Architectural and Biochemical Adaptations in Skeletal Muscle and Bone Following Rotator Cuff Injury in a Rat Model

Overview

Journal J Bone Joint Surg Am

Specialties General Surgery
Orthopedics

Date 2015 Apr 3

PMID 25834081

Citations 9

Authors

Eugene J Sato

Megan L Killian

Anthony J Choi

Evie Lin

Alexander D Choo

Ana E Rodriguez-Soto

Chanteak T Lim

Stavros Thomopoulos

Leesa M Galatz

Samuel R Ward

Affiliations

Soon will be listed here.

Abstract

Background: Injury to the rotator cuff can cause irreversible changes to the structure and function of the associated muscles and bones. The temporal progression and pathomechanisms associated with these adaptations are unclear. The purpose of this study was to investigate the time course of structural muscle and osseous changes in a rat model of a massive rotator cuff tear.

Methods: Supraspinatus and infraspinatus muscle architecture and biochemistry and humeral and scapular morphological parameters were measured three days, eight weeks, and sixteen weeks after dual tenotomy with and without chemical paralysis via botulinum toxin A (BTX).

Results: Muscle mass and physiological cross-sectional area increased over time in the age-matched control animals, decreased over time in the tenotomy+BTX group, and remained nearly the same in the tenotomy-alone group. Tenotomy+BTX led to increased extracellular collagen in the muscle. Changes in scapular bone morphology were observed in both experimental groups, consistent with reductions in load transmission across the joint.

Conclusions: These data suggest that tenotomy alone interferes with normal age-related muscle growth. The addition of chemical paralysis yielded profound structural changes to the muscle and bone, potentially leading to impaired muscle function, increased muscle stiffness, and decreased bone strength.

Clinical Relevance: Structural musculoskeletal changes occur after tendon injury, and these changes are severely exacerbated with the addition of neuromuscular compromise.

Citing Articles

Geometric modeling predicts architectural adaptations are not responsible for the force deficit following tenotomy in the rotator cuff.

Meyer G J Biomech. 2022; 138:111105.

PMID: 35504146 PMC: 9652701. DOI: 10.1016/j.jbiomech.2022.111105.

Arthroscopy-Assisted Reduction and Internal Fixation versus Open Reduction and Internal Fixation for Glenoid Fracture with Scapular Involvement: A Retrospective Cohort Study.

Lin I, Lin T, Chang H, Lin C, Tsai C, Lo C J Clin Med. 2022; 11(4).

PMID: 35207402 PMC: 8875088. DOI: 10.3390/jcm11041131.

Orthopedic Interface Repair Strategies Based on Native Structural and Mechanical Features of the Multiscale Enthesis.

Locke R, Abraham A, Killian M ACS Biomater Sci Eng. 2020; 3(11):2633-2643.

PMID: 32832593 PMC: 7440099. DOI: 10.1021/acsbiomaterials.6b00599.

Partial-width injuries of the rat rotator cuff heal with fibrosis.

Lemmon E, Locke R, Szostek A, Ganji E, Killian M Connect Tissue Res. 2018; 59(5):437-446.

PMID: 29874950 PMC: 6324170. DOI: 10.1080/03008207.2018.1485666.

Impaired contractile function of the supraspinatus in the acute period following a rotator cuff tear.

Valencia A, Iyer S, Spangenburg E, Gilotra M, Lovering R BMC Musculoskelet Disord. 2017; 18(1):436.

PMID: 29121906 PMC: 5679320. DOI: 10.1186/s12891-017-1789-5.

References

Warren C, Krzesinski P, Greaser M . Vertical agarose gel electrophoresis and electroblotting of high-molecular-weight proteins. Electrophoresis. 2003; 24(11):1695-702. DOI: 10.1002/elps.200305392. View

Joshi S, Kim H, Feeley B, Liu X . Differential ubiquitin-proteasome and autophagy signaling following rotator cuff tears and suprascapular nerve injury. J Orthop Res. 2013; 32(1):138-44. PMC: 3856942. DOI: 10.1002/jor.22482. View

Galatz L, Ball C, Teefey S, Middleton W, Yamaguchi K . The outcome and repair integrity of completely arthroscopically repaired large and massive rotator cuff tears. J Bone Joint Surg Am. 2004; 86(2):219-24. DOI: 10.2106/00004623-200402000-00002. View

Killian M, Lim C, Thomopoulos S, Charlton N, Kim H, Galatz L . The effect of unloading on gene expression of healthy and injured rotator cuffs. J Orthop Res. 2013; 31(8):1240-8. PMC: 3690165. DOI: 10.1002/jor.22345. View

Samagh S, Kramer E, Melkus G, Laron D, Bodendorfer B, Natsuhara K . MRI quantification of fatty infiltration and muscle atrophy in a mouse model of rotator cuff tears. J Orthop Res. 2012; 31(3):421-6. DOI: 10.1002/jor.22233. View

Liu X, Joshi S, Samagh S, Dang Y, Laron D, Lovett D . Evaluation of Akt/mTOR activity in muscle atrophy after rotator cuff tears in a rat model. J Orthop Res. 2012; 30(9):1440-6. DOI: 10.1002/jor.22096. View

Kim H, Galatz L, Lim C, Havlioglu N, Thomopoulos S . The effect of tear size and nerve injury on rotator cuff muscle fatty degeneration in a rodent animal model. J Shoulder Elbow Surg. 2011; 21(7):847-58. PMC: 3217129. DOI: 10.1016/j.jse.2011.05.004. View

Liu X, Laron D, Natsuhara K, Manzano G, Kim H, Feeley B . A mouse model of massive rotator cuff tears. J Bone Joint Surg Am. 2012; 94(7):e41. DOI: 10.2106/JBJS.K.00620. View

Karsenty G, Ferron M . The contribution of bone to whole-organism physiology. Nature. 2012; 481(7381):314-20. PMC: 9047059. DOI: 10.1038/nature10763. View

10.

Mannava S, Plate J, Whitlock P, Callahan M, Seyler T, Koman L . Evaluation of in vivo rotator cuff muscle function after acute and chronic detachment of the supraspinatus tendon: an experimental study in an animal model. J Bone Joint Surg Am. 2011; 93(18):1702-11. DOI: 10.2106/JBJS.J.00184. View

11.

Meyer D, Gerber C, von Rechenberg B, Wirth S, Farshad M . Amplitude and strength of muscle contraction are reduced in experimental tears of the rotator cuff. Am J Sports Med. 2011; 39(7):1456-61. DOI: 10.1177/0363546510396305. View

12.

Winters T, Takahashi M, Lieber R, Ward S . Whole muscle length-tension relationships are accurately modeled as scaled sarcomeres in rabbit hindlimb muscles. J Biomech. 2010; 44(1):109-15. PMC: 3003754. DOI: 10.1016/j.jbiomech.2010.08.033. View

13.

Ward S, Sarver J, Eng C, Kwan A, Wurgler-Hauri C, Perry S . Plasticity of muscle architecture after supraspinatus tears. J Orthop Sports Phys Ther. 2010; 40(11):729-35. PMC: 4321894. DOI: 10.2519/jospt.2010.3279. View

14.

Tomioka T, Minagawa H, Kijima H, Yamamoto N, Abe H, Maesani M . Sarcomere length of torn rotator cuff muscle. J Shoulder Elbow Surg. 2009; 18(6):955-9. DOI: 10.1016/j.jse.2009.03.009. View

15.

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. 2008; 467(2):457-64. PMC: 2628494. DOI: 10.1007/s11999-008-0565-0. View

16.

Costouros J, Porramatikul M, Lie D, Warner J . Reversal of suprascapular neuropathy following arthroscopic repair of massive supraspinatus and infraspinatus rotator cuff tears. Arthroscopy. 2007; 23(11):1152-61. DOI: 10.1016/j.arthro.2007.06.014. View

17.

Gimbel J, Van Kleunen J, Lake S, Williams G, Soslowsky L . The role of repair tension on tendon to bone healing in an animal model of chronic rotator cuff tears. J Biomech. 2006; 40(3):561-8. DOI: 10.1016/j.jbiomech.2006.02.010. View

18.

Mallon W, Wilson R, Basamania C . The association of suprascapular neuropathy with massive rotator cuff tears: a preliminary report. J Shoulder Elbow Surg. 2006; 15(4):395-8. DOI: 10.1016/j.jse.2005.10.019. View

19.

Gerber C, Meyer D, Schneeberger A, 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(9):1973-82. DOI: 10.2106/00004623-200409000-00016. View

20.

Gimbel J, Mehta S, Van Kleunen J, Williams G, Soslowsky L . The tension required at repair to reappose the supraspinatus tendon to bone rapidly increases after injury. Clin Orthop Relat Res. 2004; (426):258-65. DOI: 10.1097/01.blo.0000136831.17696.80. View