Abstract
The aim of this study is to evaluate the diagnostic utility of ultrasonographic enthesitis assessment in patients with non-radiographic axial spondyloarthritis (nr-axSpA) and to compare different sonographic scoring methods. Patients with nr-axSpA (n = 30) and mechanical back pain (MBP) (n = 30) were enrolled in the study with standardized clinical criteria. For both of the groups, a total of 18 entheses were evaluated in each patient with B mode ultrasound and power Doppler by a sonographer who is blinded to initial clinical and radiological assessments. Glasgow Ultrasound Enthesitis Scoring System (GUESS), Madrid Sonographic Enthesitis Index (MASEI) and D’Agostino grading system were performed. Intra-rater and inter-rater reliability analyses were evaluated with the intraclass correlation coefficient (ICC). There was at least one enthesitis in 96.7% of patients with nr-axSpA. Median values of the number of enthesitis were 5 in nr-axSpA and 0 in MBP. Mean GUESS total scores were 0.9 in MBP and 4.5 in nr-axSpA. Mean MASEI total scores were 2.3 and 10.5, respectively. The sensitivities were 96.7% and 93.3% for GUESS and MASEI while the detected specificities were 80% for both methods. For Intra-rater reliability analysis, ICC was calculated as 0.981 for GUESS and 0.975 for MASEI, while it was calculated as 0.964 and 0.962 for inter-rater reliability analysis. Thus, evaluation of enthesitis with ultrasound is a reliable, helpful tool for the distinction of patients with nr-axSpA from patients with MBP. We favored the use of MASEI because of assessing upper extremity, using power Doppler and having a correlation with disease activity.
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References
Bodur H, Ataman Ş, Buğdaycı DS, Rezvani A, Nas K, Uzunca K, Emlakçıoğlu E, Karatepe AG, Durmuş B, Sezgin M (2012) Description of the registry of patients with ankylosing spondylitis in Turkey: TRASD-IP. Rheumatol Int 32(1):169–176
Nakashima Y, Ohishi M, Okazaki K, Fukushi J-I, Oyamada A, Hara D, Doi T, Akasaki Y, Yamada H, Iwamoto Y (2016) Delayed diagnosis of ankylosing spondylitis in a Japanese population. Mod Rheumatol 26(3):421–425
Rudwaleit M, van der Heijde D, Landewe R, Listing J, Akkoc N, Brandt J, Braun J, Chou CT, Collantes-Estevez E, Dougados M, Huang F, Gu J, Khan MA, Kirazli Y, Maksymowych WP, Mielants H, Sorensen IJ, Ozgocmen S, Roussou E, Valle-Onate R, Weber U, Wei J, Sieper J (2009) The development of Assessment of SpondyloArthritis international Society classification criteria for axial spondyloarthritis (part II): validation and final selection. Ann Rheum Dis 68(6):777–783
Sieper J, Hu X, Black CM, Grootscholten K, van den Broek RW, Kachroo S (2017) Systematic review of clinical, humanistic, and economic outcome comparisons between radiographic and non-radiographic axial spondyloarthritis. Semin Arthritis Rheum 46(6):746–753
Balint PV, D’agostino MA (2012) Spondyloarthritis: a journey within and around the joint. Rheumatology 51(suppl_7):vii13–vii17
Mander M, Simpson J, McLellan A, Walker D, Goodacre J, Dick WC (1987) Studies with an enthesis index as a method of clinical assessment in ankylosing spondylitis. Ann Rheum Dis 46(3):197–202
Heuft-Dorenbosch L, Spoorenberg A, Van Tubergen A, Landewe R, Van der Tempel H, Mielants H, Dougados M, Van der Heijde D (2003) Assessment of enthesitis in ankylosing spondylitis. Ann Rheum Dis 62(2):127–132
Maksymowych WP, Mallon C, Morrow S, Shojania K, Olszynski WP, Wong RL, Sampalis J, Conner-Spady B (2009) Development and validation of the spondyloarthritis research consortium of Canada (SPARCC) enthesitis index. Ann Rheum Dis 68(6):948–953
Balint PV, Kane D, Wilson H, McInnes IB, Sturrock RD (2002) Ultrasonography of entheseal insertions in the lower limb in spondyloarthropathy. Ann Rheum Dis 61(10):905–910
Wakefield RJ, Balint PV, Szkudlarek M, Filippucci E, Backhaus M, D’Agostino M-A, Sanchez EN, Iagnocco A, Schmidt WA, Bruyn GA (2005) Musculoskeletal ultrasound including definitions for ultrasonographic pathology. J Rheumatol 32(12):2485–2487
Gandjbakhch F, Terslev L, Joshua F, Wakefield RJ, Naredo E, D’Agostino MA, Force OUT (2011) Ultrasound in the evaluation of enthesitis: status and perspectives. Arthritis Res Ther 13(6):1–15
Alcalde M, Acebes JC, Cruz M, Gonzalez-Hombrado L, Herrero-Beaumont G, Sánchez-Pernaute O (2007) A sonographic enthesitic index of lower limbs is a valuable tool in the assessment of ankylosing spondylitis. Ann Rheum Dis 66(8):1015–1019
de Miguel E, Cobo T, Muñoz-Fernández S, Naredo E, Usón J, Acebes JC, Andréu JL, Martín-Mola E (2009) Validity of enthesis ultrasound assessment in spondyloarthropathy. Ann Rheum Dis 68(2):169–174
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
Sieper J, Rudwaleit M, Baraliakos X, Brandt J, Braun J, Burgos-Vargas R, Dougados M, Hermann K, Landewe R, Maksymowych W (2009) The Assessment of Spondylo Arthritis international Society (ASAS) handbook: a guide to assess spondyloarthritis. Ann Rheum Dis 68(Suppl 2):ii1–ii44
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
Rudwaleit M, Jurik A-G, Hermann KA, Landewé R, van der Heijde D, Baraliakos X, Marzo-Ortega H, Østergaard M, Braun J, Sieper J (2009) Defining active sacroiliitis on magnetic resonance imaging (MRI) for classification of axial spondyloarthritis: a consensual approach by the ASAS/OMERACT MRI group. Ann Rheum Dis 68(10):1520–1527
Lanfranchi M-A, Leluc O, Tavano A, Wormser C, Morange S, Chagnaud C, Pradel V, Lafforgue P, Pham T (2017) Are ultrasound findings similar in patients with axial spondyloarthritis and in athlete entheses? J Rheumatol 44(5):609–612
de Miguel E, Muñoz-Fernández S, Castillo C, Cobo-Ibáñez T, Martín-Mola E (2011) Diagnostic accuracy of enthesis ultrasound in the diagnosis of early spondyloarthritis. Ann Rheum Dis 70(3):434–439
D’Agostino MA, Terslev L (2016) Imaging evaluation of the entheses. Rheum Dis Clin N Am 42(4):679–693
D’agostino MA, Aegerter P, Bechara K, Salliot C, Judet O, Chimenti MS, Monnet D, Le Parc J-M, Landais P, Breban M (2011) How to diagnose spondyloarthritis early? Accuracy of peripheral enthesitis detection by power Doppler ultrasonography. Ann Rheum Dis 70(8):1433–1440
Falcão S, De Miguel E, Castillo C, Branco J, Martín-Mola E (2012) Doppler ultrasound—a valid and reliable tool to assess spondyloarthritis. Acta Reumatol Port 37(3):212–217
Torp-Pedersen S, Christensen R, Szkudlarek M, Ellegaard K, D’agostino MA, Iagnocco A, Naredo E, Balint P, Wakefield RJ, Torp-Pedersen A (2015) Power and color Doppler ultrasound settings for inflammatory flow: impact on scoring of disease activity in patients with rheumatoid arthritis. Arthritis Rheumatol 67(2):386–395
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All procedures performed in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The study was approved by local ethic committee of Marmara University School of Medicine [approval number: (09.2015.125/70737436-050.06.04-)]. The manuscript has two authors and each author is responsible for the content and writing of the paper.
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Ozsoy-Unubol, T., Yagci, I. Is ultrasonographic enthesitis evaluation helpful for diagnosis of non-radiographic axial spondyloarthritis?. Rheumatol Int 38, 2053–2061 (2018). https://doi.org/10.1007/s00296-018-4164-4
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DOI: https://doi.org/10.1007/s00296-018-4164-4