Biological factors in the pathogenesis of rotator cuff tears

Sports Medicine and Arthroscopy Review

Volumn 19, Issue 3, 2011, Pages 194-201

  Maffulli, Nicola ^a   Longo, Umile Giuseppe ^b,c   Berton, Alessandra ^c   Loppini, Mattia ^c   Denaro, Vincenzo ^c  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b ROYAL FREE LONDON NHS FOUNDATION TRUST   (United Kingdom)

^c UNIVERSITY CAMPUS BIO MEDICO   (Italy)

Author keywords

apoptosis; genetics; pathogenesis; rotator cuff tear; sports; tendon

Indexed keywords

BIOLOGICAL FACTOR; CASPASE 3; CASPASE 8; CHOLESTEROL; COLLAGEN FIBER; COLLAGEN TYPE 5; CYTOKINE; FAS LIGAND; FLICE INHIBITORY PROTEIN; GLUCOSE; GLUTAMIC ACID; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 70; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INTERSTITIAL COLLAGENASE; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MITOGEN ACTIVATED PROTEIN KINASE 12; MITOGEN ACTIVATED PROTEIN KINASE P38; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE 1; TENASCIN; TRIACYLGLYCEROL;

ABRASION; ACROMION; AGING; APOPTOSIS; COMPRESSION; ENVIRONMENTAL FACTOR; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENETIC SUSCEPTIBILITY; GLUCOSE BLOOD LEVEL; HEREDITY; HISTOPATHOLOGY; HUMAN; HUMERUS; LIPID STORAGE; MENISCECTOMY; MICROARRAY ANALYSIS; MICROVASCULARIZATION; MUSCLE ATROPHY; NONHUMAN; OSTEOPHYTE; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVIEW; ROTATOR CUFF RUPTURE; SHOULDER PAIN; SMOKING; STRESS;

APOPTOSIS; BIOLOGICAL FACTORS; CYTOKINES; FEMALE; HUMANS; LIPID METABOLISM; MALE; METALLOPROTEASES; ROTATOR CUFF; SHOULDER JOINT; TENDON INJURIES;

EID: 80051761078     PISSN: 10628592     EISSN: 15381951     Source Type: Journal    
DOI: 10.1097/JSA.0b013e3182250cad     Document Type: Review

References (154)

1. Bunker T. Rotator cuff disease. Curr Orthopaedic. 2002;16:223-233.
2. Roquelaure Y, Ha C, Leclerc A, et al. Epidemiologic surveillance of upper-extremity musculoskeletal disorders in the working population. Arthritis Rheum. 2006;55:765-778. (Pubitemid 44619191)
3. Maffulli N, Longo UG, Gougoulias N, et al. Long-term health outcomes of youth sports injuries. Br J Sports Med. 2010;44:21-25.
4. Maffulli N, Longo UG, Loppini M, et al. Current treatment options for tendinopathy. Expert Opin Pharmacother. 2010;11:2177-2186.
5. Maffulli N, Longo UG, Spiezia F, et al. Sports injuries in young athletes: long-term outcome and prevention strategies. Phys Sports Med. 2010;38:29-34.
6. Maffulli N, Longo UG, Gougoulias N, et al. Sport injuries: a review of outcomes. Br Med Bull. 2011;97:47-80.
7. Maffulli N, Longo U, Denaro V. The pathogenesis and surgical treatment of tears of the rotator cuff. J Bone Joint Surg Br. 2008; http://www.jbjs.org.uk/ cgi/eletters/90-B/?7/827#top.
8. Longo UG, Franceschi F, Ruzzini L, et al. Histopathology of the supraspinatus tendon in rotator cuff tears. Am J Sports Med. 2008;36:533-538. (Pubitemid 351253387)
9. Franceschi F, Longo UG, Ruzzini L, et al. To detach the long head of the biceps tendon after tenodesis or not: outcome analysis at the 4-year follow-up of two different techniques. Int Orthop. 2007;31:537-545. (Pubitemid 47101361)
10. Fukuda H, Hamada K, Nakajima T, et al. Pathology and pathogenesis of the intratendinous tearing of the rotator cuff viewed from en bloc histologic sections. Clin Orthop Relat Res. 1994;304:60-67. (Pubitemid 24230665)
11. Maffulli N, Longo UG, Gougoulias N, et al. Ipsilateral free semitendinosus tendon graft transfer for reconstruction of chronic tears of the achilles tendon. BMC Musculoskelet Disord. 2008;9:100.
12. Matthews TJ, Hand GC, Rees JL, et al. Pathology of the torn rotator cuff tendon. Reduction in potential for repair as tear size increases. J Bone Joint Surg Br. 2006;88:489-495.
13. Almekinders LC, Weinhold PS, Maffulli N. Compression etiology in tendinopathy. Clin Sports Med. 2003;22:703-710. (Pubitemid 37175572)
14. Nho SJ, Yadav H, Shindle MK, et al. Rotator cuff degeneration: etiology and pathogenesis. Am J Sports Med. 2008;36:987-993. (Pubitemid 351551265)
15. Yuan J, Murrell GA, Wei AQ, et al. Apoptosis in rotator cuff tendinopathy. J Orthop Res. 2002;20:1372-1379.
16. Yuan J, Murrell GA, Trickett A, et al. Involvement of cytochrome c release and caspase-3 activation in the oxidative stress-induced apoptosis in human tendon fibroblasts. Biochim Biophys Acta. 2003;1641:35-41. (Pubitemid 36638707)
17. Tran SE, Meinander A, Holmstrom TH, et al. Heat stress downregulates FLIP and sensitizes cells to Fas receptormediated apoptosis. Cell Death Differ. 2003;10:1137-1147. (Pubitemid 37258579)
18. Wang F, Murrell GA, Wang MX. Oxidative stress-induced c-Jun. N-terminal kinase (JNK) activation in tendon cells upregulates MMP1 mRNA and protein expression. J Orthop Res. 2007;25:378-389. (Pubitemid 46455908)
19. Millar NL, Wei AQ, Molloy TJ, et al. Cytokines and apoptosis in supraspinatus tendinopathy. J Bone Joint Surg Br. 2009;91:417-424.
20. Millar NL, Wei AQ, Molloy TJ, et al. Heat shock protein and apoptosis in supraspinatus tendinopathy. Clin Orthop Relat Res. 2008;466:1569-1576.
21. Harvie P, Ostlere SJ, Teh J, et al. Genetic influences in the aetiology of tears of the rotator cuff. Sibling risk of a fullthickness tear. J Bone Joint Surg Br. 2004;86:696-700. (Pubitemid 39077218)
22. September AV, Schwellnus MP, Collins M. Tendon and ligament injuries: the genetic component. Br J Sports Med. 2007;41:241-246; discussion 246. (Pubitemid 350143335)
23. Neer C, Poppen N. Supraspinatus outlet. Orthop Trans. 1987;11:234.
24. Neer CS II. Anterior acromioplasty for the chronic impingement syndrome in the shoulder: a preliminary report. J Bone Joint Surg Am. 1972;54:41-50.
25. Bigliani L, Morrison D, April E. The morphology of the acromion and rotator cuff impingement. Orthop Trans. 1986;10:228.
26. MacGillivray JD, Fealy S, Potter HG, et al. Multiplanar analysis of acromion morphology. Am J Sports Med. 1998;26:836-840. (Pubitemid 28555160)
27. Wang JC, Shapiro MS. Changes in acromial morphology with age. J Shoulder Elbow Surg. 1997;6:55-59. (Pubitemid 127674879)
28. Shah NN, Bayliss NC, Malcolm A. Shape of the acromion: congenital or acquired-a macroscopic, radiographic, and microscopic study of acromion. J Shoulder Elbow Surg. 2001;10:309-316. (Pubitemid 33601570)
29. Loehr J, Uhthoff H. The pathogenesis of degenerative rotator cuff tears. Orthopedic Trans. 1987;11:237.
30. Ogata S, Uhthoff HK. Acromial enthesopathy and rotator cuff tear. A radiologic and histologic postmortem investigation of the coracoacromial arch. Clin Orthop Relat Res. 1990;254:39-48. (Pubitemid 20145881)
31. Sano H, Ishii H, Trudel G, et al. Histologic evidence of degeneration at the insertion of 3 rotator cuff tendons: a comparative study with human cadaveric shoulders. J Shoulder Elbow Surg. 1999;8:574-579.
32. Ozaki J, Fujimoto S, Nakagawa Y, et al. Tears of the rotator cuff of the shoulder associated with pathological changes in the acromion. A study in cadavera. J Bone Joint Surg Am. 1988;70:1224-1230.
33. Thompson WO, Debski RE, Boardman ND, 3rd, et al. A biomechanical analysis of rotator cuff deficiency in a cadaveric model. Am J Sports Med. 1996;24:286-292. (Pubitemid 26152146)
34. Wuelker N, Plitz W, Roetman B, et al. Function of the supraspinatus muscle. Abduction of the humerus studied in cadavers. Acta Orthop Scand. 1994;65:442-446. (Pubitemid 24331056)
35. Edelson G, Teitz C. Internal impingement in the shoulder. J Shoulder Elbow Surg. 2000;9:308-315.
36. Barr K. Rotator cuff disease. Phys Med Rehabil Clin N Am. 2004;15:475-491. (Pubitemid 38625650)
37. Chambler AF, Pitsillides AA, Emery RJ. Acromial spur formation in patients with rotator cuff tears. J Shoulder Elbow Surg. 2003;12:314-321. (Pubitemid 36960098)
38. Sarkar K, Taine W, Uhthoff HK. The ultrastructure of the coracoacromial ligament in patients with chronic impingement syndrome. Clin Orthop Relat Res. 1990;254:49-54. (Pubitemid 20145882)
39. Yamaguchi K, Ditsios K, Middleton WD, et al. The demographic and morphological features of rotator cuff disease. A comparison of asymptomatic and symptomatic shoulders. J Bone Joint Surg Am. 2006;88:1699-1704. (Pubitemid 44200206)
40. Harryman DT II, Hettrich CM, Smith KL, et al. A prospective multipractice investigation of patients with fullthickness rotator cuff tears: the importance of comorbidities, practice, and other covariables on self-assessed shoulder function and health status. J Bone Joint Surg Am. 2003;85-A:690-696. (Pubitemid 36538719)
41. Baumgarten KM, Gerlach D, Galatz LM, et al. Cigarette smoking increases the risk for rotator cuff tears. Clin Orthop Relat Res. 2010;468:1534-1541.
42. Mallon WJ, Misamore G, Snead DS, et al. The impact of preoperative smoking habits on the results of rotator cuff repair. J Shoulder Elbow Surg. 2004;13:129-132. (Pubitemid 38283836)
43. Mosley L, Fineseth F. Cigarette smoking: impairment of digital blood flow and wound healing in the hand. Hand. 1977;9:97-101.
44. Leow YH, Maibach HI. Cigarette smoking, cutaneous vasculature, and tissue oxygen. Clin Dermatol. 1998;16:579-584. (Pubitemid 29372792)
45. Itoi E, Minagawa H, Konno N, et al. Relationship between smoking and rotator cuff tears. J Shoulder Elbow Surg. 1996;5:S124.
46. Galatz LM, Silva MJ, Rothermich SY, et al. Nicotine delays tendon-to-bone healing in a rat shoulder model. J Bone Joint Surg Am. 2006;88:2027-2034. (Pubitemid 44352750)
47. Jorgensen LN, Kallehave F, Christensen E, et al. Less collagen production in smokers. Surgery. 1998;123:450-455. (Pubitemid 28201227)
48. Chen AL, Shapiro JA, Ahn AK, et al. Rotator cuff repair in patients with type I diabetes mellitus. J Shoulder Elbow Surg. 2003;12:416-421. (Pubitemid 37237510)
49. Nakajima T, Rokuuma N, Hamada K, et al. Histological and biomechanical characteristics of the supraspinatus tendon. J Shoulder Elbow Surg. 1994;3:79-87.
50. Lindblom K, Palmer I. Ruptures of the tendon aponeurosis of the shoulder joint. Acta Chir Scand. 1939;82:133-142.
51. Bey MJ, Song HK, Wehrli FW, et al. Intratendinous strain fields of the intact supraspinatus tendon: the effect of glenohumeral joint position and tendon region. J Orthop Res. 2002;20:869-874. (Pubitemid 34823011)
52. Burkhart SS, Esch JC, Jolson RS. The rotator crescent and rotator cable: an anatomic description of the shoulder's "suspension bridge". Arthroscopy. 1993;9:611-616. (Pubitemid 24004154)
53. Hashimoto T, Nobuhara K, Hamada T. Pathologic evidence of degeneration as a primary cause of rotator cuff tear. Clin Orthop Relat Res. 2003;415:111-120. (Pubitemid 37329045)
54. Kannus P, Jozsa L. Histopathological changes preceding spontaneous rupture of a tendon. A controlled study of 891 patients. J Bone Joint Surg Am. 1991;73:1507-1525.
55. Matsen F. Rotator cuff. In: Rockwood CA Jr, Matsen FA III, eds. The Shoulder. Philadelphia, PA: W B Saunders. 1998:755-839.
56. Lohr JF, Uhthoff HK. The microvascular pattern of the supraspinatus tendon. Clin Orthop Relat Res. 1990;254;35-38. (Pubitemid 20145880)
57. Fukuda H, Hamada K, Yamanaka K. Pathology and pathogenesis of bursal-side rotator cuff tears viewed from en bloc histologic sections. Clin Orthop Relat Res. 1990;254:75-80. (Pubitemid 20145886)
58. Swiontkowski M, Iannotti J, Boulas H, et al. Intraoperative assessment of rotator cuff vascularity using laser Doppler flowmetry. In: Post M, Morrey BF, Hawkins RJ, eds. Surgery of the Shoulder. St. Louis, Mo: Mosby. 1990:208-212.
59. Goutallier D, Postel JM, Bernageau J, et al. Fatty infiltration of disrupted rotator cuff muscles. Rev Rhum Engl Ed. 1995;62:415-422.
60. Melis B, Nemoz C, Walch G. Muscle fatty infiltration in rotator cuff tears: descriptive analysis of 1688 cases. Orthop Traumatol Surg Res. 2009;95:319-324.
61. Gladstone JN, Bishop JY, Lo IK, et al. Fatty infiltration and atrophy of the rotator cuff do not improve after rotator cuff repair and correlate with poor functional outcome. Am J Sports Med. 2007;35:719-728. (Pubitemid 46956285)
62. Rubino LJ, Sprott DC, Stills HF Jr., et al. Fatty infiltration does not progress after rotator cuff repair in a rabbit model. Arthroscopy. 2008;24:936-940.
63. Cohen JJ. Apoptosis. Immunol Today. 1993;14:126-130. (Pubitemid 23068297)
64. White E. Life, death, and the pursuit of apoptosis. Genes Dev. 1996;10:1-15. (Pubitemid 26025294)
65. Macaya A. [Apoptosis in the nervous system]. Rev Neurol. 1996;24:1356-1360.
66. Tsan MF, Gao B. Cytokine function of heat shock proteins. Am J Physiol Cell Physiol. 2004;286:C739-C744. (Pubitemid 38543800)
67. Wolf BB, Green DR. Suicidal tendencies: apoptotic cell death by caspase family proteinases. J Biol Chem. 1999;274:20049-20052.
68. Lian O, Scott A, Engebretsen L, et al. Excessive apoptosis in patellar tendinopathy in athletes. Am J Sports Med. 2007;35:605-611. (Pubitemid 46953067)
69. Scott A, Khan KM, Heer J, et al. High strain mechanical loading rapidly induces tendon apoptosis: an ex vivo rat tibialis anterior model. Br J Sports Med. 2005;39:e25.
70. Leeuwenburgh C, Hollander J, Leichtweis S, et al. Adaptations of glutathione antioxidant system to endurance training are tissue and muscle fiber specific. Am J Physiol. 1997;272:R363-R369.
71. Mosser DD, Caron AW, Bourget L, et al. Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis. Mol Cell Biol. 1997;17:5317-5327. (Pubitemid 27357630)
72. Jaattela M, Wissing D, Bauer PA, et al. Major heat shock protein hsp70 protects tumor cells from tumor necrosis factor cytotoxicity. Embo J. 1992;11:3507-3512.
73. Bellmann K, Jaattela M, Wissing D, et al. Heat shock protein hsp70 overexpression confers resistance against nitric oxide. FEBS Lett. 1996;391:185-188. (Pubitemid 26325740)
74. Arnoczky SP, Tian T, Lavagnino M, et al. Activation of stress-activated protein kinases (SAPK) in tendon cells following cyclic strain: the effects of strain frequency, strain magnitude, and cytosolic calcium. J Orthop Res. 2002;20:947-952.
75. Szomor ZL, Appleyard RC, Murrell GA. Overexpression of nitric oxide synthases in tendon overuse. J Orthop Res. 2006;24:80-86. (Pubitemid 43772611)
76. Riley GP. Gene expression and matrix turnover in overused and damaged tendons. Scand J Med Sci Sports. 2005;15:241-251. (Pubitemid 41032388)
77. Qi J, Chi L, Maloney M, et al. Interleukin-1beta increases elasticity of human bioartificial tendons. Tissue Eng. 2006;12:2913-2925. (Pubitemid 46141257)
78. Sun HB, Li Y, Fung DT, et al. Coordinate regulation of IL-1beta and MMP-13 in rat tendons following subrupture fatigue damage. Clin Orthop Relat Res. 2008;466:1555-1561.
79. Nguyen MT, Lue H, Kleemann R, et al. The cytokine macrophage migration inhibitory factor reduces pro-oxidative stress-induced apoptosis. J Immunol. 2003;170:3337-3347. (Pubitemid 36302213)
80. Tsuzaki M, Bynum D, Almekinders L, et al. ATP modulates load-inducible IL-1beta, COX 2, and MMP-3 gene expression in human tendon cells. J Cell Biochem. 2003;89:556-562. (Pubitemid 36648777)
81. Voloshin I, Gelinas J, Maloney MD, et al. Proinflammatory cytokines and metalloproteases are expressed in the subacromial bursa in patients with rotator cuff disease. Arthroscopy. 2005;21:1076.
82. Riley GP, Harrall RL, Cawston TE, et al. Tenascin-C and human tendon degeneration. Am J Pathol. 1996;149:933-943. (Pubitemid 26334177)
83. Riley GP, Harrall RL, Constant CR, et al. Tendon degeneration and chronic shoulder pain: changes in the collagen composition of the human rotator cuff tendons in rotator cuff tendinitis. Ann Rheum Dis. 1994;53:359-366. (Pubitemid 24198922)
84. Gross J, Harper E, Harris ED, et al. Animal collagenases: specificity of action, and structures of the substrate cleavage site. Biochem Biophys Res Commun. 1974;61:605-612.
85. Gotoh M, Hamada K, Yamakawa H, et al. 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;15:33-39. (Pubitemid 27111198)
86. Gomez DE, Alonso DF, Yoshiji H, et al. Tissue inhibitors of metalloproteinases: structure, regulation and biological functions. Eur J Cell Biol. 1997;74:111-122. (Pubitemid 27455388)
87. Gupta S, Barrett T, Whitmarsh AJ, et al. Selective interaction of JNK protein kinase isoforms with transcription factors. Embo J. 1996;15:2760-2770. (Pubitemid 26176253)
88. Skutek M, van Griensven M, Zeichen J, et al. Cyclic mechanical stretching of human patellar tendon fibroblasts: activation of JNK and modulation of apoptosis. Knee Surg Sports Traumatol Arthrosc. 2003;11:122-129. (Pubitemid 38249661)
89. Filomeni G, Aquilano K, Civitareale P, et al. Activation of c-Jun-N-terminal kinase is required for apoptosis triggered by glutathione disulfide in neuroblastoma cells. Free Radic Biol Med. 2005;39:345-354. (Pubitemid 40910191)
90. Magra M, Maffulli N. Genetic aspects of tendinopathy. J Sci Med Sport. 2008;11:243-247. (Pubitemid 351602047)
91. Gwilym SE, Watkins B, Cooper CD, et al. Genetic influences in the progression of tears of the rotator cuff. J Bone Joint Surg Br. 2009;91:915-917.
92. Maffulli N, Walley G, Sayana MK, et al. Eccentric calf muscle training in athletic patients with achilles tendinopathy. Disabil Rehabil. 2008;30:1677-1684.
93. Buskila D. Genetics of chronic pain states. Best Pract Res Clin Rheumatol. 2007;21:535-547. (Pubitemid 46972005)
94. Molloy TJ, Kemp MW, Wang Y, et al. Microarray analysis of the tendinopathic rat supraspinatus tendon: glutamate signaling and its potential role in tendon degeneration. J Appl Physiol. 2006;101:1702-1709. (Pubitemid 44904492)
95. Nicholls DG. Mitochondrial dysfunction and glutamate excitotoxicity studied in primary neuronal cultures. Curr Mol Med. 2004;4:149-177. (Pubitemid 38425912)
96. Hynd MR, Scott HL, Dodd PR. Glutamate-mediated excitotoxicity and neurodegeneration in Alzheimer's disease. Neurochem Int. 2004;45:583-595. (Pubitemid 38844879)
97. Danbolt NC. Glutamate uptake. Prog Neurobiol. 2001;65:1-105. (Pubitemid 32479155)
98. Rothman SM. The neurotoxicity of excitatory amino acids is produced by passive chloride influx. J Neurosci. 1985;5:1483-1489. (Pubitemid 15041463)
99. Alfredson H, Ljung BO, Thorsen K, et al. In vivo investigation of ECRB tendons with microdialysis technique-no signs of inflammation but high amounts of glutamate in tennis elbow. Acta Orthop Scand. 2000;71 475-479.
100. Alfredson H, Thorsen K, Lorentzon R. In situ microdialysis in tendon tissue: high levels of glutamate, but not prostaglandin E2 in chronic Achilles tendon pain. Knee Surg Sports Traumatol Arthrosc. 1999;7:378-381.
101. Molloy TJ, Wang Y, Horner A, et al. Microarray analysis of healing rat Achilles tendon: evidence for glutamate signaling mechanisms and embryonic gene expression in healing tendon tissue. J Orthop Res. 2006;24:842-855. (Pubitemid 43804980)
102. 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;17:66-70. (Pubitemid 29117756)
103. Spencer GJ, Genever PG. Long-term potentiation in bone-a role for glutamate in strain-induced cellular memory. BMC Cell Biol. 2003;4:9.
104. Murano S, Shinomiya M, Shirai K, et al. Characteristic features of long-living patients with familial hypercholesterolemia in Japan. J Am Geriatr Soc. 1993;41:253-257. (Pubitemid 23078114)
105. Ozgurtas T, Yildiz C, Serdar M, et al. Is high concentration of serum lipids a risk factor for Achilles tendon rupture. Clin Chim Acta. 2003;331:25-28. (Pubitemid 36412022)
106. Zehntner MK, Reitamo T, Mordasini R, et al. [Traumatic rupture of the Achilles tendon and hyperlipidemia]. Unfallheilkunde. 1984;87:226-229. (Pubitemid 14104526)
107. Mathiak G, Wening JV, Mathiak M, et al. Serum cholesterol is elevated in patients with Achilles tendon ruptures. Arch Orthop Trauma Surg. 1999;119:280-284. (Pubitemid 29408398)
108. Wendelboe AM, Hegmann KT, Gren LH, et al. Associations between body-mass index and surgery for rotator cuff tendinitis. J Bone Joint Surg Am. 2004;86-A:743-747. (Pubitemid 38436716)
109. Kim K, Owen W, Williams D, et al. A comparison between BMI and conicity index on predicting coronary heart disease: the Framingham Heart Study. Ann Epidemiol 2000;10:424-431.
110. Hubert HB, Feinleib M, McNamara PM, et al. Obesity as an independent risk factor for cardiovascular disease: a 26-year follow-up of participants in the Framingham Heart Study. Circulation. 1983;67:968-977. (Pubitemid 13080473)
111. Siervogel RM, Wisemandle W, Maynard LM, et al. Lifetime overweight status in relation to serial changes in body composition and risk factors for cardiovascular disease: The Fels Longitudinal Study. Obes Res. 2000;8:422-430.
112. Abboud JA, Kim JS. The effect of hypercholesterolemia on rotator cuff disease. Clin Orthop Relat Res. 2010;468:1493-1497.
113. Longo UG, Franceschi F, Spiezia F, et al. Triglycerides and total serum cholesterol in rotator cuff tears: do they matter. Br J Sports Med. 2010;44:948-951.
114. Longo UG, Franceschi F, Ruzzini L, et al. Characteristics at haematoxylin and eosin staining of ruptures of the long head of the biceps tendon. Br J Sports Med. 2009;43:603-607.
115. Crouse JR, Grundy SM, Ahrens EH Jr. Cholesterol distribution in the bulk tissues of man: variation with age. J Clin Invest. 1972;51:1292-1296.
116. Tall AR, Small DM, Lees RS. Interaction of collagen with the lipids of tendon xanthomata. J Clin Invest. 1978;62:836-846. (Pubitemid 9032265)
117. von Bahr S, Movin T, Papadogiannakis N, et al. Mechanism of accumulation of cholesterol and cholestanol in tendons and the role of sterol 27-hydroxylase (CYP27A1). Arterioscler Thromb Vasc Biol. 2002;22:1129-1135. (Pubitemid 34764863)
118. Brewer BJ. Aging of the rotator cuff. Am J Sports Med. 1979;7:102-110. (Pubitemid 9154370)
119. Rothman RH, Parke WW. The vascular anatomy of the rotator cuff. Clin Orthop Relat Res. 1965;41:176-186.
120. Ronnemaa T, Juva K, Kulonen E. Effect of hyperlipidemic rat serum on the synthesis of collagen by chick embryo fibroblasts. Atherosclerosis. 1975;21:315-324.
121. Reddy GK. Glucose-mediated in vitro glycation modulates biomechanical integrity of the soft tissues but not hard tissues. J Orthop Res. 2003;21:738-743. (Pubitemid 36758219)
122. Reddy GK, Stehno-Bittel L, Enwemeka CS. Glycationinduced matrix stability in the rabbit Achilles tendon. Arch Biochem Biophys. 2002;399:174-180. (Pubitemid 34848604)
123. Bai P, Phua K, Hardt T, et al. Glycation alters collagen fibril organization. Connect Tissue Res. 1992;28:1-12.
124. Longo UG, Franceschi F, Ruzzini L, et al. Higher fasting plasma glucose levels within the normoglycaemic range and rotator cuff tears. Br J Sports Med. 2009;43:284-287.
125. Tirosh A, Shai I, Tekes-Manova D, et al. Normal fasting plasma glucose levels and type 2 diabetes in young men. N Engl J Med. 2005;353:1454-1462. (Pubitemid 41400919)
126. Longo UG, Lamberti A, Maffulli N, et al. Tissue engineered biological augmentation for tendon healing: a systematic review. Br Med Bull. 2010 Sep. 17. [Epub ahead of print]. PMID:20851817.
127. Longo UG, Lamberti A, Maffulli N, et al. Tendon augmentation grafts: a systematic review. Br Med Bull. 2010;94:165-188.
128. Castricini R, Longo UG, De Benedetto M, et al. Platelet-Rich Plasma Augmentation for Arthroscopic Rotator Cuff Repair: A Randomized Controlled Trial. Am J Sports Med. 2011;39:258-265.
129. Forriol F, Longo UG, Concejo C, et al. Platelet-rich plasma, rhOP-1 (rhBMP-7) and frozen rib allograft for the reconstruction of bony mandibular defects in sheep. A pilot experimental study. Injury. 2009;40(Suppl 3):S44-S49.
130. Lippi G, Longo UG, Maffulli N. Genetics and sports. Br Med Bull. 2010;93:27-47.
131. Franceschi F, Longo UG, Ruzzini L, et al. Arthroscopic management of calcific tendinitis of the subscapularis tendon. Knee Surg Sports Traumatol Arthrosc. 2007;15:1482-1485.
132. Franceschi F, Ruzzini L, Longo UG, et al. Equivalent clinical results of arthroscopic single-row and double-row suture anchor repair for rotator cuff tears: a randomized controlled trial. Am J Sports Med. 2007;35:1254-1260. (Pubitemid 47084206)
133. Franceschi F, Longo UG, Ruzzini L, et al. The Roman Bridge: a "double pulley-suture bridges" technique for rotator cuff repair. BMC Musculoskelet Disord. 2007;8:123.
134. Franceschi F, Longo UG, Ruzzini L, et al. No advantages in repairing a type II superior labrum anterior and posterior (SLAP) lesion when associated with rotator cuff repair in patients over age 50: a randomized controlled trial. Am J Sports Med. 2008;36:247-253.
135. Franceschi F, Longo UG, Ruzzini L, et al. Soft tissue tenodesis of the long head of the biceps tendon associated to the Roman Bridge repair. BMC Musculoskelet Disord. 2008;9:78.
136. Longo UG, Franceschi F, Spiezia F, et al. The low-profile Roman bridge technique for knotless double-row repair of the rotator cuff. Arch Orthop Trauma Surg. 2011;131:357-361.
137. Ames PR, Longo UG, Denaro V, et al. Achilles tendon problems: not just an orthopaedic issue. Disabil Rehabil. 2008;30:1646-1650.
138. Longo UG, Ronga M, Maffulli N. Acute ruptures of the achilles tendon. Sports Med Arthrosc. 2009;17:127-138.
139. Denaro V, Ruzzini L, Longo UG, et al. Effect of dihydrotestosterone on cultured human tenocytes from intact supraspinatus tendon. Knee Surg Sports Traumatol Arthrosc. 2010;18:971-976.
140. Denaro V, Ruzzini L, Barnaba SA, et al. Effect of pulsed electromagnetic fields on human tenocyte cultures from supraspinatus and quadriceps tendons. Am J Phys Med Rehabil. 2011;90:119-127.
141. Franceschi F, Longo UG, Ruzzini L, et al. Circulating substance P levels and shoulder joint contracture after arthroscopic repair of the rotator cuff. Br J Sports Med. 2008;42:742-745.
142. Khanna A, Friel M, Gougoulias N, et al. Prevention of adhesions in surgery of the flexor tendons of the hand: what is the evidence. Br Med Bull. 2009;90:85-109.
143. Knobloch K, Schreibmueller L, Longo UG, et al. Eccentric exercises for the management of tendinopathy of the main body of the Achilles tendon with or without an AirHeel Brace. A randomized controlled trial. B: Effects of compliance. Disabil Rehabil. 2008;30:1692-1696.
144. Longo UG, Oliva F, Olivia F, et al. Oxygen species and overuse tendinopathy in athletes. Disabil Rehabil. 2008;30:1563-1571.
145. Longo UG, Rittweger J, Garau G, et al. No influence of age, gender, weight, height, and impact profile in achilles tendinopathy in masters track and field athletes. Am J Sports Med. 2009;37:1400-1405.
146. Longo UG, Fazio V, Poeta ML, et al. Bilateral consecutive rupture of the quadriceps tendon in a man with BstUI polymorphism of the COL5A1 gene. Knee Surg Sports Traumatol Arthrosc. 2010;18:514-518.
147. Longo UG, Rittweger J, Garau G, et al. Patellar tendinopathy in master track and field athletes: influence of impact profile, weight, height, age and gender. Knee Surg Sports Traumatol Arthrosc. 2011;19:508-512.
148. Longo UG, Forriol F, Campi S, et al. Animal models for translational research on shoulder pathologies: from bench to bedside. Sports Med Arthrosc. 2011. In press.
149. Longo UG, Berton A, Alexander S, et al. Biological resurfacing for early osteoarthritis of the shoudler. Sports Med Arthrosc. 2011. In press.
150. Maffulli N, Longo UG. Conservative management for tendinopathy: is there enough scientific evidence. Rheumatology (Oxford). 2008;47:390-391.
151. Maffulli N, Longo UG. How do eccentric exercises work in tendinopathy. Rheumatology (Oxford). 2008;47:1444-1445.
152. Maffulli N, Longo UG, Maffulli GD, et al. Marked pathological changes proximal and distal to the site of rupture in acute Achilles tendon ruptures. Knee Surg Sports Traumatol Arthrosc. 2011;19:680-687.
153. Maffulli N, Longo UG, Denaro V. Novel approaches for the management of tendinopathy. J Bone Joint Surg Am. 2010;92:2604-2613.
154. Franceschi F, Longo UG, Ruzzini L, et al. Arthroscopic salvage of failed arthroscopic Bankart repair: a prospective study with a minimum follow-up of 4 years. Am J Sports Med. 2008;36:1330-1336. (Pubitemid 352000004)