Skip to main content
SpringerLink
Log in

Biology of Rotator Cuff Injury and Repair

  • Chapter
  • First Online:
Book cover Massive and Irreparable Rotator Cuff Tears

  • 958 Accesses

Abstract

The glenohumeral joint is a complex anatomical structure commonly affected by injury such as tendinopathy and rotator cuff tears. Despite advances in surgical reconstruction of chronic rotator cuff tears, failure rates are still quite high. Significant research efforts have been focused on a better understanding of normal tendon biology, its pathological changes, the healing process and environment, and the whole shoulder stability and function. Rotator cuff injury has indeed a multifactorial pathogenesis, which includes anatomical, mechanical, and biological factors. Many theories have been postulated to explain this pathogenesis, trying to unify intrinsic and extrinsic theories. The precise role of each factor is not fully understood yet, although recent evidence strongly suggests that most of the tendinopathies and tendon ruptures are caused by primary failed healing response. The goals of tendon repair are to restore its force transmission function and recreate the relationships with the surrounding tissues, which allow the tendon to move smoothly. The success of tendon healing depends on the activation of cellular elements able to synthesize a new extracellular matrix and to remodel it with structural properties suitable for sustaining tensile loads. This chapter intends to give an overview on tendon histology and structure, shoulder joint motion and stability, causes of injury and mechanisms of tendon healing, including the possible pitfalls in this process.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 79.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 99.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 139.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Józsa L, Kannus P. Histopathological findings in spontaneous tendon ruptures. Scand J Med Sci Sports. 1997;7(2):113–8.

    Article  PubMed  Google Scholar 

  2. Kastelic J, Galeski A, Baer E. The multicomposite structure of tendon. Connect Tissue Res. 1978;6(1):11–23.

    Article  CAS  PubMed  Google Scholar 

  3. Kannus P. Etiology and pathophysiology of chronic tendon disorders in sports. Scand J Med Sci Sports. April 1997;7(2):78–85.

    Article  CAS  PubMed  Google Scholar 

  4. Aström M, Rausing A. Chronic Achilles tendinopathy. A survey of surgical and histopathologic findings. Clin Orthop. 1995;316:151–64.

    Article  Google Scholar 

  5. Kvist M, Józsa L, Järvinen M, Kvist H. Fine structural alterations in chronic Achilles paratenonitis in athletes. Pathol Res Pract. 1985;180(4):416–23.

    Article  CAS  PubMed  Google Scholar 

  6. Kannus P. Structure of the tendon connective tissue. Scand. J Med Sci Sports. 2000;10(6):312–20.

    Article  CAS  Google Scholar 

  7. Bank RA, Robins SP, Wijmenga C, Breslau-Siderius LJ, Bardoel AF, van der Sluijs HA. Defective collagen crosslinking in bone, but not in ligament or cartilage, in Bruck syndrome: indications for a bone-specific telopeptide lysyl hydroxylase on chromosome 17. Proc Natl Acad Sci U S A. 1999;96(3):1054–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Riley GP, Harrall RL, Cawston TE, Hazleman BL, Mackie EJ. Tenascin-C and human tendon degeneration. Am J Pathol. 1996;149(3):933–43.

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Perez-Castro AV, Vogel KG. In situ expression of collagen and proteoglycan genes during development of fibrocartilage in bovine deep flexor tendon. J Orthop Res. 1999;17(1):139–48.

    Article  CAS  PubMed  Google Scholar 

  10. Spindler KP, Andrish JT, Miller RR, Tsujimoto K, Diz DI. Distribution of cellular repopulation and collagen synthesis in a canine anterior cruciate ligament autograft. J Orthop Res. 1996;14(3):384–9.

    Article  CAS  PubMed  Google Scholar 

  11. Cawston TE, Curry VA, Summers CA, Clark IM, Riley GP, Life PF. The role of oncostatin M in animal and human connective tissue collagen turnover and its localization within the rheumatoid joint. Arthritis Rheum. 1998;41(10):1760–71.

    Article  CAS  PubMed  Google Scholar 

  12. Murphy G, Willenbrock F. Tissue inhibitors of matrix metalloendopeptidases. Methods Enzymol. 1995;248:496–510.

    Article  CAS  PubMed  Google Scholar 

  13. Millar AW, Brown PD, Moore J. Results of single and repeat dose studies of the oral matrix metalloproteinase inhibitor marimastat in healthy male volunteers. Br J Clin Pharmacol. 1998;45:21–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Cooper RR, Misol S. Tendon and ligament insertion. A light and electron microscopic study. J Bone Joint Surg Am. 1970;52(1):1–20.

    Article  CAS  PubMed  Google Scholar 

  15. Khan KM, Bonar F, Desmond PM, Cook JL, Young DA, Visentini PJ. Patellar tendinosis (jumper’s knee): findings at histopathologic examination, US, and MR imaging. Victorian Institute of Sport Tendon Study Group. Radiology. 1996;200(3):821–7.

    Article  CAS  PubMed  Google Scholar 

  16. Clark JM, Harryman DT. Tendons, ligaments, and capsule of the rotator cuff. Gross and microscopic anatomy. J Bone Joint Surg Am. 1992;74(5):713–25.

    Article  CAS  PubMed  Google Scholar 

  17. Lapiere CM, Nusgens B, Pierard GE. Interaction between collagen type I and type III in conditioning bundles organization. Connect Tissue Res. 1977;5(1):21–9.

    Article  CAS  PubMed  Google Scholar 

  18. Bailey AJ. Tissue and species specificity in the crosslinking of collagen. Pathol Biol. 1974;22(8):675–80.

    CAS  PubMed  Google Scholar 

  19. Berenson MC, Blevins FT, Plaas AH, Vogel KG. Proteoglycans of human rotator cuff tendons. J Orthop Res. 1996;14(4):518–25.

    Article  CAS  PubMed  Google Scholar 

  20. Riley G. Tendinopathy—from basic science to treatment. Nat Clin Pract Rheumatol. 2008;4(2):82–9.

    Article  PubMed  Google Scholar 

  21. Järvinen M, Józsa L, Kannus P, Järvinen TL, Kvist M, Leadbetter W. Histopathological findings in chronic tendon disorders. Scand J Med Sci Sports. 1997;7(2):86–95.

    Article  PubMed  Google Scholar 

  22. Movin T, Kristoffersen-Wiberg M, Shalabi A, Gad A, Aspelin P, Rolf C. Intratendinous alterations as imaged by ultrasound and contrast medium-enhanced magnetic resonance in chronic achillodynia. Foot Ankle Int. 1998;19(5):311–7.

    Article  CAS  PubMed  Google Scholar 

  23. Schubert TEO, Weidler C, Lerch K, Hofstädter F, Straub RH. Achilles tendinosis is associated with sprouting of substance P positive nerve fibres. Ann Rheum Dis. 2005;64(7):1083–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Gotoh M, Hamada K, Yamakawa H, Tomonaga A, Inoue A, Fukuda H. Significance of granulation tissue in torn supraspinatus insertions: an immunohistochemical study with antibodies against interleukin-1 beta, cathepsin D, and matrix metalloprotease-1. J Orthop Res. 1997;15(1):33–9.

    Article  CAS  PubMed  Google Scholar 

  25. Zhang J, Wang JH-C. Production of PGE(2) increases in tendons subjected to repetitive mechanical loading and induces differentiation of tendon stem cells into non-tenocytes. J Orthop Res. 2010;28(2):198–203.

    PubMed  Google Scholar 

  26. Alfredson H, Lorentzon R. Intratendinous glutamate levels and eccentric training in chronic Achilles tendinosis: a prospective study using microdialysis technique. Knee Surg Sports Traumatol Arthrosc J. 2003;11(3):196–9.

    Article  Google Scholar 

  27. Uhthoff HK, Sano H. Pathology of failure of the rotator cuff tendon. Orthop Clin North Am. 1997;28(1):31–41.

    Article  CAS  PubMed  Google Scholar 

  28. Ker RF, Wang XT, Pike AV. Fatigue quality of mammalian tendons. J Exp Biol. 2000;203(Pt 8):1317–27.

    CAS  PubMed  Google Scholar 

  29. Chard MD, Cawston TE, Riley GP, Gresham GA, Hazleman BL. Rotator cuff degeneration and lateral epicondylitis: a comparative histological study. Ann Rheum Dis. 1994;53(1):30–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Chard MD, Hazleman BL. Tennis elbow—a reappraisal. Br J Rheumatol. 1989;28(3):186–90.

    Article  CAS  PubMed  Google Scholar 

  31. Fukuda H, Hamada K, Yamanaka K. Pathology and pathogenesis of bursal-side rotator cuff tears viewed from en bloc histologic sections. Clin Orthop. 1990;254:75–80.

    Google Scholar 

  32. Riley GP, Goddard MJ, Hazleman BL. Histopathological assessment and pathological significance of matrix degeneration in supraspinatus tendons. Rheumatology (Oxford). 2001;40(2):229–30.

    Article  CAS  Google Scholar 

  33. Nixon JE, DiStefano V. Ruptures of the rotator cuff. Orthop Clin North Am. 1975;6(2):423–47.

    CAS  PubMed  Google Scholar 

  34. Kjellin I, Ho CP, Cervilla V, Haghighi P, Kerr R, Vangness CT. Alterations in the supraspinatus tendon at MR imaging: correlation with histopathologic findings in cadavers. Radiology. 1991;181(3):837–41.

    Article  CAS  PubMed  Google Scholar 

  35. Pettersson G. Rupture of the tendon aponeurosis of the shoulder joint in anterio-inferior disclocation: a study on the origin and occurrence of ruptures. Acta Chir Scand. 1942;87(suppl 77):1–184.

    Google Scholar 

  36. Pajala A, Melkko J, Leppilahti J, Ohtonen P, Soini Y, Risteli J. Tenascin-C and type I and III collagen expression in total Achilles tendon rupture. An immunohistochemical study. Histol Histopathol. 2009;24(10):1207–11.

    CAS  PubMed  Google Scholar 

  37. Eriksen HA, Pajala A, Leppilahti J, Risteli J. Increased content of type III collagen at the rupture site of human Achilles tendon. J Orthop Res. 2002;20(6):1352–7.

    Article  CAS  PubMed  Google Scholar 

  38. Soslowsky LJ, Fryhofer GW. Tendon homeostasis in hypercholesterolemia. Adv Exp Med Biol. 2016;920:151–65.

    Article  CAS  PubMed  Google Scholar 

  39. Taylor B, Cheema A, Soslowsky L. Tendon pathology in hypercholesterolemia and familial hypercholesterolemia. Curr Rheumatol Rep. 2017;19(12):76.

    Article  PubMed  CAS  Google Scholar 

  40. Beason DP, Abboud JA, Kuntz AF, Bassora R, Soslowsky LJ. Cumulative effects of hypercholesterolemia on tendon biomechanics in a mouse model. J Orthop Res. 2011;29(3):380–3.

    Article  PubMed  Google Scholar 

  41. Beason DP, Tucker JJ, Lee CS, Edelstein L, Abboud JA, Soslowsky LJ. Rat rotator cuff tendon-to-bone healing properties are adversely affected by hypercholesterolemia. J Shoulder Elbow Surg. 2014;23(6):867–72.

    Article  PubMed  Google Scholar 

  42. Lin TT-L, Lin C-H, Chang C-L, Chi C-H, Chang S-T, Sheu WH-H. The effect of diabetes, hyperlipidemia, and statins on the development of rotator cuff disease: a nationwide, 11-year, longitudinal, population-based follow-up study. Am J Sports Med. 2015;43(9):2126–32.

    Article  PubMed  Google Scholar 

  43. Longo UG, Franceschi F, Spiezia F, Forriol F, Maffulli N, Denaro V. Triglycerides and total serum cholesterol in rotator cuff tears: do they matter. Br J Sports Med. 2010;44(13):948–51.

    Article  CAS  PubMed  Google Scholar 

  44. Abboud JA, Kim JS. The effect of hypercholesterolemia on rotator cuff disease. Clin Orthop. 2010;468(6):1493–7.

    Article  PubMed  Google Scholar 

  45. Kruth HS. Cholesterol accumulation in vascular smooth muscle cells incorporated into platelet-rich plasma clots. Lab Investig J Tech Methods Pathol. 1985;53(6):634–8.

    CAS  Google Scholar 

  46. Artieda M, Cenarro A, Junquera C, Lasierra P, Martínez-Lorenzo MJ, Pocoví M. Tendon xanthomas in familial hypercholesterolemia are associated with a differential inflammatory response of macrophages to oxidized LDL. FEBS Lett. 2005;579(20):4503–12.

    Article  CAS  PubMed  Google Scholar 

  47. Rönnemaa T, Juva K, Kulonen E. Effect of hyperlipidemic rat serum on the synthesis of collagen by chick embryo fibroblasts. Atherosclerosis. 1975;21(3):315–24.

    Article  PubMed  Google Scholar 

  48. Nunes RLV, Bruschini H, Utsunomia K, Silveira MA, Teodoro WR, Leite KRM. Influence of a hypercholesterolemic diet on the collagen composition of the bladder wall extracellular matrix in rats. Histol Histopathol. 2012;27(6):745–52.

    CAS  PubMed  Google Scholar 

  49. Oberkersch R, Maccari F, Bravo AI, Volpi N, Gazzaniga S, Calabrese GC. Atheroprotective remodelling of vascular dermatan sulphate proteoglycans in response to hypercholesterolaemia in a rat model. Int J Exp Pathol. 2014;95(3):181–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Chung SW, Park H, Kwon J, Choe GY, Kim SH, Oh JH. Effect of hypercholesterolemia on fatty infiltration and quality of tendon-to-bone healing in a rabbit model of a chronic rotator cuff tear: electrophysiological, biomechanical, and histological analyses. Am J Sports Med. 2016;44(5):1153–64.

    Article  PubMed  Google Scholar 

  51. Rolf C, Movin T. Etiology, histopathology, and outcome of surgery in achillodynia. Foot Ankle Int. 1997;18(9):565–9.

    Article  CAS  PubMed  Google Scholar 

  52. Franceschi F, Papalia R, Paciotti M, Franceschetti E, Di Martino A, Maffulli N. Obesity as a risk factor for tendinopathy: a systematic review. Int J Endocrinol. 2014;2014:670262.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Giai Via A, Papa G, Oliva F, Maffulli N. Tendinopathy. Curr Phys Med Rehabil Rep. 2016.

    Google Scholar 

  54. Moor BK, Röthlisberger M, Müller DA, Zumstein MA, Bouaicha S, Ehlinger M. Age, trauma and the critical shoulder angle accurately predict supraspinatus tendon tears. Orthop Traumatol Surg Res. 2014;100(5):489–94.

    Article  CAS  PubMed  Google Scholar 

  55. Gerber C, Snedeker JG, Baumgartner D, Viehöfer AF. Supraspinatus tendon load during abduction is dependent on the size of the critical shoulder angle: a biomechanical analysis. J Orthop Res. 2014;32(7):952–7.

    Article  PubMed  Google Scholar 

  56. Nyffeler RW, Werner CML, Sukthankar A, Schmid MR, Gerber C. Association of a large lateral extension of the acromion with rotator cuff tears. J Bone Joint Surg Am. 2006;88(4):800–5.

    PubMed  Google Scholar 

  57. Neer CS. Anterior acromioplasty for the chronic impingement syndrome in the shoulder: a preliminary report. J Bone Joint Surg Am. 1972;54(1):41–50.

    Article  PubMed  Google Scholar 

  58. Bigliani LU, Ticker JB, Flatow EL, Soslowsky LJ, Mow VC. The relationship of acromial architecture to rotator cuff disease. Clin Sports Med. 1991;10(4):823–38.

    CAS  PubMed  Google Scholar 

  59. Seitz AL, Michener LA. Ultrasonographic measures of subacromial space in patients with rotator cuff disease: a systematic review. J Clin Ultrasound. 2011;39(3):146–54.

    Article  PubMed  Google Scholar 

  60. Maffulli N, Longo UG, Berton A, Loppini M, Denaro V. Biological factors in the pathogenesis of rotator cuff tears. Sports Med Arthrosc Rev. 2011;19(3):194–201.

    Article  PubMed  Google Scholar 

  61. Soslowsky LJ, Thomopoulos S, Tun S, Flanagan CL, Keefer CC, Mastaw J, Neer Award 1999. Overuse activity injures the supraspinatus tendon in an animal model: a histologic and biomechanical study. J Shoulder Elbow Surg. 2000;9(2):79–84.

    Article  CAS  PubMed  Google Scholar 

  62. Soslowsky LJ, Thomopoulos S, Esmail A, Flanagan CL, Iannotti JP, Williamson JD. Rotator cuff tendinosis in an animal model: role of extrinsic and overuse factors. Ann Biomed Eng. 2002;30(8):1057–63.

    Article  PubMed  Google Scholar 

  63. Gia Via A, De Cupis M, Spoliti M, Oliva F. Clinical and biological aspects of rotator cuff tears. Muscles Ligaments Tendons J. 2013;3(2):70–9.

    Article  Google Scholar 

  64. Yamaguchi K, Ditsios K, Middleton WD, Hildebolt CF, Galatz LM, Teefey SA. The demographic and morphological features of rotator cuff disease. A comparison of asymptomatic and symptomatic shoulders. J Bone Joint Surg Am. 2006;88(8):1699–704.

    Article  PubMed  Google Scholar 

  65. Carbone S, Gumina S, Arceri V, Campagna V, Fagnani C, Postacchini F. The impact of preoperative smoking habit on rotator cuff tear: cigarette smoking influences rotator cuff tear sizes. J Shoulder Elbow Surg. 2012;21(1):56–60.

    Article  PubMed  Google Scholar 

  66. Lundgreen K, Lian OB, Scott A, Nassab P, Fearon A, Engebretsen L. Rotator cuff tear degeneration and cell apoptosis in smokers versus nonsmokers. Arthrosc J Arthrosc Relat Surg. 2014;30(8):936–41.

    Article  Google Scholar 

  67. Baumgarten KM, Gerlach D, Galatz LM, Teefey SA, Middleton WD, Ditsios K. Cigarette smoking increases the risk for rotator cuff tears. Clin Orthop. 2010;468(6):1534–41.

    Article  PubMed  Google Scholar 

  68. Lohr JF, Uhthoff HK. The microvascular pattern of the supraspinatus tendon. Clin Orthop. 1990;254:35–8.

    Google Scholar 

  69. Brooks CH, Revell WJ, Heatley FWA. quantitative histological study of the vascularity of the rotator cuff tendon. J Bone Joint Surg Br. 1992;74(1):151–3.

    Article  CAS  PubMed  Google Scholar 

  70. Snedeker JG, Gautieri A. The role of collagen crosslinks in ageing and diabetes—the good, the bad, and the ugly. Muscles Ligaments Tendons J. 2014;4(3):303–8.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Ahmed N. Advanced glycation endproducts—role in pathology of diabetic complications. Diabetes Res Clin Pract. 2005;67(1):3–21.

    Article  CAS  PubMed  Google Scholar 

  72. Li Y, Fessel G, Georgiadis M, Snedeker JG. Advanced glycation end-products diminish tendon collagen fiber sliding. Matrix Biol J Int Soc Matrix Biol. 2013;32(3–4):169–77.

    Article  CAS  Google Scholar 

  73. Gautieri A, Passini FS, Silván U, Guizar-Sicairos M, Carimati G, Volpi P. Advanced glycation end-products: mechanics of aged collagen from molecule to tissue. Matrix Biol J Int Soc. 2017;59:95–108.

    Article  CAS  Google Scholar 

  74. Chung SW, Choi BM, Kim JY, Lee Y-S, Yoon JP, Oh K-S. Altered gene and protein expressions in torn rotator cuff tendon tissues in diabetic patients. Arthrosc J Arthrosc Relat Surg. 2017;33(3):518–526.e1.

    Article  Google Scholar 

  75. Duncan WS. Relationship of thyroid disease to chronic nonspecific arthritis. JAMA. 1932;99(15):1239.

    Article  Google Scholar 

  76. Oliva F, Osti L, Padulo J, Maffulli N. Epidemiology of the rotator cuff tears: a new incidence related to thyroid disease. Muscles Ligaments Tendons J. 2014;4(3):309–14.

    Article  PubMed  PubMed Central  Google Scholar 

  77. Oliva F, Berardi AC, Misiti S, Verga Falzacappa C, Falzacappa CV, Iacone A. Thyroid hormones enhance growth and counteract apoptosis in human tenocytes isolated from rotator cuff tendons. Cell Death Dis. 2013;4:e705.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Berardi AC, Oliva F, Berardocco M, la Rovere M, Accorsi P, Maffulli N. Thyroid hormones increase collagen I and cartilage oligomeric matrix protein (COMP) expression in vitro human tenocytes. Muscles Ligaments Tendons J. 2014;4(3):285–91.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Beason DP, Hsu JE, Marshall SM, McDaniel AL, Temel RE, Abboud JA. Hypercholesterolemia increases supraspinatus tendon stiffness and elastic modulus across multiple species. J Shoulder Elbow Surg. 2013;22(5):681–6.

    Article  PubMed  Google Scholar 

  80. Beason DP, Hsu JE, Edelstein L, Lee CS, Tucker JJ, Abboud JA. Effect of diet-induced hypercholesterolemia on rotator cuff tendon mechanics in a rat model. Trans Orthop Res Soc. 2011;36:22.

    Google Scholar 

  81. Bhattacharyya AK, Connor WE, Mausolf FA, Flatt AD. Turnover of xanthoma cholesterol in hyperlipoproteinemia patients. Lab Clin Med. 1976;87:503–18.

    CAS  Google Scholar 

  82. Tashjian RZ, Farnham JM, Albright FS, Teerlink CC, Cannon-Albright LA. Evidence for an inherited predisposition contributing to the risk for rotator cuff disease. J Bone Joint Surg Am. 2009;91(5):1136–42.

    Article  PubMed  PubMed Central  Google Scholar 

  83. Harvie P, Ostlere SJ, Teh J, McNally EG, Clipsham K, Burston BJ. Genetic influences in the aetiology of tears of the rotator cuff. Sibling risk of a full-thickness tear. J Bone Joint Surg Br. 2004;86(5):696–700.

    Article  CAS  PubMed  Google Scholar 

  84. Tashjian RZ, Farnham JM, Granger EK, Teerlink CC, Cannon-Albright LA. Evidence for an environmental and inherited predisposition contributing to the risk for global tendinopathies or compression neuropathies in patients with rotator cuff tears. Orthop J Sports Med. 2016;4(4):2325967116642173.

    Article  PubMed  PubMed Central  Google Scholar 

  85. Molloy TJ, Kemp MW, Wang Y, Murrell G. Microarray analysis of the tendinopathic rat supraspinatus tendon: glutamate signaling and its potential role in tendon degeneration. J Appl Physiol. 2006;101(6):1702–9.

    Article  CAS  PubMed  Google Scholar 

  86. Hynd MR, Scott HL, Dodd PR. Glutamate-mediated excitotoxicity and neurodegeneration in Alzheimer’s disease. Neurochem Int. 2004;45(5):583–95.

    Article  CAS  PubMed  Google Scholar 

  87. Skerry TM. Identification of novel signaling pathways during functional adaptation of the skeleton to mechanical loading: the role of glutamate as a paracrine signaling agent in the skeleton. J Bone Miner Metab. 1999;17(1):66–70.

    Article  CAS  PubMed  Google Scholar 

  88. Orth T, Paré J, Froehlich JE. Current concepts on the genetic factors in rotator cuff pathology and future implications for sports physical therapists. Int J Sports Phys Ther. 2017;12(2):273–85.

    PubMed  PubMed Central  Google Scholar 

  89. Osti L, Buda M, Del Buono A, Osti R, Massari L, Maffulli N. Apoptosis and rotator cuff tears: scientific evidence from basic science to clinical findings. Br Med Bull. 2017;122(1):123–33.

    Article  CAS  PubMed  Google Scholar 

  90. Yuan J, Murrell GAC, Wei A-Q, Wang M-X. Apoptosis in rotator cuff tendonopathy. J Orthop Res. 2002;20(6):1372–9.

    Article  PubMed  Google Scholar 

  91. Wu B, Chen J, Rosa TD, Yu Q, Wang A, Xu J. Cellular response and extracellular matrix breakdown in rotator cuff tendon rupture. Arch Orthop Trauma Surg. 2011;131(3):405–11.

    Article  PubMed  Google Scholar 

  92. Suzanne M, Steller H. Letting go: modification of cell adhesion during apoptosis. J Biol. 2009;8(5):49.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  93. Wolf BB, Green DR. Suicidal tendencies: apoptotic cell death by caspase family proteinases. J Biol Chem. 1999;274(29):20049–52.

    Article  CAS  PubMed  Google Scholar 

  94. Lee H-J, Kim Y-S, Ok J-H, Song H-J. Apoptosis occurs throughout the diseased rotator cuff. Am J Sports Med. 2013;41(10):2249–55.

    Article  PubMed  Google Scholar 

  95. Riley GP, Curry V, DeGroot J, van El B, Verzijl N, Hazleman BL. Matrix metalloproteinase activities and their relationship with collagen remodelling in tendon pathology. Matrix Biol J Int Soc Matrix Biol. 2002;21(2):185–95.

    Article  CAS  Google Scholar 

  96. Castagna A, Cesari E, Garofalo R, Gigante A, Conti M, Markopoulos N. Matrix metalloproteases and their inhibitors are altered in torn rotator cuff tendons, but also in the macroscopically and histologically intact portion of those tendons. Muscles Ligaments Tendons J. 2013;3(3):132–8.

    PubMed  PubMed Central  Google Scholar 

  97. Tashjian RZ, Granger EK, Farnham JM, Cannon-Albright LA, Teerlink CC. Genome-wide association study for rotator cuff tears identifies two significant single-nucleotide polymorphisms. J Shoulder Elbow Surg. 2016;25(2):174–9.

    Article  PubMed  Google Scholar 

  98. Tashjian RZ, Granger EK, Zhang Y, Teerlink CC, Cannon-Albright LA. Identification of a genetic variant associated with rotator cuff repair healing. J Shoulder Elbow Surg. 2016;25(6):865–72.

    Article  PubMed  Google Scholar 

  99. Zumstein M-A, Lädermann A, Raniga S, Schär M-O. The biology of rotator cuff healing. Orthop Traumatol Surg Res. 2017;103(1S):S1–10.

    Article  PubMed  Google Scholar 

  100. Beredjiklian PK. Biologic aspects of flexor tendon laceration and repair. J Bone Joint Surg Am. 2003;85-A(3):539–50.

    Article  Google Scholar 

  101. Andrianjafiniony T, Dupré-Aucouturier S, Letexier D, Couchoux H, Desplanches D. Oxidative stress, apoptosis, and proteolysis in skeletal muscle repair after unloading. Am J Physiol Cell Physiol. 2010;299(2):C307–15.

    Article  CAS  PubMed  Google Scholar 

  102. Arnold L, Henry A, Poron F, Baba-Amer Y, van Rooijen N, Plonquet A. Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J Exp Med. 2007;204(5):1057–69.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Murphy PG, Loitz BJ, Frank CB, Hart DA. Influence of exogenous growth factors on the synthesis and secretion of collagen types I and III by explants of normal and healing rabbit ligaments. Biochem Cell Biol Biochim Biol Cell. 1994;72(9–10):403–9.

    Article  CAS  Google Scholar 

  104. Hays PL, Kawamura S, Deng X-H, Dagher E, Mithoefer K, Ying L. The role of macrophages in early healing of a tendon graft in a bone tunnel. J Bone Joint Surg Am. 2008;90(3):565–79.

    Article  PubMed  Google Scholar 

  105. Zanou N, Gailly P. Skeletal muscle hypertrophy and regeneration: interplay between the myogenic regulatory factors (MRFs) and insulin-like growth factors (IGFs) pathways. Cell Mol Life Sci. 2013;70(21):4117–30.

    Article  CAS  PubMed  Google Scholar 

  106. Frey E, Regenfelder F, Sussmann P, Zumstein M, Gerber C, Born W. Adipogenic and myogenic gene expression in rotator cuff muscle of the sheep after tendon tear. J Orthop Res. 2009;27(4):504–9.

    Article  CAS  PubMed  Google Scholar 

  107. Lee YS, Jeong JY, Park C-D, Kang SG, Yoo JC. Evaluation of the risk factors for a rotator cuff retear after repair surgery. Am J Sports Med. 2017;45(8):1755–61.

    Article  PubMed  Google Scholar 

  108. Tashjian RZ, Hollins AM, Kim H-M, Teefey SA, Middleton WD, Steger-May K. Factors affecting healing rates after arthroscopic double-row rotator cuff repair. Am J Sports Med. 2010;38(12):2435–42.

    Article  PubMed  Google Scholar 

  109. Diebold G, Lam P, Walton J, Murrell GAC. Relationship between age and rotator cuff retear: a study of 1,600 consecutive rotator cuff repairs. J Bone Joint Surg Am. 2017;99(14):1198–205.

    Article  PubMed  Google Scholar 

  110. Kwon J, Kim SH, Lee YH, Kim TI, Oh JH. The rotator cuff healing index: a new scoring system to predict rotator cuff healing after surgical repair. Am J Sports Med. 2019;47(1):173–80.

    Article  PubMed  Google Scholar 

  111. Chillemi C, Petrozza V, Garro L, Sardella B, Diotallevi R, Ferrara A. Rotator cuff re-tear or non-healing: histopathological aspects and predictive factors. Knee Surg Sports Traumatol Arthrosc. 2011;19(9):1588–96.

    Article  CAS  PubMed  Google Scholar 

  112. Plate JF, Brown PJ, Walters J, Clark JA, Smith TL, Freehill MT. Advanced age diminishes tendon-to-bone healing in a rat model of rotator cuff repair. Am J Sports Med. 2014;42(4):859–68.

    Article  PubMed  Google Scholar 

  113. Galatz LM, Silva MJ, Rothermich SY, Zaegel MA, Havlioglu N, Thomopoulos S. Nicotine delays tendon-to-bone healing in a rat shoulder model. J Bone Joint Surg Am. 2006;88(9):2027–34.

    CAS  PubMed  Google Scholar 

  114. Park JH, Oh K-S, Kim TM, Kim J, Yoon JP, Kim JY. Effect of smoking on healing failure after rotator cuff repair. Am J Sports Med. 2018;46(12):2960–8.

    Article  PubMed  Google Scholar 

  115. Bedi A, Fox AJS, Harris PE, Deng X-H, Ying L, Warren RF. Diabetes mellitus impairs tendon-bone healing after rotator cuff repair. J Shoulder Elbow Surg. 2010;19(7):978–88.

    Article  PubMed  PubMed Central  Google Scholar 

  116. Chen AL, Shapiro JA, Ahn AK, Zuckerman JD, Cuomo F. Rotator cuff repair in patients with type I diabetes mellitus. J Shoulder Elbow Surg. 2003;12(5):416–21.

    Article  PubMed  Google Scholar 

  117. Garcia GH, Liu JN, Wong A, Cordasco F, Dines DM, Dines JS. Hyperlipidemia increases the risk of retear after arthroscopic rotator cuff repair. J Shoulder Elbow Surg. 2017;26(12):2086–90.

    Article  PubMed  Google Scholar 

  118. Tanaka K, Kanazawa T, Gotoh M, Tanesue R, Nakamura H, Ohzono H. Effects of estrogen-deficient state on rotator cuff healing. Am J Sports Med. 2019;47(2):389–97.

    Article  PubMed  Google Scholar 

  119. Angeline ME, Ma R, Pascual-Garrido C, Voigt C, Deng XH, Warren RF. Effect of diet-induced vitamin D deficiency on rotator cuff healing in a rat model. Am J Sports Med. 2014;42(1):27–34.

    Article  PubMed  Google Scholar 

  120. Ryu KJ, Kim BH, Lee Y, Dan J, Kim JH, Low Serum Vitamin D. Is not correlated with the severity of a rotator cuff tear or retear after arthroscopic repair. Am J Sports Med. 2015;43(7):1743–50.

    Article  PubMed  Google Scholar 

  121. Randelli P, Cucchi D, Ragone V, de Girolamo L, Cabitza P, Randelli M. History of rotator cuff surgery. Knee Surg Sports Traumatol Arthrosc J. 2015;23(2):344–62.

    Article  Google Scholar 

  122. Spennacchio P, Banfi G, Cucchi D, D’Ambrosi R, Cabitza P, Randelli P. Long-term outcome after arthroscopic rotator cuff treatment. Knee Surg Sports Traumatol Arthrosc J. 2015;23(2):523–9.

    Article  Google Scholar 

  123. Walter SG, Stadler T, Thomas TS, Thomas W. Advanced rotator cuff tear score (ARoCuS): a multi-scaled tool for the classification and description of rotator cuff tears. Musculoskelet Surg. 2019;103(1):37–45.

    Article  CAS  PubMed  Google Scholar 

  124. Milano G, Saccomanno MF, Careri S, Taccardo G, De Vitis R, Fabbriciani C. Efficacy of marrow-stimulating technique in arthroscopic rotator cuff repair: a prospective randomized study. Arthrosc J Arthrosc Relat Surg. 2013;29(5):802–10.

    Article  Google Scholar 

  125. Kida Y, Morihara T, Matsuda K-I, Kajikawa Y, Tachiiri H, Iwata Y. Bone marrow-derived cells from the footprint infiltrate into the repaired rotator cuff. J Shoulder Elbow Surg. 2013;22(2):197–205.

    Article  PubMed  Google Scholar 

  126. Jo CH, Shin JS, Park IW, Kim H, Lee SY. Multiple channeling improves the structural integrity of rotator cuff repair. Am J Sports Med. 2013;41(11):2650–7.

    Article  PubMed  Google Scholar 

  127. Nakagawa H, Morihara T, Fujiwara H, Kabuto Y, Sukenari T, Kida Y. Effect of footprint preparation on tendon-to-bone healing: a histologic and biomechanical study in a rat rotator cuff repair model. Arthrosc J Arthrosc Relat Surg. 2017;33(8):1482–92.

    Article  Google Scholar 

  128. Gereli A, Kocaoglu B, Ulku TK, Silay S, Kilinc E, Uslu S. u. a. Completion repair exhibits increased healing characteristics compared with in situ repair of partial thickness bursal rotator cuff tears. Knee Surg Sports Traumatol Arthrosc. 2018;26(8):2498–504.

    Article  PubMed  Google Scholar 

  129. Cavinatto L, Malavolta EA, Pereira CAM, Miranda-Rodrigues M, Silva LCM, Gouveia CH. Early versus late repair of rotator cuff tears in rats. J Shoulder Elbow Surg. 2018;27(4):606–13.

    Article  PubMed  Google Scholar 

  130. Mukovozov I, Byun S, Farrokhyar F, Wong I. Time to surgery in acute rotator cuff tear: a systematic review. Bone Jt Res. 2013;2(7):122–8.

    Article  CAS  Google Scholar 

  131. Ohzono H, Gotoh M, Nakamura H, Honda H, Mitsui Y, Kakuma T. Effect of preoperative fatty degeneration of the rotator cuff muscles on the clinical outcome of patients with intact tendons after arthroscopic rotator cuff repair of large/massive cuff tears. Am J Sports Med. 2017;45(13):2975–81.

    Article  PubMed  Google Scholar 

  132. Jeong HY, Kim HJ, Jeon YS, Rhee YG. Factors predictive of healing in large rotator cuff tears: is it possible to predict retear preoperatively. Am J Sports Med. 2018;46(7):1693–700.

    Article  PubMed  Google Scholar 

  133. Riboh JC, Garrigues GE. Early passive motion versus immobilization after arthroscopic rotator cuff repair. Arthrosc J Arthrosc Relat Surg. 2014;30(8):997–1005.

    Article  Google Scholar 

  134. Houck DA, Kraeutler MJ, Schuette HB, McCarty EC, Bravman JT. Early versus delayed motion after rotator cuff repair: a systematic review of overlapping meta-analyses. Am J Sports Med. 2017;45(12):2911–5.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Marco Viganò, IRCCS Orthopaedic Institute Galeazzi, for his precious help with the chapter.

Author information

Authors and Affiliations

  1. Department of Orthopaedic and Traumatology, Sant’Anna Hospital, Como, Italy

    Alessio Giai Via

  2. Department of Orthopaedics and Trauma Surgery, Universitätsklinikum, Bonn, Germany

    Davide Cucchi

  3. Orthopaedic Biotechnology Laboratory, IRCCS Orthopaedic Institute Galeazzi, Milan, Italy

    Laura de Girolamo

Authors
  1. Alessio Giai Via
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Davide Cucchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Laura de Girolamo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Laura de Girolamo .

Editor information

Editors and Affiliations

  1. Hospital das Forças Armadas and Hospital da Luz, Porto, Portugal

    Nuno Sampaio Gomes

  2. Department of Traumatology, University Medical Centre Ljubljana, Ljubljana, Slovenia

    Ladislav Kovačič

  3. ATOS Klinik München, Deutsches Schulterzentrum, München, Bayern, Germany

    Frank Martetschläger

  4. Department of Orthopaedics, University of Brescia, Brescia, Italy

    Giuseppe Milano

Rights and permissions

Reprints and permissions

Copyright information

© 2020 ESSKA

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Giai Via, A., Cucchi, D., de Girolamo, L. (2020). Biology of Rotator Cuff Injury and Repair. In: Sampaio Gomes, N., Kovačič, L., Martetschläger, F., Milano, G. (eds) Massive and Irreparable Rotator Cuff Tears. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-61162-3_2

Download citation

  • DOI: https://doi.org/10.1007/978-3-662-61162-3_2

  • Published:

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-662-61161-6

  • Online ISBN: 978-3-662-61162-3

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Search

Navigation