Strain Elastography and Tendon Response to an Exercise Program in Patients With Supraspinatus Tendinopathy: An Exploratory Study

Karen Brage, Birgit Juul-Kristensen, John Hjarbaek, Eleanor Boyle, Per Kjaer, Kim Gordon Ingwersen, Karen Brage, Birgit Juul-Kristensen, John Hjarbaek, Eleanor Boyle, Per Kjaer, Kim Gordon Ingwersen

Abstract

Background: Shoulder pain is common, with a lifetime prevalence of up to 67%. Evidence is conflicting in relation to imaging findings and pain in the shoulder. Sonoelastography can be used to estimate tissue stiffness and may be a clinically relevant technique for diagnosing and monitoring tendon healing.

Purpose: To evaluate changes in supraspinatus tendon stiffness using strain elastography (SEL) and associations with changes in patient-reported outcomes, supraspinatus tendon thickness, and grade of tendinopathy after 12 weeks of unilateral shoulder exercises in patients with supraspinatus tendinopathy.

Study design: Controlled laboratory study.

Methods: A total of 23 patients with unilateral clinical supraspinatus tendinopathy performed 12 weeks of "standard care" exercises. At baseline and follow-up, supraspinatus tendon stiffness was measured bilaterally using SEL and compared with tendinopathy grading on magnetic resonance imaging scans and tendon thickness measured using conventional ultrasound. Patient-reported outcome measures included physical function and symptoms from the Disabilities of the Arm, Shoulder and Hand questionnaire and pain rating (visual analog scale).

Results: No significant changes in SEL within or between groups (asymptomatic vs symptomatic tendon) were seen. All patient-reported outcomes showed significant improvement from baseline to follow-up, but with no change in tendinopathy grading and tendon thickness. No significant differences in the proportion of patients changing above the minimal detectable change in SEL and PROM were seen, except for discomfort while sleeping.

Conclusion: Despite no significant within-group or between-group changes in SEL, significant improvements were found in patient-reported outcomes. An acceptable agreement between patients changing above the minimal detectable change in SEL and patient-reported outcome measure was seen. Further studies should explore the use of SEL to detect changes after tendon repair and long-term training potentially in subgroups of different tendinopathy phases.

Clinical relevance: In the short term, structural changes in supraspinatus tendons could not be visualized using SEL, indicating that a longer time span should be expected in order to observe structural changes, which should be considered before return to sports. Subgrouping based on stage of tendinopathy may also be important in order to evaluate changes over time with SEL among patients with supraspinatus tendinopathy.

Registration: NCT03425357 (ClinicalTrials.gov identifier).

Keywords: rotator cuff; strain elastography; supraspinatus tendon; tendinopathy; tendon change; training; ultrasound.

Conflict of interest statement

One or more of the authors has declared the following potential conflict of interest or source of funding: This study was funded by the Region of South Denmark (Research Fund and PhD-Fund), the Danish Rheumatism Association, and the Danish Council of Radiographers. AOSSM checks author disclosures against the Open Payments Database (OPD). AOSSM has not conducted an independent investigation on the OPD and disclaims any liability or responsibility relating thereto.

© The Author(s) 2020.

Figures

Figure 1.
Figure 1.
Scatterplots of baseline values (x-axis) and changes (y-axis) in the (total) symptomatic and the asymptomatic supraspinatus tendons using raw elastography data (RAW) and the ratio with the deltoid muscle as reference (DELT). A larger baseline value and a positive change value indicate increasing tendon stiffness. The reference lines illustrate the upper and lower boundaries of the minimal detectable change (MDC).
Figure 2.
Figure 2.
Scatterplots of absolute change in (A-F) total SEL RAW and (G-L) total SEL DELT in relation to the absolute change in DASH, VAS rest, VAS activity, VAS sleep, VAS max, and tendon thickness. Corresponding minimal detectable change values are marked with horizontal and vertical lines. DASH, Disabilities of the Arm, Shoulder and Hand; DELT, deltoid muscle; RAW, raw elastography data; SEL, strain elastography; VAS, visual analog scale.
Appendix Figure A1.
Appendix Figure A1.
Scatterplots of baseline values (x-axis) and changes (y-axis) in the symptomatic (middle part of the tendon) and the asymptomatic supraspinatus tendons using raw elastography data (RAW) and the ratio with the deltoid muscle as reference (DELT). A larger baseline value and a positive change value indicate increasing tendon stiffness. The reference lines illustrate the upper and lower boundaries of the minimal detectable change (MDC).
Appendix Figure A2.
Appendix Figure A2.
Scatterplots of baseline values (x-axis) and changes (y-axis) in the symptomatic (worst part of tendon) and the asymptomatic supraspinatus tendons using raw elastography data (RAW) and the ratio with the deltoid muscle as reference (DELT). A larger baseline value and a positive change value indicate increasing tendon stiffness. The reference lines illustrate the upper and lower boundaries of the minimal detectable change (MDC).

References

    1. Alizadehkhaiyat O, Roebuck MM, Makki AT, Frostick SP. Pain, functional disability, psychological status, and health-related quality of life in patients with subacromial impingement syndrome. Cogent Med. 2017;4:1406631.
    1. Boonstra AM, Schiphorst Preuper HR, Reneman MF, Posthumus JB, Stewart RE. Reliability and validity of the visual analogue scale for disability in patients with chronic musculoskeletal pain. Int J Rehabil Res. 2008;31(2):165–169.
    1. Brage K, Hjarbaek J, Boyle E, Ingwersen KG, Kjaer P, Juul-Kristensen B. Discriminative and convergent validity of strain elastography for detecting tendinopathy within the supraspinatus tendon: a cross-sectional study. JSES Int. 2020;4(2):310–317.
    1. Brage K, Hjarbaek J, Kjaer P, Ingwersen KG, Juul-Kristensen B. Ultrasonic strain elastography for detecting abnormalities in the supraspinatus tendon: an intra- and inter-rater reliability study. BMJ Open. 2019;9(5):e027725.
    1. Busilacchi A, Olivieri M, Ulisse S, et al. Real-time sonoelastography as novel follow-up method in Achilles tendon surgery. Knee Surg Sports Traumatol Arthrosc. 2016;24(7):2124–2132.
    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(6):409–416.
    1. Danish Health Authority. National clinical guidelines for diagnoses and treatment of patients with selected shoulder impairments. Danish Health Authority; 2013.
    1. De Zordo T, Fink C, Feuchtner GM, Smekal V, Reindl M, Klauser AS. Real-time sonoelastography findings in healthy Achilles tendons. AJR Am J Roentgenol. 2009;193(2):W134–W138.
    1. Dietrich CF, Barr RG, Farrokh A, et al. Strain elastography—how to do it? Ultrasound Int Open. 2017;3(4):e137–e149.
    1. Docheva D, Muller SA, Majewski M, Evans CH. Biologics for tendon repair. Adv Drug Deliv Rev. 2015;84:222–239.
    1. Franchignoni F, Vercelli S, Giordano A, Sartorio F, Bravini E, Ferriero G. Minimal clinically important difference of the Disabilities of the Arm, Shoulder and Hand Outcome measure (DASH) and its shortened version (QuickDASH). J Orthop Sports Phys Ther. 2014;44(1):30–39.
    1. Garra BS. Elastography: history, principles, and technique comparison. Abdom Imaging. 2015;40(4):680–697.
    1. Hawkins RJ, Kennedy JC. Impingement syndrome in athletes. Am J Sports Med. 1980;8(3):151–158.
    1. Hougs Kjaer BPM, Ellegaard KPP, Wieland IP, Warming SPP, Juul-Kristensen BPP. Intra-rater and inter-rater reliability of the standardized ultrasound protocol for assessing subacromial structures. Physiother Theory Pract. 2017;33(5):398–409.
    1. Ingwersen KG, Christensen R, Sørensen L, et al. Progressive high-load strength training compared with general low-load exercises in patients with rotator cuff tendinopathy. Trials. 2015;16(1):27.
    1. Ingwersen KG, Hjarbæk J, Eshøj H, Larsen CM, Vobbe JW, Juul-Kristensen B. Ultrasound assessment for grading structural tendon changes in supraspinatus tendinopathy: an inter-rater reliability study. BMJ Open. 2016;6(5):e011746.
    1. Ingwersen KG, Jensen SL, Sorensen L, et al. Three months of progressive high-load versus traditional low-load strength training among patients with rotator cuff tendinopathy: primary results from the double-blind randomized controlled RoCTEx trial. Orthop J Sports Med. 2017;5(8):2325967117723292.
    1. Jobe FW, Jobe CM. Painful athletic injuries of the shoulder. Clin Orthop Relat Res. 1983(173):117–124.
    1. Kamper SJ, Maher CG, Mackay G. Global rating of change scales: a review of strengths and weaknesses and considerations for design. J Man Manip Ther. 2009;17(3):163–170.
    1. Kelly BT, Kadrmas WR, Speer KP. The manual muscle examination for rotator cuff strength: an electromyographic investigation. Am J Sports Med. 1996;24(5):581–588.
    1. Kelly SM, Brittle N, Allen GM. The value of physical tests for subacromial impingement syndrome: a study of diagnostic accuracy. Clin Rehabil. 2010;24(2):149–158.
    1. Kitis A, Celik E, Aslan UB, Zencir M. DASH questionnaire for the analysis of musculoskeletal symptoms in industry workers: a validity and reliability study. Appl Ergon. 2009;40(2):251–255.
    1. Kocyigit F, Kuyucu E, Kocyigit A, Herek DT, Savkin R, Aslan UB. Investigation of biomechanical characteristics of intact supraspinatus tendons in subacromial impingement syndrome: a cross-sectional study with real-time sonoelastography. Am J Phys Med Rehabil. 2016;95(8):588–596.
    1. Luime JJ, Koes BW, Hendriksen IJ, et al. Prevalence and incidence of shoulder pain in the general population: a systematic review. Scand J Rheumatol. 2004;33(2):73–81.
    1. Lundquist CB, Dossing K, Christiansen DH. Responsiveness of a Danish version of the Disabilities of the Arm, Shoulder and Hand (DASH) questionnaire. Dan Med J. 2014;61(4):A4813.
    1. Mersmann F, Bohm S, Arampatzis A. Imbalances in the development of muscle and tendon as risk factor for tendinopathies in youth athletes: a review of current evidence and concepts of prevention. Front Physiol. 2017;8:987.
    1. Neer CS II, Welsh RP. The shoulder in sports. Orthop Clin North Am. 1977;8(3):583–591.
    1. Nowicki A, Dobruch-Sobczak K. Introduction to ultrasound elastography. J Ultrasound. 2016;16(65):113–124.
    1. Olsen MF, Bjerre E, Hansen MD, Tendal B, Hilden J, Hrobjartsson A. Minimum clinically important differences in chronic pain vary considerably by baseline pain and methodological factors: systematic review of empirical studies. J Clin Epidemiol. 2018;101:87–106.e102.
    1. Prado-Costa R, Rebelo J, Monteiro-Barroso J, Preto AS. Ultrasound elastography: compression elastography and shear-wave elastography in the assessment of tendon injury. Insights Imaging. 2018;9(5):791–814.
    1. Sein ML, Walton J, Linklater J, et al. Reliability of MRI assessment of supraspinatus tendinopathy. Br J Sports Med. 2007;41(8):e9.
    1. Seo JB, Yoo JS, Ryu JW. Sonoelastography findings of supraspinatus tendon in rotator cuff tendinopathy without tear: comparison with magnetic resonance images and conventional ultrasonography. J Ultrasound. 2015;18(2):143–149.
    1. Sharma P, Maffulli N. Biology of tendon injury: healing, modeling and remodeling. J Musculoskelet Neuronal Interact. 2006;6(2):181–190.
    1. Stauffer ME, Taylor SD, Watson DJ, Peloso PM, Morrison A. Definition of nonresponse to analgesic treatment of arthritic pain: an analytical literature review of the smallest detectable difference, the minimal detectable change, and the minimal clinically important difference on the pain visual analog scale. Int J Inflam. 2011;2011:231926.
    1. Thomeé R. A comprehensive treatment approach for patellofemoral pain syndrome in young women. Phys Ther. 1997;77(12):1690–1703.
    1. Tran G, Cowling P, Smith T, et al. What imaging-detected pathologies are associated with shoulder symptoms and their persistence? A systematic literature review. Arthritis Care Res (Hoboken). 2018;70(8):1169–1184.
    1. van der Windt DA, Koes BW, de Jong BA, Bouter LM. Shoulder disorders in general practice: incidence, patient characteristics, and management. Ann Rheum Dis. 1995;54(12):959–964.
    1. von Elm E, Altman DG, Egger M, Pocock SJ, Gotzsche PC, Vandenbroucke JP. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Int J Surg. 2014;12(12):1495–1499.
    1. Zhang LN, Wan WB, Wang YX, et al. Evaluation of elastic stiffness in healing Achilles tendon after surgical repair of a tendon rupture using in vivo ultrasound shear wave elastography. Med Sci Monit. 2016;22:1186–1191.

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