The effect of tear size and nerve injury on rotator cuff muscle fatty degeneration in a rodent animal model

Journal of Shoulder and Elbow Surgery

Volumn 21, Issue 7, 2012, Pages 847-858

  Kim, H Mike ^a   Galatz, Leesa M ^a   Lim, Chanteak ^a   Havlioglu, Necat ^b   Thomopoulos, Stavros ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b St Claire Hospital   (United States)

Author keywords

Adipogenesis; Basic science study; Laboratory study; Myogenesis; Neurotomy; Tendon; Tenotomy

Indexed keywords

ADIPOGENIC FACTOR; BIOLOGICAL MARKER; MYOGENIC FACTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; GENE EXPRESSION; HISTOPATHOLOGY; INFASPINATUS MUSCLE; MOUSE; MUSCLE ATROPHY; NERVE INJURY; NONHUMAN; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR UPREGULATION; RODENT; ROTATOR CUFF; ROTATOR CUFF MUSCLE FATTY DEGENERATION; ROTATOR CUFF RUPTURE; SHOULDER; SUPRASCAPULAR NERVE; SUPRASPINATUS MUSCLE; SURGICAL TECHNIQUE; TENOTOMY;

ADIPOSE TISSUE; ANIMALS; BIOPSY, NEEDLE; DISEASE MODELS, ANIMAL; IMMUNOHISTOCHEMISTRY; INJURY SEVERITY SCORE; MICE; MICE, TRANSGENIC; MUSCLE, SKELETAL; PERIPHERAL NERVE INJURIES; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; ROTATOR CUFF; SENSITIVITY AND SPECIFICITY; SPRAINS AND STRAINS; TENDON INJURIES; TENOTOMY;

EID: 84862638075     PISSN: 10582746     EISSN: 15326500     Source Type: Journal    
DOI: 10.1016/j.jse.2011.05.004     Document Type: Article

References (40)

1. Antoniou J., Tae S.K., Williams G.R., Bird S., Ramsey M.L., Iannotti J.P. Suprascapular neuropathy. Variability in the diagnosis, treatment, and outcome. Clin Orthop Relat Res 2001, 131-138.
2. Barton E.R., Gimbel J.A., Williams G.R., Soslowsky L.J. Rat supraspinatus muscle atrophy after tendon detachment. J Orthop Res 2005, 23:259-265. 10.1016/j.orthres.2004.08.018.
3. Carpenter J.E., Thomopoulos S., Flanagan C.L., DeBano C.M., Soslowsky L.J. Rotator cuff defect healing: a biomechanical and histologic analysis in an animal model. J Shoulder Elbow Surg 1998, 7:599-605.
4. Chen A.L., Ong B.C., Rose D.J. Arthroscopic management of spinoglenoid cysts associated with SLAP lesions and suprascapular neuropathy. Arthroscopy 2003, 19:E15-E21. doi:10.1016/S0749-8063(03)00381-5.
5. Coleman S.H., Fealy S., Ehteshami J.R., MacGillivray J.D., Altchek D.W., Warren R.F., et al. Chronic rotator cuff injury and repair model in sheep. J Bone Joint Surg Am 2003, 85:2391-2402.
6. 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.
7. Das R., Rich J., Kim H.M., McAlinden A., Thomopoulos S. Effects of botulinum toxin-induced paralysis on postnatal development of the supraspinatus muscle. J Orthop Res 2011, 29:281-288. doi:10.1002/jor.21234.
8. 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. doi:10.1002/jor.20695.
9. Fuchs B., Weishaupt D., Zanetti M., Hodler J., Gerber C. Fatty degeneration of the muscles of the rotator cuff: assessment by computed tomography versus magnetic resonance imaging. J Shoulder Elbow Surg 1999, 8:599-605.
10. Galatz L.M., Ball C.M., Teefey S.A., Middleton W.D., Yamaguchi K. The outcome and repair integrity of completely arthroscopically repaired large and massive rotator cuff tears. J Bone Joint Surg Am 2004, 86:219-224.
11. Gimbel J.A., Mehta S., Van Kleunen J.P., Williams G.R., Soslowsky L.J. The tension required at repair to reappose the supraspinatus tendon to bone rapidly increases after injury. Clin Orthop Relat Res 2004, 258-265. doi:10.1097/01.blo.0000136831.17696.80.
12. Gimbel J.A., Van Kleunen J.P., Mehta S., Perry S.M., Williams G.R., Soslowsky L.J. Supraspinatus tendon organizational and mechanical properties in a chronic rotator cuff tear animal model. J Biomech 2004, 37:739-749. 10.1016/j.jbiomech.2003.09.019.
13. 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, 78-83.
14. Harryman D.T., Mack L.A., Wang K.Y., Jackins S.E., Richardson M.L., Matsen F.A. Repairs of the rotator cuff. Correlation of functional results with integrity of the cuff. J Bone Joint Surg Am 1991, 73:982-989.
15. Iannotti J.P., Naranja R.J., Gartsman G.M. Surgical treatment of the ifact cuff and reparable cuff defect: Arthroscopic and open techniques. Orthopaedic knowledge update: shoulder and elbow 1994, 151-155. American Academy of Orthopaedic Surgeons, Rosemont, IL. T.R. Norris (Ed.).
16. Jiang B., Roy R.R., Edgerton V.R. Expression of a fast fiber enzyme profile in the cat soleus after spinalization. Muscle Nerve 1990, 13:1037-1049.
17. Kim H.M., Galatz L.M., Das R., Patel N., Thomopoulos S. Musculoskeletal deformities secondary to neurotomy of the superior trunk of the brachial plexus in neonatal mice. J Orthop Res 2010, 28:1391-1398. doi:10.1002/jor.21128.
18. Koike Y., Trudel G., Uhthoff H.K. Formation of a new enthesis after attachment of the supraspinatus tendon: A quantitative histologic study in rabbits. J Orthop Res 2005, 23:1433-1440. 10.1016/j.orthres.2005.02.015.
19. Koopman R., Schaart G., Hesselink M.K. Optimisation of oil red O staining permits combination with immunofluorescence and automated quantification of lipids. Histochem Cell Biol 2001, 116:63-68.
20. Malenfant P., Joanisse D.R., Theriault R., Goodpaster B.H., Kelley D.E., Simoneau J.A. Fat content in individual muscle fibers of lean and obese subjects. Int J Obes Relat Metab Disord 2001, 25:1316-1321.
21. 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.
22. McCluskey L., Feinberg D., Dolinskas C. Suprascapular neuropathy related to a glenohumeral joint cyst. Muscle Nerve 1999, 22:772-777.
23. Musacchia X.J., Steffen J.M., Fell R.D. Disuse atrophy of skeletal muscle: animal models. Exerc Sport Sci Rev 1988, 16:61-87.
24. Naranja R.J., Iannotti J.P., Gartsman G.M. Complications in rotator cuff surgery. Orthopaedic knowledge update: shoulder and elbow 1994, 157-166. American Academy of Orthopaedic Surgeons, Rosemont, IL. T.R. Norris (Ed.).
25. Ohira Y., Yoshinaga T., Nomura T., Kawano F., Ishihara A., Nonaka I., et al. Gravitational unloading effects on muscle fiber size, phenotype and myonuclear number. Adv Space Res 2002, 30:777-781. doi:S0273-1177(02)00395-2.
26. Reno C., Marchuk L., Sciore P., Frank C.B., Hart D.A. Rapid isolation of total RNA from small samples of hypocellular, dense connective tissues. Biotechniques 1997, 22:1082-1086.
27. Romeo A.A., Rotenberg D.D., Bach B.R. Suprascapular neuropathy. J Am Acad Orthop Surg 1999, 7:358-367.
28. Rowshan K., Hadley S., Pham K., Caiozzo V., Lee T.Q., Gupta R. Development of fatty atrophy after neurologic and rotator cuff injuries in an animal model of rotator cuff pathology. J Bone Joint Surg Am 2010, 92:2270-2278. doi:10.2106/JBJS.I.00812.
29. Rubino L.J., Stills H.F., Sprott D.C., Crosby L.A. Fatty infiltration of the torn rotator cuff worsens over time in a rabbit model. Arthroscopy 2007, 23:717-722. 10.1016/j.arthro.2007.01.023.
30. Safran O., Derwin K.A., Powell K., Iannotti J.P. Changes in rotator cuff muscle volume, fat content, and passive mechanics after chronic detachment in a canine model. J Bone Joint Surg Am 2005, 87:2662-2670. doi:10.2106/JBJS.D.02421.
31. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008, 3:1101-1108. doi:10.1038/nprot.2008.73.
32. Soslowsky L.J., Carpenter J.E., DeBano C.M., Banerji I., Moalli M.R. Development and use of an animal model for investigations on rotator cuff disease. J Shoulder Elbow Surg 1996, 5:383-392.
33. Soslowsky L.J., Thomopoulos S., Esmail A., Flanagan C.L., Iannotti J.P., Williamson J.D., et al. Rotator cuff tendinosis in an animal model: role of extrinsic and overuse factors. Ann Biomedi Eng 2002, 30:1057-1063. doi:10.1114/1.1509765.
34. Stein T.P., Wade C.E. Metabolic consequences of muscle disuse atrophy. J Nutr 2005, 135:1824S-1828S. doi:135/7/1824S.
35. Thomopoulos S., Hattersley G., Rosen V., Mertens M., Galatz L., Williams G.R., et al. The localized expression of extracellular matrix components in healing tendon insertion sites: an in situ hybridization study. J Orthop Res 2002, 20:454-463. doi:10.1016/S0736-0266(01)00144-9.
36. Thomopoulos S., Kim H.M., Rothermich S.Y., Biederstadt C., Das R., Galatz L.M. Decreased muscle loading delays maturation of the tendon enthesis during postnatal development. J Orthop Res 2007, 25:1154-1163. doi:10.1002/jor.20418.
37. Thomopoulos S., Williams G.R., Soslowsky L.J. Tendon to bone healing: differences in biomechanical, structural, and compositional properties due to a range of activity levels. J Biomech Eng 2003, 125:106-113. doi:10.1115/1.1536660.
38. Uhthoff H.K., Sano H., Trudel G., Ishii H. Early reactions after reimplantation of the tendon of supraspinatus into bone. A study in rabbits. J Bone Joint Surg Br 2000, 82:1072-1076.
39. Vitale M.A., Vitale M.G., Zivin J.G., Braman J.P., Bigliani L.U., Flatow E.L. Rotator cuff repair: an analysis of utility scores and cost-effectiveness. J Shoulder Elbow Surg 2007, 16:181-187. 10.1016/j.jse.2006.06.013.
40. Westerheide K.J., Dopirak R.M., Karzel R.P., Snyder S.J. Suprascapular nerve palsy secondary to spinoglenoid cysts: results of arthroscopic treatment. Arthroscopy 2006, 22:721-727. 10.1016/j.arthro.2006.03.019.