Adaptation of Tendon Structure and Function in Tendinopathy With Exercise and Its Relationship to Clinical Outcome

in Journal of Sport Rehabilitation
Restricted access

Purchase article

USD $24.95

Student 1 year subscription

USD $74.00

1 year subscription

USD $99.00

Student 2 year subscription

USD $141.00

2 year subscription

USD $185.00

Context: Exercise is seen as the most evidence-based treatment for managing tendinopathy and although the type of exercise used to manage tendinopathy may induce adaptation in healthy tendons, it is not clear whether these adaptations occur in tendinopathy and if so whether they are associated with improved clinical outcomes. Objective: The aim of the study was to synthesize available evidence for adaptation of the Achilles tendon to eccentric exercise and the relationship between adaptation (change in tendon thickness) and clinical outcomes among people with Achilles tendinopathy. Evidence Acquisition: The search was performed in September 2018 in several databases. Studies investigating the response (clinical outcome and imaging on ultrasound/magnetic resonance imaging) of pathological tendons (tendinopathy, tendinosis, and partial rupture) to at least 12 weeks of eccentric exercise were included. Multiple studies that investigated the same interventions and outcome were pooled and presented in effect size estimates, mean difference, and 95% confidence intervals if measurement scales were the same, or standard mean difference and 95% confidence intervals if measurements scales were different. Where data could not be pooled the studies were qualitatively synthesized based on van Tulder et al. Evidence Synthesis: Eight studies met the inclusion and exclusion criteria and were included in the review. There was strong evidence that Achilles tendon thickness does not decrease in parallel with improved clinical outcomes. Conclusions: Whether a longer time to follow-up is more important than the intervention (ie, just the time per se) for a change in tendon thickness remains unknown. Future studies should investigate whether exercise (or other treatments) can be tailored to optimize tendon adaptation and function, and whether this relates to clinical outcomes.

Färnqvist is with Haninge Rehab, Handen, Sweden. Pearson is with the Centre for Health, Sport & Rehabilitation Sciences Research, University of Salford, Manchester, United Kingdom. Malliaras is with the Department of Physiotherapy, School of Primary Health Care, Faculty of Medicine, Nursing and Health Science, Monash University, Melbourne, VIC, Australia.

Färnqvist (k.farnqvist@gmail.com) is corresponding author.
Journal of Sport Rehabilitation
Article Sections
References
  • 1.

    Rio EMoseley LPurdam Cet al. The pain of tendinopathy: physiological or pathophysiological? Sports Med. 2014;44(1):923. PubMed ID: 24027089 doi:

  • 2.

    van Dijk CNvan Sterkenburg MNWiegerinck JIKarlsson JMaffulli N. Terminology for Achilles tendon related disorders. Knee Surg Sports Traumatol Arthrosc. 2011;19:835841. PubMed ID: 21222102 doi:

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3.

    Dean BJGettings PDakin SGCarr AJ. Are inflammatory cells increased in painful human tendinopathy? A systematic review. Br J Sports Med. 2016;50:216220. PubMed ID: 26246419 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Riley G. Chronic tendon pathology: molecular basis and therapeutic implications. Expert Rev Mol Med. 2005;7:125. PubMed ID: 15796783 doi:

  • 5.

    Giombini ADragoni SDi Cesare ADi Cesare MDel Buono AMaffulli N. Asymptomatic Achilles, patellar, and quadriceps tendinopathy: a longitudinal clinical and ultrasonographic study in elite fencers. Scand J Med Sci Sports. 2013;23:311316. PubMed ID: 22092963 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Miller BFOlesen JLHansen Met al. Coordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise. J Physiol. 2005;567:10211033. PubMed ID: 16002437 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Bohm SMersmann FArampatzis A. Human tendon adaptation in response to mechanical loading: a systematic review and meta-analysis of exercise intervention studies on healthy adults. Sports Med Open. 2015;1:7. PubMed ID: 27747846 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Scott ADocking SVicenzino Bet 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;47:536544. PubMed ID: 23584762 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Drew BTSmith TOLittlewood CSturrock B. Do structural changes (eg, collagen/matrix) explain the response to therapeutic exercises in tendinopathy: a systematic review. Br J Sports Med. 2014;48:966972. PubMed ID: 23118117 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Collinger JLGagnon DJacobson JImpink BGBoninger ML. Reliability of quantitative ultrasound measures of the biceps and supraspinatus tendons. Acad Radiol. 2009;16(11):14241432. PubMed ID: 19596592 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Rabello LMvan den Akker-Scheek IBrink MSMaas MDiercks RLZwerver J. Association between clinical and imaging outcomes after therapeutic loading exercise in patients diagnosed with Achilles or patellar tendinopathy at short- and long-term follow-up: a systematic review [published online ahead of print June 25 2018]. Clin J Sport Med.

    • Search Google Scholar
    • Export Citation
  • 12.

    Shalabi AMovin TKristoffersen-Wiberg MAspelin PSvensson L. Reliability in the assessment of tendon volume and intratendinous signal of the Achilles tendon on MRI: a methodological description. Knee Surg Sports Traumatol Arthrosc. 2005;13:492498. PubMed ID: 16170584 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Silbernagel KGShelley KPowell SVarrecchia S. Extended field of view ultrasound imaging to evaluate Achilles tendon length and thickness: a reliability and validity study. Muscles Ligaments Tendons J. 2016;6:104110. PubMed ID: 27331037 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Mc Auliffe SMc Creesh KPurtill HO’sullivan K. A systematic review of the reliability of diagnostic ultrasound imaging in measuring tendon size: is the error clinically acceptable? Phys Ther Sport. 2017;26:5263. PubMed ID: 28162938 doi:

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    von Wehren LBlanke FTodorov AHeisterbach PSailer JMajewski M. The effect of subacromial injections of autologous conditioned plasma versus cortisone for the treatment of symptomatic partial rotator cuff tears. Knee Surg Sports Traumatol Arthrosc. 2016;24(12):37873792. PubMed ID: 26017742 doi:

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16.

    Bosch GLin YLvan Schie HTvan De Lest CHBarneveld Avan Weeren PR. Effect of extracorporeal shock wave therapy on the biochemical composition and metabolic activity of tenocytes in normal tendinous structures in ponies. Equine Vet J. 2007;39(3):226231. PubMed ID: 17520973 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Bosch Gde Mos Mvan Binsbergen Rvan Schie HTvan de Lest CHvan Weeren PR. The effect of focused extracorporeal shock wave therapy on collagen matrix and gene expression in normal tendons and ligaments. Equine Vet J. 2009;41(4):335341. PubMed ID: 19562893 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Langberg HEllingsgaard HMadsen Tet al. Eccentric rehabilitation exercise increases peritendinous type I collagen synthesis in humans with Achilles tendinosis. Scand J Med Sci Sports. 2007;17:6166. PubMed ID: 16787448

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Magnusson SPLangberg HKjaer M. The pathogenesis of tendinopathy: balancing the response to loading. Nat Rev Rheumatol. 2010;6:262268. PubMed ID: 20308995 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Liberati AAltman DGTetzlaff Jet al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ. 2009;339:2700. PubMed ID: 19622552 doi:

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21.

    de Morton NA. The PEDro scale is a valid measure of the methodological quality of clinical trials: a demographic study. Aust J Physiother. 2009;55:129133. PubMed ID: 19463084 doi:

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22.

    Maher CGSherrington CHerbert RDMoseley AMElkins M. Reliability of the PEDro scale for rating quality of randomized controlled trials. Phys Ther. 2003;83(8):713721. PubMed ID: 12882612

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Deeks JJHiggins JPTAltman DG eds. Chapter 9: Analysing data and undertaking meta-analyses. In: Higgins JPTGreen S eds. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 (updated March 2011). The Cochrane Collaboration; 2011. Retrieved from www.cochrane-handbook.org

    • Search Google Scholar
    • Export Citation
  • 24.

    van Tulder MFurlan ABombardier CBouter L. Editorial board of the cochrane collaboration back review G. Updated method guidelines for systematic reviews in the Cochrane collaboration back review group. Spine. 2003;28:12901299.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25.

    Littlewood CMay SWalters S. Epidemiology of rotator cuff tendinopathy: a systematic review. Shoulder & Elbow. 2013;5(4):256265.

  • 26.

    Mallows ADebenham JWalker TLittlewood C. Association of psychological variables and outcome in tendinopathy: a systematic review. Br J Sports Med. 2017;51(9):743748. PubMed ID: 27852585 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Docking SIOoi CCConnell D. Tendinopathy: is imaging telling us the entire story? J Orthop Sports Phys Ther. 2015;45(11):842852. PubMed ID: 26390270 doi:

  • 28.

    Cohen J. Statistical Power Analysis for the Behavioral Sciences. 2nd ed. Hillsdale, NJ: Lawrence Erlbaum Associates; 1988.

  • 29.

    Gardin AMovin TSvensson LShalabi A. The long-term clinical and MRI results following eccentric calf muscle training in chronic Achilles tendinosis. Skeletal Radiol. 2010;39:435442. PubMed ID: 19774375 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Shalabi AKristoffersen-Wilberg MSvensson LAspelin PMovin T. Eccentric training of the gastrocnemius-soleus complex in chronic Achilles tendinopathy results in decreased tendon volume and intratendinous signal as evaluated by MRI. Am J Sports Med. 2004;32:12861296. PubMed ID: 15262655 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Beyer RKongsgaard MHougs Kjaer BOhlenschlaeger TKjaer MMagnusson SP. Heavy slow resistance versus eccentric training as treatment for Achilles tendinopathy: a randomized controlled trial. Am J Sports Med. 2015;43:17041711. PubMed ID: 26018970 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Norregaard JLarsen CCBieler TLangberg H. Eccentric exercise in treatment of Achilles tendinopathy. Scand J Med Sci Sports. 2007;17:133138. PubMed ID: 17394474

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Petersen WWelp RRosenbaum D. Chronic Achilles tendinopathy: a prospective randomized study comparing the therapeutic effect of eccentric training, the AirHeel brace, and a combination of both. Am J Sports Med. 2007;35:16591667. PubMed ID: 17569792 doi:

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34.

    Rompe JDNafe BFuria JPMaffulli N. Eccentric loading, shock-wave treatment, or a wait-and-see policy for tendinopathy of the main body of tendo Achillis: a randomized controlled trial. Am J Sports Med. 2007;35:374383. PubMed ID: 17244902 doi:

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35.

    Richards PJMcCall IWDay CBelcher JMaffulli N. Longitudinal microvascularity in Achilles tendinopathy (power Doppler ultrasound, magnetic resonance imaging time-intensity curves and the Victorian Institute of Sport Assessment-Achilles questionnaire): a pilot study. Skeletal Radiol. 2010;39(6):509521. PubMed ID: 19711073 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Tsehaie JPoot DHJOei EHGVerhaar JANde Vos RJ. Value of quantitative MRI parameters in predicting and evaluating clinical outcome in conservatively treated patients with chronic midportion Achilles tendinopathy: a prospective study. J Sci Med Sport. 2017;20:633637. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Kongsgaard MKovanen VAagaard Pet al. Corticosteroid injections, eccentric decline squat training and heavy slow resistance training in patellar tendinopathy. Scand J Med Sci Sports. 2009;19:790802. PubMed ID: 19793213 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Malliaras PBarton CJReeves NDLangberg H. Achilles and patellar tendinopathy loading programmes: a systematic review comparing clinical outcomes and identifying potential mechanisms for effectiveness. Sports Med. 2013;43(4):267286. PubMed ID: 23494258 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Kongsgaard MQvortrup KLarsen Jet al. Fibril morphology and tendon mechanical properties in patellar tendinopathy: effects of heavy slow resistance training. Am J Sports Med. 2010;38:749756. PubMed ID: 20154324 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    Heinemeier MLorentzen MPJensen Jet al. Local trauma in human patellar tendon leads to widespread changes in the tendon gene expression. J Appl Physiol. 2016;120:10001010. PubMed ID: 26769953 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Corps ANRobinson AHMovin TCosta MLHazleman BLRiley GP. Increased expression of aggrecan and biglycan mRNA in Achilles tendinopathy. Rheumatology. 2006;45:291294. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42.

    Docking SIRosengarten SDCook 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;26:557563. PubMed ID: 25943892 doi:

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 43.

    Hansen LKrogh TPEllingsen TBolvig LFredberg U. Long-term prognosis of plantar fasciitis: a 5- to 15-year follow-up study of 174 patients with ultrasound examination. Orthop J Sports Med. 2018;6(3):2325967118757983. PubMed ID: 29536022 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44.

    Horstmann TJud HMFrohlich VMundermann AGrau S. Whole-body vibration versus eccentric training or a wait-and-see approach for chronic Achilles tendinopathy: a randomized clinical trial. J Orthop Sports Phys Ther. 2013;43:794803. PubMed ID: 24175595 doi:

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 45.

    Cook JLPurdam CR. Is tendon pathology a continuum? A pathology model to explain the clinical presentation of load-induced tendinopathy. Br J Sports Med. 2009;43:409416. PubMed ID: 18812414 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46.

    Malliaras PCook J. Changes in anteroposterior patellar tendon diameter support a continuum of pathological changes. Br J Sports Med. 2011;45:10481051. PubMed ID: 21540193 doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47.

    Balius RAlvarez GBaro Fet al. A 3-arm randomized trial for Achilles tendinopathy: eccentric training, eccentric training plus a dietary supplement containing mucopolysaccharides, or passive stretching plus a dietary supplement containing mucopolysaccharides. Curr Ther Res Clin Exp. 2016;78:17. PubMed ID: 28053674 doi:

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 48.

    Begg CBPilote L. A model for incorporating historical controls in into a meta-analysis. Biometrics. 1991;47(3):899906. PubMed ID: 1742445 doi:

Article Metrics
All Time Past Year Past 30 Days
Abstract Views 705 705 162
Full Text Views 126 126 47
PDF Downloads 57 57 15
Altmetric Badge
PubMed
Google Scholar