Abstract
The glenohumeral joint is a complex anatomic structure commonly affected by injury such as tendinopathy and rotator cuff tears. This review presents an up-to-date overview of research on tendon biology and structure, shoulder joint motion and stability, tendon healing, and current and potential future repair strategies. Recent studies have provided information demonstrating the serious impact on uninjured tissues after a rotator cuff tear or other cause of altered shoulder joint mechanics. Another major focus of recent research is biological augmentation of rotator cuff repair with the goal of successfully reinstating normal tendon-to-bone structure. To effectively treat shoulder pathologies, clinicians need to understand normal tendon biology, the healing process and environment, and whole shoulder stability and function.
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Llusa M, Meri A, Ruano D. Surgical atlas of the musculoskeletal system. Rosemont, Ill.: American Academy of Orthopaedic Surgeons. 2008.
Setton LA, Elliott DM, Mow VC. Altered mechanics of cartilage with osteoarthritis: human osteoarthritis and an experimental model of joint degeneration. Osteoarthr Cartil. 1999;7:2–14.
Mehta S, Gimbel JA, Soslowsky LJ. Etiologic and pathogenetic factors for rotator cuff tendinopathy. Clin Sports Med. 2003;22:791–812.
De Maeseneer M, Van Roy P, Shahabpour M. Normal MR imaging anatomy of the rotator cuff tendons, glenoid fossa, labrum, and ligaments of the shoulder. Radiol Clin North Am. 2006;44:479–87. vii.
Clark JM, Harryman 2nd DT. Tendons, ligaments, and capsule of the rotator cuff. Gross and microscopic anatomy. J Bone Joint Surg Am. 1992;74:713–25.
Curtis AS, Burbank KM, Tierney JJ, Scheller AD, Curran AR. The insertional footprint of the rotator cuff: an anatomic study. Arthroscopy. 2006;22:609.e1.
Thomopoulos S, Williams GR, Gimbel JA, Favata M, Soslowsky LJ. Variation of biomechanical, structural, and compositional properties along the tendon to bone insertion site. J Orthop Res. 2003;21:413–9.
Soslowsky LJ, Carpenter JE, Bucchieri JS, Flatow EL. Biomechanics of the rotator cuff. Orthop Clin North Am. 1997;28:17–30.
Gautieri A, Vesentini S, Redaelli A, Buehler MJ. Hierarchical structure and nanomechanics of collagen microfibrils from the atomistic scale up. Nano Lett. 2011;11:757–66.
Lake SP, Miller KS, Elliott DM, Soslowsky LJ. Effect of fiber distribution and realignment on the nonlinear and inhomogeneous mechanical properties of human supraspinatus tendon under longitudinal tensile loading. J Orthop Res. 2009;27:1596–602.
Miller KS, Edelstein L, Connizzo BK, Soslowsky LJ. Effect of preconditioning and stress relaxation on local collagen fiber re-alignment: inhomogeneous properties of rat supraspinatus tendon. J Biomech Eng. 2012;134:031007.
Matsuhashi T, Hooke AW, Zhao KD, Goto A, Sperling JW, Steinmann SP, et al. Tensile properties of a morphologically split supraspinatus tendon. Clin Anat. 2014;27:702–6.
Bigliani LU, Pollock RG, Soslowsky LJ, Flatow EL, Pawluk RJ, Mow VC. Tensile properties of the inferior glenohumeral ligament. J Orthop Res. 1992;10:187–97.
Moore SM, Ellis B, Weiss JA, McMahon PJ, Debski RE. The glenohumeral capsule should be evaluated as a sheet of fibrous tissue: a validated finite element model. Ann Biomed Eng. 2010;38:66–76.
Bahk M, Keyurapan E, Tasaki A, Sauers EL, McFarland EG. Laxity testing of the shoulder: a review. Am J Sports Med. 2007;35:131–44.
Halder AM, Kuhl SG, Zobitz ME, Larson D, An KN. Effects of the glenoid labrum and glenohumeral abduction on stability of the shoulder joint through concavity-compression: an in vitro study. J Bone Joint Surg Am. 2001;83-A:1062–9.
Turkel SJ, Panio MW, Marshall JL, Girgis FG. Stabilizing mechanisms preventing anterior dislocation of the glenohumeral joint. J Bone Joint Surg Am. 1981;63:1208–17.
Malicky DM, Soslowsky LJ, Blasier RB, Shyr Y. Anterior glenohumeral stabilization factors: progressive effects in a biomechanical model. J Orthop Res. 1996;14:282–8.
Soslowsky LJ, Malicky DM, Blasier RB. Active and passive factors in inferior glenohumeral stabilization: a biomechanical model. J Shoulder Elbow Surg. 1997;6:371–9.
Blasier RB, Soslowsky LJ, Malicky DM, Palmer ML. Posterior glenohumeral subluxation: active and passive stabilization in a biomechanical model. J Bone Joint Surg Am. 1997;79:433–40.
Lee TQ, Black AD, Tibone JE, McMahon PJ. Release of the coracoacromial ligament can lead to glenohumeral laxity: a biomechanical study. J Shoulder Elbow Surg. 2001;10:68–72.
Abboud JA, Soslowsky LJ. Interplay of the static and dynamic restraints in glenohumeral instability. Clin Orthop Relat Res. 2002;400:48–57.
Lugo R, Kung P, Ma CB. Shoulder biomechanics. Eur J Radiol. 2008;68:16–24.
Moor BK, Bouaicha S, Rothenfluh DA, Sukthankar A, Gerber C. Is there an association between the individual anatomy of the scapula and the development of rotator cuff tears or osteoarthritis of the glenohumeral joint?: A radiological study of the critical shoulder angle. Bone Joint J. 2013;95-B:935–41.
Thompson WO, Debski RE, Boardman 3rd ND, Taskiran E, Warner JJ, Fu FH, et al. A biomechanical analysis of rotator cuff deficiency in a cadaveric model. Am J Sports Med. 1996;24:286–92.
Parsons IM, Apreleva M, Fu FH, Woo SL. The effect of rotator cuff tears on reaction forces at the glenohumeral joint. J Orthop Res. 2002;20:439–46.
Maeda E, Fleischmann C, Mein CA, Shelton JC, Bader DL, Lee DA. Functional analysis of tenocytes gene expression in tendon fascicles subjected to cyclic tensile strain. Connect Tissue Res. 2010;51:434–44.
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.
Soslowsky LJ, Thomopoulos S, Tun S, Flanagan CL, Keefer CC, Mastaw J, et al. Neer Award 1999. Overuse activity injures the supraspinatus tendon in an animal model: a histologic and biomechanical study. J Shoulder Elbow Surg. 2000;9:79–84.
Archambault JM, Jelinsky SA, Lake SP, Hill AA, Glaser DL, Soslowsky LJ. Rat supraspinatus tendon expresses cartilage markers with overuse. J Orthop Res. 2007;25:617–24.
Attia M, Scott A, Duchesnay A, Carpentier G, Soslowsky LJ, Huynh MB, et al. Alterations of overused supraspinatus tendon: a possible role of glycosaminoglycans and HARP/pleiotrophin in early tendon pathology. J Orthop Res. 2012;30:61–71. In a rat model, GAG expression and accumulation after 4 weeks of overuse continues for up to 16 weeks and may sequester the HARP cytokine, influencing tenocyte phenotype.
Millar NL, Wei AQ, Molloy TJ, Bonar F, Murrell GA. Cytokines and apoptosis in supraspinatus tendinopathy. J Bone Joint Surg (Br). 2009;91:417–24.
Perry SM, McIlhenny SE, Hoffman MC, Soslowsky LJ. Inflammatory and angiogenic mRNA levels are altered in a supraspinatus tendon overuse animal model. J Shoulder Elbow Surg. 2005;14:79S–83.
de Castro PA, Ejnisman B, de Seixas Alves MT, Uyeda LF, Nouailhetas VL, Han SW, et al. Overuse of training increases mechanoreceptors in supraspinatus tendon of rats SHR. J Orthop Res. 2011;29:1771–4.
Maganaris CN, Narici MV, Almekinders LC, Maffulli N. Biomechanics and pathophysiology of overuse tendon injuries: ideas on insertional tendinopathy. Sports Med. 2004;34:1005–17.
Magnusson SP, Langberg H, Kjaer M. The pathogenesis of tendinopathy: balancing the response to loading. Nat Rev Rheumatol. 2010;6:262–8.
Neer 2nd CS. Anterior acromioplasty for the chronic impingement syndrome in the shoulder: a preliminary report. J Bone Joint Surg Am. 1972;54:41–50.
Evanko SP, Vogel KG. Proteoglycan synthesis in fetal tendon is differentially regulated by cyclic compression in vitro. Arch Biochem Biophys. 1993;307:153–64.
McFarland EG, Maffulli N, Del Buono A, Murrell GA, Garzon-Muvdi J, Petersen SA. Impingement is not impingement: the case for calling it “Rotator Cuff Disease”. Muscles Ligaments Tendons J. 2013;3:196–200.
Papadonikolakis A, McKenna M, Warme W, Martin BI, 3rd Matsen FA. Published evidence relevant to the diagnosis of impingement syndrome of the shoulder. J Bone Joint Surg Am. 2011;93:1827–32.
Shi LL, Edwards TB. The role of acromioplasty for management of rotator cuff problems: where is the evidence? Adv Orthop. 2012;2012:467571.
Fung DT, Wang VM, Andarawis-Puri N, Basta-Pljakic J, Li Y, Laudier DM, et al. Early response to tendon fatigue damage accumulation in a novel in vivo model. J Biomech. 2010;43:274–9.
Frisch KE, Marcu D, Baer GS, Thelen DG, Vanderby R. The influence of partial and full thickness tears on infraspinatus tendon strain patterns. J Biomech Eng. 2014;136:051004. Investigates tendon strain patterns after defect formation, determining that tendons are more sensitive to bursal defects and localized strain is induced directly next to partial thickness tears.
Oh JH, Jun BJ, McGarry MH, Lee TQ. Does a critical rotator cuff tear stage exist?: a biomechanical study of rotator cuff tear progression in human cadaver shoulders. J Bone Joint Surg Am. 2011;93:2100–9.
Mesiha MM, Derwin KA, Sibole SC, Erdemir A, McCarron JA. The biomechanical relevance of anterior rotator cuff cable tears in a cadaveric shoulder model. J Bone Joint Surg Am. 2013;95:1817–24.
Hsu JE, Reuther KE, Sarver JJ, Lee CS, Thomas SJ, Glaser DL, et al. Restoration of anterior-posterior rotator cuff force balance improves shoulder function in a rat model of chronic massive tears. J Orthop Res. 2011;29:1028–33.
Hwang E, Carpenter JE, Hughes RE, Palmer ML. Shoulder labral pathomechanics with rotator cuff tears. J Biomech. 2014;47:1733–8.
Reuther KE, Sarver JJ, Schultz SM, Lee CS, Sehgal CM, Glaser DL, et al. Glenoid cartilage mechanical properties decrease after rotator cuff tears in a rat model. J Orthop Res. 2012;30:1435–9. Demonstrates changes in articular cartilage of the glenoid after rotator cuff tear in a rat model.
Reuther KE, Thomas SJ, Evans EF, Tucker JJ, Sarver JJ, Ilkhani-Pour S, et al. Returning to overuse activity following a supraspinatus and infraspinatus tear leads to joint damage in a rat model. J Biomech. 2013;46:1818–24.
Kramer EJ, Bodendorfer BM, Laron D, Wong J, Kim HT, Liu X, et al. Evaluation of cartilage degeneration in a rat model of rotator cuff tear arthropathy. J Shoulder Elbow Surg. 2013;22:1702–9.
Reuther KE, Thomas SJ, Sarver JJ, Tucker JJ, Lee CS, Gray CF, et al. Effect of return to overuse activity following an isolated supraspinatus tendon tear on adjacent intact tendons and glenoid cartilage in a rat model. J Orthop Res. 2013;31:710–5.
Reuther KE, Thomas SJ, Tucker JJ, Sarver JJ, Gray CF, Rooney SI, et al. Disruption of the anterior-posterior rotator cuff force balance alters joint function and leads to joint damage in a rat model. J Orthop Res. 2014;32:638–44. This study brings to light the damaging effects of shoulder instability after rotator cuff tears.
Ditsios K, Boutsiadis A, Kapoukranidou D, Chatzisotiriou A, Kalpidis I, Albani M, et al. Chronic massive rotator cuff tear in rats: in vivo evaluation of muscle force and three-dimensional histologic analysis. J Shoulder Elbow Surg. 2014. A thorough review of biceps tendinopathy and treatment options, focusing on comorbidity of the rotator cuff. doi:10.1016/j.jse.2014.04.016
Sato EJ, Killian ML, Choi AJ, Lin E, Esparza MC, Galatz LM, et al. Skeletal muscle fibrosis and stiffness increase after rotator cuff tendon injury and neuromuscular compromise in a rat model. J Orthop Res. 2014;32:1111–6.
Kikukawa K, Ide J, Kikuchi K, Morita M, Mizuta H, Ogata H. Hypertrophic changes of the teres minor muscle in rotator cuff tears: quantitative evaluation by magnetic resonance imaging. J Shoulder Elbow Surg. 2014. doi:10.1016/j.jse.2014.03.014
Chen CH, Hsu KY, Chen WJ, Shih CH. Incidence and severity of biceps long head tendon lesion in patients with complete rotator cuff tears. J Trauma. 2005;58:1189–93.
Wu PT, Jou IM, Yang CC, Lin CJ, Yang CY, Su FC, et al. The severity of the long head biceps tendinopathy in patients with chronic rotator cuff tears: macroscopic versus microscopic results. J Shoulder Elbow Surg. 2014;23:1099–106.
Peltz CD, Perry SM, Getz CL, Soslowsky LJ. Mechanical properties of the long-head of the biceps tendon are altered in the presence of rotator cuff tears in a rat model. J Orthop Res. 2009;27:416–20.
Ditsios K, Agathangelidis F, Boutsiadis A, Karataglis D, Papadopoulos P. Long head of the biceps pathology combined with rotator cuff tears. Adv Orthop. 2012;2012:405472.
Giphart JE, Elser F, Dewing CB, Torry MR, Millett PJ. The long head of the biceps tendon has minimal effect on in vivo glenohumeral kinematics: a biplane fluoroscopy study. Am J Sports Med. 2012;40:202–12. Comparison of mechanics between tenodesed shoulders and healthy contralateral controls in five patients. No dramatic alterations in glenohumeral positioning during dynamic motion were seen, suggesting a low probability of long-term effects after such treatment.
Zhang Q, Zhou J, Ge H, Cheng B. Tenotomy or tenodesis for long head biceps lesions in shoulders with reparable rotator cuff tears: a prospective randomised trial. Knee Surg Sports Traumatol Arthrosc. 2013. Well-designed prospective trial on treatment of LH biceps lesions in conjunction with rotator cuff repair. doi:10.1007/s00167-013-2587-8
Thomas SJ, Reuther KE, Tucker JJ, Sarver JJ, Yannascoli SM, Caro AC, et al. Biceps detachment decreases joint damage in a rotator cuff tear rat model. Clin Orthop Relat Res. 2014;472:2404–12. Biceps tenotomy concurrent with rotator cuff tear improves joint function and decreases secondary joint damage compared to rotator cuff tear alone.
Ricchetti ET, Aurora A, Iannotti JP, Derwin KA. Scaffold devices for rotator cuff repair. J Shoulder Elbow Surg. 2012;21:251–65.
Bishop J, Klepps S, Lo IK, Bird J, Gladstone JN, Flatow EL. Cuff integrity after arthroscopic versus open rotator cuff repair: a prospective study. J Shoulder Elbow Surg. 2006;15:290–9.
Colvin AC, Egorova N, Harrison AK, Moskowitz A, Flatow EL. National trends in rotator cuff repair. J Bone Joint Surg Am. 2012;94:227–33.
Aleem AW, Brophy RH. Outcomes of rotator cuff surgery: what does the evidence tell us? Clin Sports Med. 2012;31:665–74.
Burkhart SS, Denard PJ, Konicek J, Hanypsiak BT. Biomechanical validation of load-sharing rip-stop fixation for the repair of tissue-deficient rotator cuff tears. Am J Sports Med. 2014;42:457–62.
Gartsman GM, Drake G, Edwards TB, Elkousy HA, Hammerman SM, O’Connor DP, et al. Ultrasound evaluation of arthroscopic full-thickness supraspinatus rotator cuff repair: single-row versus double-row suture bridge (transosseous equivalent) fixation. Results of a prospective, randomized study. J Shoulder Elbow Surg. 2013;22:1480–7.
McCormick F, Gupta A, Bruce B, Harris J, Abrams G, Wilson H, et al. Single-row, double-row, and transosseous equivalent techniques for isolated supraspinatus tendon tears with minimal atrophy: a retrospective comparative outcome and radiographic analysis at minimum 2-year follow up. Int J Shoulder Surg. 2014;8:15–20.
Peltz CD, Sarver JJ, Dourte LM, Wurgler-Hauri CC, Williams GR, Soslowsky LJ. Exercise following a short immobilization period is detrimental to tendon properties and joint mechanics in a rat rotator cuff injury model. J Orthop Res. 2010;28:841–5.
Lafosse L, Lanz U, Saintmard B, Campens C. Arthroscopic repair of subscapularis tear: surgical technique and results. Orthop Traumatol Surg Res. 2010;96:S99–108.
Edwards SL, Lynch TS, Saltzman MD, Terry MA, Nuber GW. Biologic and pharmacologic augmentation of rotator cuff repairs. J Am Acad Orthop Surg. 2011;19:583–9. Reviews recent approaches taken to augment the healing response after surgical repair of a torn rotator cuff.
Edelstein L, Thomas SJ, Soslowsky LJ. Rotator cuff tears: what have we learned from animal models? J Musculoskelet Neuronal Interact. 2011;11:150–62.
Gimbel JA, Van Kleunen JP, Mehta S, Perry SM, Williams GR, Soslowsky LJ. Supraspinatus tendon organizational and mechanical properties in a chronic rotator cuff tear animal model. J Biomech. 2004;37:739–49.
Mall NA, Tanaka MJ, Choi LS, Paletta Jr GA. Factors affecting rotator cuff healing. J Bone Joint Surg Am. 2014;96:778–88. Thorough review of surgical techniques, rehab protocols, and patient-specific factors influencing outcomes of rotator cuff repair.
Ilkhani-Pour S, Dunkman A, Solsowsky L. The basic science of rotator cuff tendons and healing. In: Nicholson GP, editor. Orthopaedic knowledge update: shoulder and elbow. 4th ed. Rosemont: American Academy of Orthopaedic Surgeons; 2013. p. 13–29.
Hoppe S, Alini M, Benneker LM, Milz S, Boileau P, Zumstein MA. Tenocytes of chronic rotator cuff tendon tears can be stimulated by platelet-released growth factors. J Shoulder Elbow Surg. 2013;22:340–9. Tendon cells taken from patients with chronic rotator cuff tears have inherently low proliferative capacity and collagen production. Supplementing media with 10% PRGFs substantially increased cell proliferation (>fourfold) and extracellular matrix expression (>10,000-fold).
Galatz LM, Sandell LJ, Rothermich SY, Das R, Mastny A, Havlioglu N, et al. Characteristics of the rat supraspinatus tendon during tendon-to-bone healing after acute injury. J Orthop Res. 2006;24:541–50.
Kovacevic D, Fox AJ, Bedi A, Ying L, Deng XH, Warren RF, et al. Calcium-phosphate matrix with or without TGF-beta3 improves tendon-bone healing after rotator cuff repair. Am J Sports Med. 2011;39:811–9.
Mazzocca AD, McCarthy MB, Chowaniec D, Cote MP, Judson CH, Apostolakos J, et al. Bone marrow-derived mesenchymal stem cells obtained during arthroscopic rotator cuff repair surgery show potential for tendon cell differentiation after treatment with insulin. Arthroscopy. 2011;27:1459–71.
Wong I, Burns J, Snyder S. Arthroscopic GraftJacket repair of rotator cuff tears. J Shoulder Elbow Surg. 2010;19:104–9.
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Julianne Huegel and Alexis A. Williams declare that they have no conflict of interest.
Louis J. Soslowsky declares the receipt of grants from DJO, Orthofix, and Amniox, outside of the submitted work.
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Huegel, J., Williams, A.A. & Soslowsky, L.J. Rotator Cuff Biology and Biomechanics: a Review of Normal and Pathological Conditions. Curr Rheumatol Rep 17, 476 (2015). https://doi.org/10.1007/s11926-014-0476-x
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DOI: https://doi.org/10.1007/s11926-014-0476-x