Rheumatol 2005; 32(12):2485–2487.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  14. International Study Group for Behcet’s Disease. Criteria for diagnosis of Behcet’s disease [review]. Lancet 1990; 335:1078–1080.

    Google Scholar 

  15. Akkoc Y, Karatepe AG, Akar S, Kirazli Y, Akkoc N. A Turkish version of the Bath Ankylosing Spondylitis Disease Activity Index: reliability and validity. Rheumatol Int 2005; 25(4):280–280284.

    Article  PubMed  Google Scholar 

  16. Karatepe AG, Akkoc Y, Akar S, Kirazli Y, Akkoc N. The Turkish versions of the Bath Ankylosing Spondylitis and Dougados Functional Indices: reliability and validity. Rheumatol Int 2005; 25(8):612–618.

    Article  PubMed  Google Scholar 

  17. Duruöz MT, Doward L, Turan Y, Cerrahoglu L, Yurtkuran M, Calis M, et al. Translation and validation of the Turkish version of the Ankylosing Spondylitis Quality of Life (ASQOL) questionnaire. Rheumatol Int 2013; 33(11):2717–2722.

    Article  PubMed  Google Scholar 

  18. Jenkinson TR, Mallorie PA, Whitelock HC, Kennedy LG, Garrett SL, Calin A. Defining spinal mobility in ankylosing spondylitis (AS): the Bath AS Metrology Index. J Rheumatol 1994; 21:1694–1698.

    CAS  PubMed  Google Scholar 

  19. Lawton G, Bhakta BB, Chamberlain MA, Tennant A. The Behcet’s disease activity index. Rheumatology (Oxford) 2004; 43(1):73–78.

    Article  CAS  Google Scholar 

  20. Sudoł-Szopińska I, Zaniewicz-Kaniewska K, Kwiatkowska B. Spectrum of ultrasound pathologies of Achilles tendon, plantar aponeurosis and flexor digiti brevis tendon heel entheses in patients with clinically suspected enthesitis. Pol J Radiol 2014; 79:402–408.

    Article  PubMed  PubMed Central  Google Scholar 

  21. MacKay K, Mack C, Brophy S, Calin A. The Bath Ankylosing Spondylitis Radiology Index (BASRI): a new, validated approach to disease assessment. Arthritis Rheum 1998; 41(12):2263–22632270.

    Article  CAS  PubMed  Google Scholar 

  22. De Miguel E, Cobo T, Muñoz-Fernández S, Naredo E, Usón J, Acebes JC, et al. Validity of enthesis ultrasound assessment in spondyloarthropathy. Ann Rheum Dis 2009; 68(2):169–174.

    Article  PubMed  Google Scholar 

  23. Rezvani A, Bodur H, Ataman S, Kaya T, Buğdaycı DS, Demir SE et al. Correlations among enthesitis, clinical, radiographic and quality of life parameters in patients with ankylosing spondylitis. Mod Rheumatol 2014; 24(4):651–656.

    Article  PubMed  Google Scholar 

  24. McGonagle D, Marzo-Ortega H, Benjamin M, Emery P. Report on the Second International Enthesitis Workshop. Arthritis Rheum 2003; 48(4):896–905.

    Article  PubMed  Google Scholar 

  25. Alcalde M, Acebes JC, Cruz M, González-Hombrado L, Herrero-Beaumont G, Sánchez-Pernaute O. A sonographic enthesitic index of lower limbs is a valuable tool in the assessment of ankylosing spondylitis. Ann Rheum Dis 2007; 66(8):1015–1019.

    Article  CAS  PubMed  Google Scholar 

  26. François RJ, Braun J, Khan MA. Entheses and enthesitis: a histopathologic review and relevance to spondyloarthritides. Curr Opin Rheumatol 2001; 13(4):255–264.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  28. Lehtinen A, Taavitsainen M, Leirisalo-Repo M. Sonographic analysis of enthesopathy in the lower extremities of patients with spondylarthropathy. Clin Exp Rheumatol 1994; 12(2):143–148.

    CAS  PubMed  Google Scholar 

  29. Chang HK, Lee DH, Jung SM, Choi SJ, Kim JU, Choi YJ, et al. The comparison between Behçet’s disease and spondyloarthritides: does Behçet’s disease belong to the spondyloarthropathy complex?. J Korean Med Sci 2002; 17(4):524–529.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Yurdakul S, Yazici H, Tüzün Y, Pazarli H, Yalçin B, Altaç M, et al. The arthritis of Behçet’s disease: a prospective study. Ann Rheum Dis 1983; 42(5):505–515.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Mata Arnaiz MC, de Miguel Mendieta E. Usefulness of ultrasonography in the assessment of peripheral enthesis in spondyloarthritis. Reumatol Clin 2014; 10(2):113–119.

    Article  PubMed  Google Scholar 

  32. Galluzzo E, Lischi DM, Taglione E, Lombardini F, Pasero G, Perri G, Riente L. Sonographic analysis of the ankle in patients with psoriatic arthritis. Scand J Rheumatol 2000; 29(1):52–55.

    Article  CAS  PubMed  Google Scholar 

  33. Spadaro A, Iagnocco A, Perrotta FM, Modesti M, Scarno A, Valesini G. Clinical and ultrasonography assessment of peripheral enthesitis in ankylosing spondylitis. Rheumatology (Oxford) 2011; 50(11):2080–2086.

    Article  Google Scholar 

  34. Ozkan F, Cetin GY, Inci MF, Bakan B, Yuksel M, Ekerbicer HC, Sayarlioglu M. Increased enthesopathy in patients with familial Mediterranean fever: evaluation with a new sonographic enthesitis index. J Ultrasound Med 2013; 32(2):325–332.

    Article  PubMed  Google Scholar 

  35. Borman P, Koparal S, Babaoğlu S, Bodur H. Ultrasound detection of entheseal insertions in the foot of patients with spondyloarthropathy. Clin Rheumatol 2006; 25(3):373–377.

    Article  PubMed  Google Scholar 

  36. Kiris A, Kaya A, Ozgocmen S, Kocakoc E. Assessment of enthesitis in ankylosing spondylitis by power Doppler ultrasonography. Skeletal Radiol 2006; 35(7):522–528.

    Article  PubMed  Google Scholar 

  37. Benjamin M, McGonagle D. The anatomical basis for disease localisation in seronegative spondyloarthropathy at entheses and related sites. J Anat 2001; 199(Pt 5):503–526.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. McGonagle D. Enthesitis: an autoinflammatory lesion linking nail and joint involvement in psoriatic disease. J Eur Acad Dermatol Venereol 2009; 23: Suppl 1:9–13.

    Article  CAS  PubMed  Google Scholar 

  39. Y Ezzat, W Gaber, SF Abd El-Rahman, M Ezzat, M El Sayed. Ultrasonographic evaluation of lower limb enthesis in patients with early spondyloarthropathie. Egypt Rheumatol 2013; 35:29–35.

    Article  Google Scholar 

  40. Rudwaleit M, Haibel H, Baraliakos X, Listing J, Märker-Hermann E, Zeidler H, et al. The early disease stage in axial spondylarthritis: results from the German Spondyloarthritis Inception Cohort. Arthritis Rheum 2009; 60(3):717–727.

    Article  CAS  PubMed  Google Scholar 

  41. Heuft-Dorenbosch L, van Tubergen A, Spoorenberg A, Landewé R, Dougados M, Mielants H, et al. The influence of peripheral arthritis on disease activity in ankylosing spondylitis patients as measured with the Bath Ankylosing Spondylitis Disease Activity Index. Arthritis Rheum 2004; 51(2):154–159.

    Article  PubMed  Google Scholar 

  42. Spoorenberg A, van Tubergen A, Landewé R, Dougados M, van der Linden S, Mielants H, et al. Measuring disease activity in ankylosing spondylitis: patient and physician have different perspectives. Rheumatology (Oxford) 2005; 44(6):789–795.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Rheumatology and Rehabilitation, Physical Medicine, Faculty of Medicine, Benha University, Al Qalyubia, Egypt

    E. A. Baraka & W. A. Hassan

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  1. E. A. Baraka
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Correspondence to E. A. Baraka.

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Baraka, E.A., Hassan, W.A. Musculoskeletal ultrasonographic evaluation of lower limb enthesopathy in ankylosing spondylitis and Behçet’s disease: Relation to clinical status and disease activity. Egypt Rheumatol Rehabil 43, 108–116 (2016). https://doi.org/10.4103/1110-161X.189641

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