Staging achilles tendinopathy using ultrasound imaging: the development and investigation of a new ultrasound imaging criteria based on the continuum model of tendon pathology

Wesley Matthews, Richard Ellis, James W Furness, Evelyne Rathbone, Wayne Hing, Wesley Matthews, Richard Ellis, James W Furness, Evelyne Rathbone, Wayne Hing

Abstract

Aim: To develop a standardised ultrasound imaging (USI)-based criteria for the diagnosis of tendinopathy that aligns with the continuum model of tendon pathology. Secondary aims were to assess both the intra-rater and inter-rater reliability of the criteria.

Methods: A criteria was developed following a face validity assessment and a total of 31 Achilles tendon ultrasound images were analysed. Intra-rater and inter-rater reliability were assessed for overall tendinopathy stage (normal, reactive/early dysrepair or late dysrepair/degenerative) as well as for individual parameters (thickness, echogenicity and vascularity). Quadratic weighted kappa (kw) was used to report on reliability.

Results: Intra-rater reliability was 'substantial' for overall tendinopathy staging (kw rater A; 0.77, 95% CI 0.59 to 0.94, rater B; 0.70, 95% CI 0.52 to 0.89) and ranged from 'substantial' to 'almost perfect' for thickness (kw rater A; 0.75, 95% CI 0.59 to 0.90, rater B; 0.84, 95% CI 0.71 to 0.98), echogenicity (kw rater A; 0.78, 95% CI 0.62 to 0.95, rater B; 0.73, 95% CI 0.58 to 0.89) and vascularity (kw rater A; 0.86, 95% CI 0.74 to 0.98, rater B; 0.89, 95% CI 0.79 to 0.99). Inter-rater reliability ranged from 'substantial' to 'almost perfect' for overall tendinopathy staging (kw round 1; 0.75, 95% CI 0.58 to 0.91, round 2; 0.81, 95% CI 0.63 to 0.99), thickness (kw round 1; 0.65, 95% CI 0.48 to 0.83, round 2; 0.77, 95% CI 0.60 to 0.93), echogenicity (kw round 1; 0.70, 95% CI 0.54 to 0.85, round 2; 0.76, 95% CI 0.58 to 0.94) and vascularity (kw round 1; 0.89, 95% CI 0.79 to 0.99, round 2; 0.86, 95% CI 0.74 to 0.98). Inter-rater reliability increased from 'substantial' in round 1 (kw 0.75, 95% CI 0.58 to 0.91) to 'almost perfect' in round 2 (0.81, 95% CI 0.63 to 0.99).

Conclusion: Intra-rater and inter-rater reliability were 'substantial' to 'almost perfect' when utilising an USI-based criteria to diagnose Achilles tendinopathy. This is the first study to use the continuum model of tendon pathology to develop an USI-based criteria to diagnose tendinopathy.

Keywords: diagnosis; tendinopathy; tendinosis; tendon; ultrasound.

Conflict of interest statement

Competing interests: None declared.

© Author(s) (or their employer(s)) 2020. Re-use permitted under CC BY-NC. No commercial re-use. See rights and permissions. Published by BMJ.

Figures

Figure 1
Figure 1
Flow chart of overall study design.
Figure 2
Figure 2
US-based criteria staging tendinopathy using the continuum model of tendon pathology.

References

    1. Scott A, Squier K, Alfredson H, et al. . Icon 2019: international scientific tendinopathy symposium consensus: clinical terminology. Br J Sports Med 2020;54:260–2. 10.1136/bjsports-2019-100885
    1. Scott A, Ashe MC. Common tendinopathies in the upper and lower extremities. Curr Sports Med Rep 2006;5:233–41. 10.1097/01.CSMR.0000306421.85919.9c
    1. McCreesh K, Lewis J. Continuum model of tendon pathology—where are we now? Int J Exp Pathol 2013;94:242–7. 10.1111/iep.12029
    1. Rees JD, Maffulli N, Cook J. Management of tendinopathy. Am J Sports Med 2009;37:1855–67. 10.1177/0363546508324283
    1. Cassel M, Baur H, Hirschmüller A, et al. . Prevalence of Achilles and patellar tendinopathy and their association to intratendinous changes in adolescent athletes. Scand J Med Sci Sports 2015;25:e310–8. 10.1111/sms.12318
    1. Hopkins C, Fu S-C, Chua E, et al. . Critical review on the socio-economic impact of tendinopathy. Asia Pac J Sports Med Arthrosc Rehabil Technol 2016;4:9–20. 10.1016/j.asmart.2016.01.002
    1. Abate M, Silbernagel KG, Siljeholm C, et al. . Pathogenesis of tendinopathies: inflammation or degeneration? Arthritis Res Ther 2009;11:235–35. 10.1186/ar2723
    1. Arnoczky SP, Lavagnino M, Egerbacher M. The mechanobiological aetiopathogenesis of tendinopathy: is it the over-stimulation or the under-stimulation of tendon cells? Int J Exp Pathol 2007;88:217–26. 10.1111/j.1365-2613.2007.00548.x
    1. Cook JL, Purdam CR. Is tendon pathology a continuum? A pathology model to explain the clinical presentation of load-induced tendinopathy. Br J Sports Med 2009;43:409–16. 10.1136/bjsm.2008.051193
    1. Fu S-C, Rolf C, Cheuk Y-C, et al. . Deciphering the pathogenesis of tendinopathy: a three-stages process. Sports Med Arthrosc Rehabil Ther Technol 2010;2:30. 10.1186/1758-2555-2-30
    1. Cook JL, Rio E, Purdam CR, et al. . Revisiting the continuum model of tendon pathology: what is its merit in clinical practice and research? Br J Sports Med 2016;50:1187–91. 10.1136/bjsports-2015-095422
    1. Rees JD, Stride M, Scott A. Tendons—time to revisit inflammation. Br J Sports Med 2014;48:1553–7. 10.1136/bjsports-2012-091957
    1. Scott A, Docking S, Vicenzino B, et al. . Sports and exercise-related tendinopathies: a review of selected topical issues by participants of the second International scientific tendinopathy symposium (ISTS) Vancouver 2012. Br J Sports Med 2013;47:536–44. 10.1136/bjsports-2013-092329
    1. Coombes BK, Bisset L, Vicenzino B. Management of lateral elbow tendinopathy: one size does not fit all. J Orthop Sports Phys Ther 2015;45:938–49. 10.2519/jospt.2015.5841
    1. Lewis J, McCreesh K, Roy J-S, et al. . Rotator cuff tendinopathy: navigating the diagnosis-management conundrum. J Orthop Sports Phys Ther 2015;45:923–37. 10.2519/jospt.2015.5941
    1. Lewis J. Rotator cuff related shoulder pain: assessment, management and uncertainties. Man Ther 2016;23:57–68. 10.1016/j.math.2016.03.009
    1. Malliaras P, Cook J, Purdam C, et al. . Patellar tendinopathy: clinical diagnosis, load management, and advice for challenging case presentations. J Orthop Sports Phys Ther 2015;45:887–98. 10.2519/jospt.2015.5987
    1. Scase E, Purdam C, Cook J. Matching tendinopathy stage with efficacious intervention. Soundeffects 2011;4:14–18.
    1. Maffulli N, Khan KM, Puddu G. Overuse tendon conditions: time to change a confusing terminology. Arthroscopy 1998;14:840–3. 10.1016/S0749-8063(98)70021-0
    1. Littlewood C, Malliaras P, Bateman M, et al. . The central nervous system-—an additional consideration in 'rotator cuff tendinopathy' and a potential basis for understanding response to loaded therapeutic exercise. Man Ther 2013;18:468–72. 10.1016/j.math.2013.07.005
    1. Coombes BK, Bisset L, Vicenzino B. A new integrative model of lateral epicondylalgia. Br J Sports Med 2009;43:252–8. 10.1136/bjsm.2008.052738
    1. Cook JL, Khan KM, Kiss ZS, et al. . Reproducibility and clinical utility of tendon palpation to detect patellar tendinopathy in young basketball players. Victorian Institute of sport tendon Study Group. Br J Sports Med 2001;35:65. 10.1136/bjsm.35.1.65
    1. Grimaldi A, Mellor R, Nicolson P, et al. . Utility of clinical tests to diagnose MRI-confirmed gluteal tendinopathy in patients presenting with lateral hip pain. Br J Sports Med 2017;51:519–24. 10.1136/bjsports-2016-096175
    1. Hutchison A-M, Evans R, Bodger O, et al. . What is the best clinical test for Achilles tendinopathy? Foot Ankle Surg 2013;19:112–7. 10.1016/j.fas.2012.12.006
    1. Khan KM, Forster BB, Robinson J, et al. . Are ultrasound and magnetic resonance imaging of value in assessment of Achilles tendon disorders? A two year prospective study. Br J Sports Med 2003;37:149–53. 10.1136/bjsm.37.2.149
    1. Warden SJ, Kiss ZS, Malara FA, et al. . Comparative accuracy of magnetic resonance imaging and ultrasonography in confirming clinically diagnosed patellar tendinopathy. Am J Sports Med 2007;35:427–36. 10.1177/0363546506294858
    1. Westacott DJ, Minns JI, Foguet P. The diagnostic accuracy of magnetic resonance imaging and ultrasonography in gluteal tendon tears—a systematic review. Hip Int 2011;21:637–45. 10.5301/HIP.2011.8759
    1. Rio E, Moseley L, Purdam C, et al. . The pain of tendinopathy: physiological or pathophysiological? Sports Med 2014;44:9–23. 10.1007/s40279-013-0096-z
    1. Docking SI, Ooi CC, Connell D. Tendinopathy: is imaging telling us the entire story? J Orthop Sports Phys Ther 2015;45:842–52. 10.2519/jospt.2015.5880
    1. McAuliffe S, McCreesh K, Culloty F, et al. . Can ultrasound imaging predict the development of Achilles and patellar tendinopathy? A systematic review and meta-analysis. Br J Sports Med 2016;50:1516–23. 10.1136/bjsports-2016-096288
    1. Matthews W, Ellis R, Furness J, et al. . Classification of tendon matrix change using ultrasound imaging: a systematic review and meta-analysis. Ultrasound Med Biol 2018;44:2059–80. 10.1016/j.ultrasmedbio.2018.05.022
    1. Ingwersen KG, Hjarbaek J, Eshoej H, et al. . Ultrasound assessment for grading structural tendon changes in supraspinatus tendinopathy: an inter-rater reliability study. BMJ Open 2016;6:e011746. 10.1136/bmjopen-2016-011746
    1. Sunding K, Fahlström M, Werner S, et al. . Evaluation of Achilles and patellar tendinopathy with greyscale ultrasound and colour Doppler: using a four-grade scale. Knee Surg Sports Traumatol Arthrosc 2016;24:1988–96. 10.1007/s00167-014-3270-4
    1. Ellis R, Manuel T. Identifying tendon matrix changes with ultrasound imaging: a literature review and proposed ultrasound criteria for staging for tendinopathy. Physiotherapy 2015;101:eS357 10.1016/j.physio.2015.03.570
    1. Malliaras P, Purdam C, Maffulli N, et al. . Temporal sequence of greyscale ultrasound changes and their relationship with neovascularity and pain in the patellar tendon. Br J Sports Med 2010;44:944–7. 10.1136/bjsm.2008.054916
    1. Drew BT, Smith TO, Littlewood C, et al. . Do structural changes (EG, collagen/matrix) explain the response to therapeutic exercises in tendinopathy: a systematic review. Br J Sports Med 2014;48:966–72. 10.1136/bjsports-2012-091285
    1. Patijn J. Reproducibility and validity studies of diagnostic procedures in manual/musculoskeletal medicine protocol formats, 2nd edition.. Journal of Orthopaedic Medicine 2002;24:58–70. 10.1080/1355297X.2002.11736340
    1. Boone D, Halligan S, Mallett S, et al. . Systematic review: bias in imaging studies—the effect of manipulating clinical context, recall bias and reporting intensity. Eur Radiol 2012;22:495–505. 10.1007/s00330-011-2294-0
    1. Sarris I, Ioannou C, Dighe M, et al. . Standardization of fetal ultrasound biometry measurements: improving the quality and consistency of measurements. Ultrasound Obstet Gynecol 2011;38:681–7. 10.1002/uog.8997
    1. Tudorache S, Cara M, Iliescu DG, et al. . First trimester two- and four-dimensional cardiac scan: intra- and interobserver agreement, comparison between methods and benefits of color Doppler technique. Ultrasound Obstet Gynecol 2013;42:659–68. 10.1002/uog.12459
    1. Chen W, Lou EHM, Zhang PQ, et al. . Reliability of assessing the coronal curvature of children with scoliosis by using ultrasound images. J Child Orthop 2013;7:521–9. 10.1007/s11832-013-0539-y
    1. Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977;33:159–74. 10.2307/2529310
    1. Lowry R. VassarStats: website for statistical computation. New York, USA: Vassar College, 2019.
    1. Lexell JE, Downham DY. How to assess the reliability of measurements in rehabilitation. Am J Phys Med Rehabil 2005;84:719–23. 10.1097/01.phm.0000176452.17771.20
    1. Del Baño-Aledo ME, Martínez-Payá JJ, Ríos-Díaz J, et al. . Ultrasound measures of tendon thickness: intra-rater, inter-rater and inter-machine reliability. Muscles Ligaments Tendons J 2017;7:192–9. 10.11138/mltj/2017.7.1.192
    1. Poltawski L, Ali S, Jayaram V, et al. . Reliability of sonographic assessment of tendinopathy in tennis elbow. Skeletal Radiol 2012;41:83–9. 10.1007/s00256-011-1132-4
    1. Gellhorn AC, Carlson MJ. Inter-rater, intra-rater, and inter-machine reliability of quantitative ultrasound measurements of the patellar tendon. Ultrasound Med Biol 2013;39:791–6. 10.1016/j.ultrasmedbio.2012.12.001
    1. Mc Auliffe S, Mc Creesh K, Purtill H, et al. . A systematic review of the reliability of diagnostic ultrasound imaging in measuring tendon size: is the error clinically acceptable? Phys Ther Sport 2017;26:52–63. 10.1016/j.ptsp.2016.12.002
    1. Archambault JM, Wiley JP, Bray RC, et al. . Can sonography predict the outcome in patients with achillodynia? J Clin Ultrasound 1998;26:335–9. 10.1002/(SICI)1097-0096(199809)26:7<335::AID-JCU1>;2-A
    1. Boesen AP, Boesen MI, Torp-Pedersen S, et al. . Associations between abnormal ultrasound color Doppler measures and tendon pain symptoms in badminton players during a season: a prospective cohort study. Am J Sports Med 2012;40:548–55. 10.1177/0363546511435478
    1. Comin J, Cook JL, Malliaras P, et al. . The prevalence and clinical significance of sonographic tendon abnormalities in asymptomatic ballet dancers: a 24-month longitudinal study. Br J Sports Med 2013;47:89–92. 10.1136/bjsports-2012-091303
    1. Cook JL, Khan KM, Kiss ZS, et al. . Asymptomatic hypoechoic regions on patellar tendon ultrasound: a 4-year clinical and ultrasound follow-up of 46 tendons. Scand J Med Sci Sports 2001;11:321–7. 10.1034/j.1600-0838.2001.110602.x
    1. Cook JL, Khan KM, Kiss ZS, et al. . Prospective imaging study of asymptomatic patellar tendinopathy in elite junior basketball players. J Ultrasound Med 2000;19:473–9. 10.7863/jum.2000.19.7.473
    1. de Jonge S, de Vos RJ, Van Schie HTM, et al. . One-Year follow-up of a randomised controlled trial on added splinting to eccentric exercises in chronic midportion Achilles tendinopathy. Br J Sports Med 2010;44:673–7. 10.1136/bjsm.2008.052142
    1. Khan KM, Cook JL, Kiss ZS, et al. . Patellar tendon ultrasonography and jumper's knee in female basketball players: a longitudinal study. Clin J Sport Med 1997;7:199–206. 10.1097/00042752-199707000-00009
    1. van Schie HTM, de Vos RJ, de Jonge S, et al. . Ultrasonographic tissue characterisation of human Achilles tendons: quantification of tendon structure through a novel non-invasive approach. Br J Sports Med 2010;44:1153–9. 10.1136/bjsm.2009.061010
    1. Docking S, Rosengarten S, Daffy J, et al. . The role of ultrasound tissue characterisation in the management and prevention of tendinopathy in athletes. J Sci Med Sport 2013;16:e85–6. 10.1016/j.jsams.2013.10.206
    1. Docking S, Rio E, Cook J. When pictures tell more than a thousand words: the clinical role of imaging for tendinopathy and emergence of UTC. J Sci Med Sport 2013;16:e85 10.1016/j.jsams.2013.10.204
    1. Docking SI, Rosengarten SD, Cook J. Achilles tendon structure improves on UTC imaging over a 5-month pre-season in elite Australian football players. Scand J Med Sci Sports 2016;26:557–63. 10.1111/sms.12469
    1. Docking SI, Cook J. Pathological tendons maintain sufficient aligned fibrillar structure on ultrasound tissue characterization (UTC). Scand J Med Sci Sports 2016;26:675–83. 10.1111/sms.12491
    1. Docking S, Bedi H, Jowett C, et al. . Improvement in pain and function is not mediated by changes in tissue structure following surgery for Achilles tendinopathy. J Sci Med Sport 2015;19:e100 10.1016/j.jsams.2015.12.371
    1. Mapes-Gonnella T. The impact of education. J Diagn Med Sonog 2013;29:260–8. 10.1177/8756479313504148
    1. Naredo E, Möller I, Moragues C, et al. . Interobserver reliability in musculoskeletal ultrasonography: results from a "Teach the Teachers" rheumatologist course. Ann Rheum Dis 2006;65:14–9. 10.1136/ard.2005.037382
    1. Brage K, Hjarbaek J, Kjaer P, et al. . Ultrasonic strain elastography for detecting abnormalities in the supraspinatus tendon: an intra- and inter-rater reliability study. BMJ Open 2019;9:e027725. 10.1136/bmjopen-2018-027725

Source: PubMed

Sponsorzy i współpracownicy

Warunki medyczne

Interwencje lekowe

3
Subskrybuj