Muscle degeneration in rotator cuff tears

Journal of Shoulder and Elbow Surgery

Volumn 21, Issue 2, 2012, Pages 164-174

  Laron, Dominique ^a   Samagh, Sanjum P ^a   Liu, Xuhui ^b   Kim, Hubert T ^a,b   Feeley, Brian T ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Fatty infiltration; Muscle atrophy; Review Article; Rotator cuff tear

Indexed keywords

ATROGIN 1; COLLAGENASE 3; GELATINASE A; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INITIATION FACTOR 4G; MAMMALIAN TARGET OF RAPAMYCIN; MUSCLE RING FINGER 1 PROTEIN; PROTEIN KINASE B; SOMATOMEDIN C; TRANSCRIPTION FACTOR FKHR; TRANSFORMING GROWTH FACTOR BETA;

ACROMIOHUMERAL INTERVAL; ACROMION; CELL STRUCTURE; DAILY LIFE ACTIVITY; DENERVATION; DISEASE ASSOCIATION; DISEASE SEVERITY; DOWN REGULATION; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; EXTRACELLULAR MATRIX; FIBROBLAST; HUMAN; HUMERUS HEAD; INFRASPINATUS MUSCLE; JOINT EFFUSION; MOLECULAR PATHOLOGY; MUSCLE ATROPHY; MUSCLE CELL; MUSCULOSKELETAL SYSTEM PARAMETERS; MYOFIBROBLAST; MYOFIBROSIS; NERVE INJURY; NONHUMAN; PRIORITY JOURNAL; PROADIPOCYTE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REVIEW; ROTATOR CUFF RUPTURE; SHOULDER; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SOLEUS MUSCLE; STEM CELL; SUPRASCAPULAR NERVE INJURY; SUPRASPINATUS MUSCLE; SYNOVIAL FLUID; TENDON; UPREGULATION; VASCULAR ENDOTHELIUM;

ADIPOSE TISSUE; ANIMALS; CYTOSKELETAL PROTEINS; FEMALE; HUMANS; INJURY SEVERITY SCORE; MAGNETIC RESONANCE IMAGING; MALE; MUSCULAR ATROPHY; PROGNOSIS; RISK FACTORS; ROTATOR CUFF; TENDON INJURIES;

EID: 84862966205     PISSN: 10582746     EISSN: 15326500     Source Type: Journal    
DOI: 10.1016/j.jse.2011.09.027     Document Type: Review

References (94)

1. Agata N., Sasai N., Inoue-Miyazu M., Kawakami K., Hayakawa K., Kobayashi K., et al. Repetitive stretch suppresses denervation-induced atrophy of soleus muscle in rats. Muscle Nerve 2009, 39:456-462. 10.1002/mus.21103.
2. Aitken K.J., Block G., Lorenzo A., Herz D., Sabha N., Dessouki O., et al. Mechanotransduction of extracellular signal-regulated kinases 1 and 2 mitogen-activated protein kinase activity in smooth muscle is dependent on the extracellular matrix and regulated by matrix metalloproteinases. Am J Pathol 2006, 169:459-470. 10.2353/ajpath.2006.050969.
3. Albritton M.J., Graham R.D., Richards R.S., Basamania C.J. An anatomic study of the effects on the suprascapular nerve due to retraction of the supraspinatus muscle after a rotator cuff tear. J Shoulder Elbow Surg 2003, 12:497-500. 10.1016/S1058274603001824.
4. Bedi A., Kovacevic D., Hettrich C., Gulotta L.V., Ehteshami J.R., Warren R.F., et al. The effect of matrix metalloproteinase inhibition on tendon-to-bone healing in a rotator cuff repair model. J Shoulder Elbow Surg 2010, 19:384-391. 10.1016/j.jse.2009.07.010.
5. Berry H., Kong K., Hudson A.R., Moulton R.J. Isolated suprascapular nerve palsy: a review of nine cases. Can J Neurol Sci 1995, 22:301-304.
6. Bey M.J., Ramsey M.L., Soslowsky L.J. Intratendinous strain fields of the supraspinatus tendon: effect of a surgically created articular-surface rotator cuff tear. J Shoulder Elbow Surg 2002, 11:562-569. 10.1067/mse.2002.126767.
7. Bodine S.C. mTOR signaling and the molecular adaptation to resistance exercise. Med Sci Sports Exerc 2006, 38:1950-1957. 10.1249/01.mss.0000233797.24035.35.
8. Bodine S.C., Stitt T.N., Gonzalez M., Kline W.O., Stover G.L., Bauerlein R., et al. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy invivo. Nat Cell Biol 2001, 3:1014-1019.
9. Boykin R.E., Friedman D.J., Higgins L.D., Warner J.J. Suprascapular neuropathy. J Bone Joint Surg Am 2010, 92:2348-2364. 10.2106/JBJS.I.01743.
10. Boykin R.E., Friedman D.J., Zimmer Z.R., Oaklander A.L., Higgins L.D., Warner J.J. Suprascapular neuropathy in a shoulder referral practice. J Shoulder Elbow Surg 2011, 20:983-988. 10.1016/j.jse.2010.10.039.
11. Brack A.S., Conboy M.J., Roy S., Lee M., Kuo C.J., Keller C., et al. Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 2007, 317:807-810. 10.1126/science.1144090.
12. Buckingham M., Montarras D. Skeletal muscle stem cells. Curr Opin Genet Dev 2008, 18:330-336. 10.1016/j.gde.2008.06.005.
13. Burkhart S.S. Arthroscopic treatment of massive rotator cuff tears. Clin Orthop Relat Res 2001, 390:107-118.
14. Burkhart S.S., Barth J.R., Richards D.P., Zlatkin M.B., Larsen M. Arthroscopic repair of massive rotator cuff tears with stage 3 and 4 fatty degeneration. Arthroscopy 2007, 23:347-354. 10.1016/j.arthro.2006.12.012.
15. Burkhart S.S., Danaceau S.M., Pearce C.E. Arthroscopic rotator cuff repair: analysis of results by tear size and by repair technique-margin convergence versus direct tendon-to-bone repair. Arthroscopy 2001, 17:905-912.
16. Caplan A.I., Correa D. The MSC: an injury drugstore. Cell Stem Cell 2011, 9:11-15. 10.1016/j.stem.2011.06.008.
17. Cencetti F., Bernacchioni C., Nincheri P., Donati C., Bruni P. Transforming growth factor-beta1 induces transdifferentiation of myoblasts into myofibroblasts via up-regulation of sphingosine kinase-1/S1P3 axis. Mol Biol Cell 2010, 21:1111-1124. 10.1091/mbc.E09-09-0812.
18. Chan Y.S., Li Y., Foster W., Horaguchi T., Somogyi G., Fu F.H., et al. Antifibrotic effects of suramin in injured skeletal muscle after laceration. J Appl Physiol 2003, 95:771-780. 10.1152/japplphysiol.00915.2002.
19. Chen X., Li Y. Role of matrix metalloproteinases in skeletal muscle: migration, differentiation, regeneration and fibrosis. Cell Adh Migr 2009, 3:337-341.
20. Cheung S., Dillon E., Tham S.C., Feeley B.T., Link T.M., Steinbach L., et al. The presence of fatty infiltration in the infraspinatus: its relation with the condition of the supraspinatus tendon. Arthroscopy 2011, 27:463-470. 10.1016/j.arthro.2010.09.014.
21. Choi H.R., Kondo S., Hirose K., Ishiguro N., Hasegawa Y., Iwata H. Expression and enzymatic activity of MMP-2 during healing process of the acute supraspinatus tendon tear in rabbits. J Orthop Res 2002, 20:927-933. 10.1016/S0736-0266(02)00016-5.
22. Cofield R.H., Parvizi J., Hoffmeyer P.J., Lanzer W.L., Ilstrup D.M., Rowland C.M. Surgical repair of chronic rotator cuff tears. A prospective long-term study. J Bone Joint Surg Am 2001, 83:71-77.
23. Collins D.N., Harryman D.T. Arthroplasty for arthritis and rotator cuff deficiency. Orthop Clin North Am 1997, 28:225-239.
24. Constantin D., Constantin-Teodosiu D., Layfield R., Tsintzas K., Bennett A.J., Greenhaff P.L. PPARdelta agonism induces a change in fuel metabolism and activation of an atrophy programme, but does not impair mitochondrial function in rat skeletal muscle. J Physiol 2007, 583:381-390. 10.1113/jphysiol.2007.135459.
25. Costouros J.G., Porramatikul M., Lie D.T., Warner J.J. Reversal of suprascapular neuropathy following arthroscopic repair of massive supraspinatus and infraspinatus rotator cuff tears. Arthroscopy 2007, 23:1152-1161. 10.1016/j.arthro.2007.06.014.
26. Csete M., Walikonis J., Slawny N., Wei Y., Korsnes S., Doyle J.C., et al. Oxygen-mediated regulation of skeletal muscle satellite cell proliferation and adipogenesis in culture. J Cell Physiol 2001, 189:189-196.
27. Cummins C.A., Messer T.M., Nuber G.W. Suprascapular nerve entrapment. J Bone Joint Surg Am 2000, 82:415-424.
28. Dogra C., Changotra H., Wergedal J.E., Kumar A. Regulation of phosphatidylinositol 3-kinase (PI3K)/Akt and nuclear factor-kappa B signaling pathways in dystrophin-deficient skeletal muscle in response to mechanical stretch. J Cell Physiol 2006, 208:575-585. 10.1002/jcp.20696.
29. Dreyer H.C., Glynn E.L., Lujan H.L., Fry C.S., DiCarlo S.E., Rasmussen B.B. Chronic paraplegia-induced muscle atrophy downregulates the mTOR/S6K1 signaling pathway. J Appl Physiol 2008, 104:27-33. 10.1152/japplphysiol.00736.2007.
30. Ecklund K.J., Lee T.Q., Tibone J., Gupta R. Rotator cuff tear arthropathy. J Am Acad Orthop Surg 2007, 15:340-349.
31. Edstrom E., Altun M., Hagglund M., Ulfhake B. Atrogin-1/MAFbx and MuRF1 are downregulated in aging-related loss of skeletal muscle. J Gerontol A Biol Sci Med Sci 2006, 61:663-674.
32. Fabis J., Danilewicz M., Omulecka A. Rabbit supraspinatus tendon detachment: effects of size and time after tenotomy on morphometric changes in the muscle. Acta Orthop Scand 2001, 72:282-286.
33. Feeley B.T., Gallo R.A., Craig E.V. Cuff tear arthropathy: current trends in diagnosis and surgical management. J Shoulder Elbow Surg 2009, 18:484-494. 10.1016/j.jse.2008.11.003.
34. Ferretti A., De Carli A., Fontana M. Injury of the suprascapular nerve at the spinoglenoid notch. The natural history of infraspinatus atrophy in volleyball players. Am J Sports Med 1998, 26:759-763.
35. Foletta V.C., White L.J., Larsen A.E., Leger B., Russell A.P. The role and regulation of MAFbx/atrogin-1 and MuRF1 in skeletal muscle atrophy. Pflugers Arch 2011, 461:325-335. 10.1007/s00424-010-0919-9.
36. Foster W., Li Y., Usas A., Somogyi G., Huard J. Gamma interferon as an antifibrosis agent in skeletal muscle. J Orthop Res 2003, 21:798-804. 10.1016/S0736-0266(03)00059-7.
37. Frey E., Regenfelder F., Sussmann P., Zumstein M., Gerber C., Born W., et al. Adipogenic and myogenic gene expression in rotator cuff muscle of the sheep after tendon tear. J Orthop Res 2009, 27:504-509. 10.1002/jor.20695.
38. Fukushima K., Badlani N., Usas A., Riano F., Fu F., Huard J. The use of an antifibrosis agent to improve muscle recovery after laceration. Am J Sports Med 2001, 29:394-402.
39. Gerber C., Meyer D.C., Frey E., von Rechenberg B., Hoppeler H., Frigg R., et al. Neer Award 2007: reversion of structural muscle changes caused by chronic rotator cuff tears using continuous musculotendinous traction. An experimental study in sheep. J Shoulder Elbow Surg 2009, 18:163-171. 10.1016/j.jse.2008.09.003.
40. Gerber C., Meyer D.C., Schneeberger A.G., Hoppeler H., von Rechenberg B. Effect of tendon release and delayed repair on the structure of the muscles of the rotator cuff: an experimental study in sheep. J Bone Joint Surg Am 2004, 86:1973-1982.
41. Gerber C., Walch G. Massive rotator cuff tears. Orthopaedic knowledge update. Shoulder and elbow 2001, 191-196. American Academy of Orthopaedic Surgeons, Rosemont (IL). T.R. Norris (Ed.).
42. Gladstone J.N., Bishop J.Y., Lo I.K., Flatow E.L. 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. 10.1177/0363546506297539.
43. Goutallier D., Postel J.M., Bernageau J., Lavau L., Voisin M.C. Fatty muscle degeneration in cuff ruptures. Pre- and postoperative evaluation by CT scan. Clin Orthop Relat Res 1994, 304:78-83.
44. Hosoyama T., Ishiguro N., Yamanouchi K., Nishihara M. Degenerative muscle fiber accelerates adipogenesis of intramuscular cells via RhoA signaling pathway. Differentiation 2009, 77:350-359. 10.1016/j.diff.2008.11.001.
45. Joe A.W., Yi L., Natarajan A., Le Grand F., So L., Wang J., et al. Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat Cell Bio 2010, 12:153-163. 10.1038/ncb2015.
46. Karalaki M., Fili S., Philippou A., Koutsilieris M. Muscle regeneration: cellular and molecular events. InVivo 2009, 23:779-796.
47. Kimura N., Kumamoto T., Oniki T., Nomura M., Nakamura K., Abe Y., et al. Role of ubiquitin-proteasome proteolysis in muscle fiber destruction in experimental chloroquine-induced myopathy. Muscle Nerve 2009, 39:521-528. 10.1002/mus.21223.
48. Kwon O., Tranter M., Jones W.K., Sankovic J.M., Banerjee R.K. Differential translocation of nuclear factor-kappaB in a cardiac muscle cell line under gravitational changes. J Biomech Eng 2009, 131:064503. 10.1115/1.3128718.
49. Lakemeier S., Braun J., Efe T., Foelsch C., Archontidou-Aprin E., Fuchs-Winkelmann S., et al. Expression of matrix metalloproteinases 1, 3, and 9 in differing extents of tendon retraction in the torn rotator cuff. Knee Surg Sports Traumatol Arthrosc 2011, 19:1760-1765. 10.1007/s00167-010-1367-y.
50. Lefterova M.I., Zhang Y., Steger D.J., Schupp M., Schug J., Cristancho A., et al. PPARgamma and C/EBP factors orchestrate adipocyte biology via adjacent binding on a genome-wide scale. Genes Dev 2008, 22:2941-2952. 10.1101/gad.1709008.
51. Leger B., Cartoni R., Praz M., Lamon S., Deriaz O., Crettenand A., et al. Akt signaling through GSK-3beta, mTOR, and Foxo1 is involved in human skeletal muscle hypertrophy and atrophy. J Physiol 2006, 576:923-933. 10.1113/jphysiol.2006.116715.
52. Leger B., Senese R., Al-Khodairy A.W., Deriaz O., Gobelet C., Giacobino J.P., et al. Atrogin-1, MuRF1, and FoXO, as well as phosphorylated GSK-3beta and 4E-BP1 are reduced in skeletal muscle of chronic spinal cord-injured patients. Muscle Nerve 2009, 40:69-78. 10.1002/mus.21293.
53. Li H., Malhotra S., Kumar A. Nuclear factor-kappa B signaling in skeletal muscle atrophy. J Mol Med (Berl) 2008, 86:1113-1126. 10.1007/s00109-008-0373-8.
54. Li Y., Fu F.H., Huard J. Cutting-edge muscle recovery: using antifibrosis agents to improve healing. Phys Sportsmed 2005, 33:44-50. 10.3810/psm.2005.05.91.
55. Liu X, Manzano G, Kim HT, Feeley BT. The role of mTOR in the development of muscle atrophy in a rat model of rotator cuff tears. Presented at the International Society of Arthroscopy, Knee Surgery & Orthopaedic Sports Medicine Annual Meeting, Rio de Janeiro, Brazil, May 15-19, 2011.
56. Liu X., Manzano G., Kim H.T., Feeley B.T. A rat model of massive rotator cuff tears. J Orthop Res 2011, 29:588-595. 10.1002/jor.21266.
57. Macaulay A.A., Greiwe R.M., Bigliani L.U. Rotator cuff deficient arthritis of the glenohumeral joint. Clin Orthop Surg 2010, 2:196-202. 10.4055/cios.2010.2.4.196.
58. Mallon W.J., Wilson R.J., Basamania C.J. The association of suprascapular neuropathy with massive rotator cuff tears: a preliminary report. J Shoulder Elbow Surg 2006, 15:395-398. 10.1016/j.jse.2005.10.019.
59. Mammucari C., Schiaffino S., Sandri M. Downstream of Akt: FoxO3 and mTOR in the regulation of autophagy in skeletal muscle. Autophagy 2008, 4:524-526.
60. Martin S.D., Warren R.F., Martin T.L., Kennedy K., O'Brien S.J., Wickiewicz T.L. Suprascapular neuropathy. Results of non-operative treatment. J Bone Joint Surg Am 1997, 79:1159-1165.
61. Matthews T.J., Hand G.C., Rees J.L., Athanasou N.A., Carr A.J. 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. 10.1302/0301-620X.88B4.16845.
62. Melis B., DeFranco M.J., Chuinard C., Walch G. Natural history of fatty infiltration and atrophy of the supraspinatus muscle in rotator cuff tears. Clin Orthop Relat Res 2010, 468:1498-1505. 10.1007/s11999-009-1207-x.
63. Meyer D.C., Hoppeler H., von Rechenberg B., Gerber C. A pathomechanical concept explains muscle loss and fatty muscular changes following surgical tendon release. J Orthop Res 2004, 22:1004-1007. 10.1016/j.orthres.2004.02.009.
64. Miyazaki M., Noguchi M., Takemasa T. Intermittent reloading attenuates muscle atrophy through modulating Akt/mTOR pathway. Med Sci Sports Exerc 2008, 40:848-855. 10.1249/MSS.0b013e318163275f.
65. Neal S., Fields K.B. Peripheral nerve entrapment and injury in the upper extremity. Am Fam Physician 2010, 81:147-155.
66. Neer C.S., Craig E.V., Fukuda H. Cuff-tear arthropathy. J Bone Joint Surg Am 1983, 65:1232-1244.
67. Nho S.J., Yadav H., Shindle M.K., Macgillivray J.D. Rotator cuff degeneration: etiology and pathogenesis. Am J Sports Med 2008, 36:987-993. 10.1177/0363546508317344.
68. Plancher K.D., Luke T.A., Peterson R.K., Yacoubian S.V. Posterior shoulder pain: a dynamic study of the spinoglenoid ligament and treatment with arthroscopic release of the scapular tunnel. Arthroscopy 2007, 23:991-998. 10.1016/j.arthro.2007.03.098.
69. Robbins S.L., Kumar V., Cotran R.S. Pathological basis of disease 2010, Elsevier, Philadelphia. 8th ed.
70. Rosen E.D. The transcriptional basis of adipocyte development. Prostaglandins Leukot Essent Fatty Acids 2005, 73:31-34. 10.1016/j.plefa.2005.04.004.
71. Rosen E.D., Sarraf P., Troy A.E., Bradwin G., Moore K., Milstone D.S., et al. PPAR gamma is required for the differentiation of adipose tissue invivo and invitro. Mol Cell 1999, 4:611-617.
72. Sartori R., Milan G., Patron M., Mammucari C., Blaauw B., Abraham R., et al. Smad2 and 3 transcription factors control muscle mass in adulthood. Am J Physiol Cell Physiol 2009, 296:C1248-C1257. 10.1152/ajpcell.00104.2009.
73. Saupe N., Pfirrmann C.W., Schmid M.R., Jost B., Werner C.M., Zanetti M. Association between rotator cuff abnormalities and reduced acromiohumeral distance. AJR Am J Roentgenol 2006, 187:376-382. 10.2214/AJR.05.0435.
74. Schmutz S., Fuchs T., Regenfelder F., Steinmann P., Zumstein M., Fuchs B. Expression of atrophy mRNA relates to tendon tear size in supraspinatus muscle. Clin Orthop Relat Res 2009, 467:457-464. 10.1007/s11999-008-0565-0.
75. Senf S.M., Dodd S.L., Judge A.R. FOXO signaling is required for disuse muscle atrophy and is directly regulated by Hsp70. Am J Physiol Cell Physiol 2010, 298:C38-C45. 10.1152/ajpcell.00315.2009.
76. Senf S.M., Dodd S.L., McClung J.M., Judge A.R. Hsp70 overexpression inhibits NF-kappaB and Foxo3a transcriptional activities and prevents skeletal muscle atrophy. FASEB J 2008, 22:3836-3845. 10.1096/fj.08-110163.
77. Shen P.H., Lien S.B., Shen H.C., Lee C.H., Wu S.S., Lin L.C. Long-term functional outcomes after repair of rotator cuff tears correlated with atrophy of the supraspinatus muscles on magnetic resonance images. J Shoulder Elbow Surg 2008, 17:1S-7S. 10.1016/j.jse.2007.04.014.
78. Sheppard D. Transforming growth factor beta: a central modulator of pulmonary and airway inflammation and fibrosis. Proc Am Thorac Soc 2006, 3:413-417. 10.1513/pats.200601-008AW.
79. Shi H., Scheffler J.M., Zeng C., Pleitner J.M., Hannon K.M., Grant A.L., et al. Mitogen-activated protein kinase signaling is necessary for the maintenance of skeletal muscle mass. Am J Physiol Cell Physiol 2009, 296:C1040-C1048. 10.1152/ajpcell.00475.2008.
80. Shi X., Garry D.J. Muscle stem cells in development, regeneration, and disease. Genes Dev 2006, 20:1692-1708. 10.1101/gad.1419406.
81. Shindle M.K., Chen C.C., Robertson C., Ditullio A.E., Paulus M.C., Clinton C.M., et al. Full-thickness supraspinatus tears are associated with more synovial inflammation and tissue degeneration than partial-thickness tears. J Shoulder Elbow Surg 2011, 20:917-927. 10.1016/j.jse.2011.02.015.
82. Skittone L.K., Liu X., Tseng A., Kim H.T. Matrix metalloproteinase-2 expression and promoter/enhancer activity in skeletal muscle atrophy. J Orthop Res 2008, 26:357-363. 10.1002/jor.20513.
83. Southgate R.J., Neill B., Prelovsek O., El-Osta A., Kamei Y., Miura S., et al. FOXO1 regulates the expression of 4E-BP1 and inhibits mTOR signaling in mammalian skeletal muscle. J Biol Chem 2007, 282:21176-21186. 10.1074/jbc.M702039200.
84. Tontonoz P., Spiegelman B.M. Fat and beyond: the diverse biology of PPARgamma. Annu Rev Biochem 2008, 77:289-312. 10.1146/annurev.biochem.77.061307.091829.
85. Visotsky J.L., Basamania C., Seebauer L., Rockwood C.A., Jensen K.L. Cuff tear arthropathy: pathogenesis, classification, and algorithm for treatment. J Bone Joint Surg Am 2004, 86(Suppl 2):35-40.
86. Warner J.P., Krushell R.J., Masquelet A., Gerber C. Anatomy and relationships of the suprascapular nerve: anatomical constraints to mobilization of the supraspinatus and infraspinatus muscles in the management of massive rotator-cuff tears. J Bone Joint Surg Am 1992, 74:36-45.
87. Wu Z., Xie Y., Bucher N.L., Farmer S.R. Conditional ectopic expression of C/EBP beta in NIH-3T3 cells induces PPAR gamma and stimulates adipogenesis. Genes Dev 1995, 9:2350-2363.
88. Yamaguchi K., Ditsios K., Middleton W.D., Hildebolt C.F., Galatz L.M., Teefey S.A. 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. 10.2106/JBJS.E.00835.
89. Yamamoto A., Takagishi K., Osawa T., Yanagawa T., Nakajima D., Shitara H., et al. Prevalence and risk factors of a rotator cuff tear in the general population. J Shoulder Elbow Surg 2010, 19:116-120. 10.1016/j.jse.2009.04.006.
90. Yan X., Chen Y.G. Smad7: not only a regulator, but also a cross-talk mediator of TGF-beta signalling. Biochem J 2011, 434:1-10. 10.1042/BJ20101827.
91. Yan X., Liu Z., Chen Y. Regulation of TGF-beta signaling by Smad7. Acta Biochim Biophys Sin (Shanghai) 2009, 41:263-272.
92. Zehetgruber H., Noske H., Lang T., Wurnig C. Suprascapular nerve entrapment. A meta-analysis. Int Orthop 2002, 26:339-343. 10.1007/s00264-002-0392-y.
93. Zeman C.A., Arcand M.A., Cantrell J.S., Skedros J.G., Burkhead W.Z. The rotator cuff-deficient arthritic shoulder: diagnosis and surgical management. J Am Acad Orthop Surg 1998, 6:337-348.
94. Zheng B., Ohkawa S., Li H., Roberts-Wilson T.K., Price S.R. FOXO3a mediates signaling crosstalk that coordinates ubiquitin and atrogin-1/MAFbx expression during glucocorticoid-induced skeletal muscle atrophy. FASEB J 2010, 24:2660-2669. 10.1096/fj.09-151480.