Little knowledge exists about the healing process of the tendon to bone insertion, and hence little can be done to improve tissue healing. The goal of this study is to describe the healing of the supraspinatus tendon to its bony insertion under a variety of loading conditions. Tendons were surgically detached and repaired in rats. Rat shoulders were then immobilized, allowed cage activity, or exercised. Shoulders that were immobilized demonstrated superior structural (significantly higher collagen orientation), compositional (expression of extracellular matrix genes similar to the uninjured insertion), and quasilinear viscoelastic properties (A=0.30±0.10 MPa vs. 0.16±0.08 MPa, B=17.4±2.9 vs. 15.1±0.9, and vs. 233±40 s) compared to those that were exercised, contrary to expectations. With this knowledge of the healing response, treatment modalities for rotator cuff tears can be developed.
Issue Section:
Soft Tissue
1.
Kibler, B. W., 1997, “Rehabilitation of the Shoulder,” Orthopaedic Knowledge Update: Shoulder and Elbow, Norris, T. R., ed., American Academy of Orthopaedic Surgeons, pp. 289–298.
2.
Gelberman
, R. H.
, Woo
, S. L.
, Lothringer
, K.
, Akeson
, W. H.
, and Amiel
, D.
, 1982
, “Effects of Intermittent Passive Mobilization on Healing Canine Flexor Tendons
,” J. Hand Surg. [Am]
, 7
, pp. 170
–175
.3.
Gomez
, M.
, Woo
, S. L.
, Amiel
, D.
, Harwood
, F.
, Kitabayashi
, L.
, and Matyas
, J.
, 1991
, “The Effects of Increased Tension on Healing Medial Collateral Ligaments
,” Am. J. Sports Med.
, 19
, pp. 347
–354
.4.
Iannotti, J. P., Naranja, R. J., and Gartsman, G. M., 1994, “Surgical Treatment of the Intact Cuff and Repairable Cuff Defect: Arthroscopic and Open Techniques,” Orthopaedic Knowledge Update: Shoulder and Elbow, Norris, T. R., ed., Rosemont IL, American Academy of Orthopaedic Surgeons, pp. 151–156.
5.
Naranja, R. J., Iannotti, J. P., and Gartsman, G. M., 1994, “Complications in Rotator Cuff Surgery,” Orthopaedic Knowledge Update: Shoulder and Elbow, Norris, T. R., ed., Rosemont IL, American Academy of Orthopaedic Surgeons, pp. 157–166.
6.
Oguma
, H.
, Murakami
, G.
, Iwanaga
, H.
, Aoki
, M.
, and Ishii
, S.
, 2001
, “Early Anchoring Collagen Fibers at the Bone-Tendon Interface are Conducted by Woven Bone Formation: Light Microscope and Scanning Electron Microscope Observation Using a Canine Model
,” J. Orthop. Res.
, 19
, pp. 873
–880
.7.
Fujioka
, H.
, Thakur
, R.
, Wang
, G. J.
, Mizuno
, K.
, Balian
, G.
, and Hurwitz
, S. R.
, 1998
, “Comparison of Surgically Attached and Non-Attached Repair of the Rat Achilles Tendon-Bone Interface. Cellular Organization And Type X Collagen Expression
,” Connect. Tissue Res.
, 37
, pp. 205
–218
.8.
Liu
, S. H.
, Panossian
, V.
, Al-Shaikh
, R.
, Tomin
, E.
, Shepherd
, E.
, Finerman
, G. A.
, and Lane
, J. M.
, 1997
, “Morphology and Matrix Composition During Early Tendon to Bone Healing
,” Clin. Orthop. Relat. Res.
, 339
, pp. 253
–560
.9.
Rodeo
, S. A.
, Arnoczky
, S. P.
, Torzilli
, P. A.
, Hidaka
, C.
, and Warren
, R. F.
, 1993
, “Tendon Healing in a Bone Tunnel
,” J. Bone Jt. Surg.
, 74A
, pp. 1795
–1803
.10.
St. Pierre
, P.
, Olson
, E. J.
, Elliott
, J. J.
, O’Hair
, K. C.
, McKinney
, L. A.
, and Ryan
, J.
, 1995
, “Tendon Healing to Cortical Bone Compared With Healing to a Cancellous Trough
,” J. Bone Jt. Surg.
, 77A
, pp. 1858
–1866
.11.
Woo
, S. L.
, Gomez
, M. A.
, Sites
, T. J.
, Newton
, P. T.
, Orlando
, C. A.
, and Akeson
, W. H.
, 1987
, “The Biomechanical and Morphological Changes in the MCL of the Rabbit After Immobilization and Remobilization
,” J. Bone Jt. Surg.
, 69A
, pp. 1200
–1211
.12.
Woo
, S. L. Y.
, Gomez
, M. A.
, Amiel
, D.
, Ritter
, M. A.
, Gelberman
, R. H.
, and Akeson
, W. H.
, 1981
, “The Effects of Exercise on The Biomechanical and Biochemical Properties of Swine Digital Flexor Tendons
,” J. Biomech. Eng.
, 103
, pp. 51
–56
.13.
Kamps
, B. S.
, Linder
, L. H.
, DeCamp
, C. E.
, and Haut
, R. C.
, 1994
, “The Influence of Immobilization Versus Exercise on Scar Formation in the Rabbit Patellar Tendon After Excision of The Central One Third
,” Am. J. Sports Med.
, 22
, pp. 803
–811
.14.
Bray
, R. C.
, Shrive
, N. G.
, Frank
, C. B.
, and Chimich
, D. D.
, 1992
, “The Early Effects of Joint Immobilization On Medial Collateral Ligament Healing in an ACL-Deficient Knee: A Gross Anatomic and Biomechanical Investigation in the Adult Rabbit Model
,” J. Orthop. Res.
, 10
, pp. 157
–166
.15.
Fung, Y. C., 1972, “Stress-Strain-History Relations of Soft Tissues in Simple Elongation,” Biomechanics: Its Foundations And Objectives, Fung, Y. C., Perrone, N., and Anliker, M., eds., Prentice-Hall, San Diego, CA, pp. 181–208.
16.
Huang, C. Y., Wang, V. M., Roh, M. S., Pawluk, R. J., Flatow, E. L., and Mow, V. C., 1998, “Temperature Dependent Viscoelastic Properties of the Supraspinatus Tendon,” Advances in Bioengineering—American Society of Mechanical Engineering: Biomedical Engineering Division, 39, pp. 251–252.
17.
Kwan
, M. K.
, Lin
, T. H.
, and Woo
, S. L.
, 1993
, “On the Viscoelastic Properties of the Anteriomedial Bundle of the Anterior Cruciate Ligament
,” J. Biomech.
, 26
, pp. 447
–452
.18.
Woo
, S. L.
, Gomez
, M. A.
, and Akeson
, W. H.
, 1981
, “The Time and History Dependent Viscoelastic Properties of the Canine Medical Collateral Ligament
,” J. Biomech. Eng.
, 103
, pp. 293
–298
.19.
Sauren
, A. A. H. J.
, Hout
, M. C.
, Steenhoven
, A. A.
, Veldpaus
, F. E.
, and Janssen
, J. D.
, 1983
, “Mechanical Properties of Porcine Aortic Valve Tissues
,” J. Biomech.
, 16
, pp. 327
–338
.20.
Thomopoulos
, S.
, Hattersley
, G.
, Rosen
, V.
, Mertens
, M.
, Galatz
, L.
, Williams
, G. R.
, and Soslowsky
, L. J.
, 2002
, “The Localized Expression of Extracellular Matrix Components in Healing Tendon Insertion Sites: An In Situ Hybridization Study
,” J. Orthop. Res.
, 20
, pp. 454
–463
.21.
Uribe
, J. M.
, Stump
, C. S.
, Tipton
, C. M.
, and Fregosi
, R. F.
, 1992
, “Influence of Exercise Training on the Oxidative Capacity of Rat Abdominal Muscles
,” Respir. Physiol.
, 88
, pp. 171
–180
.22.
Wegner
, J. A.
, Lund
, D. D.
, Overton
, J. M.
, Edwards
, J. G.
, Oda
, R. P.
, and Tipton
, C. M.
, 1987
, “Select Cardiovascular and Metabolic Responses of Diabetic Rats to Moderate Exercise Training
,” Med. Sci. Sports Exercise
, 19
, pp. 497
–503
.23.
Soslowsky
, L. J.
, Thomopoulos
, S.
, Tun
, S.
, Flanagan
, C. L.
, Keefer
, C. C.
, Mastaw
, J.
, and Carpenter
, J. E.
, 2000
, “Overuse Activity Injures the Supraspinatus Tendon in an Animal Model. A Histologic and Biomechanical Study
,” J. Shoulder Elbow Surg.
, 9
, pp. 79
–84
.24.
Whittaker
, P.
, and Canham
, P. B.
, 1991
, “Demonstration of Quantitative Fabric Analysis of Tendon Collagen Using Two-Dimensional Polarized Light Microscopy
,” Matrix
, 11
, pp. 56
–62
.25.
Dickey
, J. P.
, Hewlett
, B. R.
, Dumas
, G. A.
, and Bednar
, D. A.
, 1998
, “Measuring Collagen Fiber Orientation: A Two Dimensional Quantitative Macroscopic Technique
,” J. Biomech. Eng.
, 120
, pp. 537
–540
.26.
Frank
, C.
, MacFarlane
, B.
, Edwards
, P.
, et al., 1991
, “A Quantitative Analysis of Matrix Alignment in Ligament Scars: A Comparison of Movement Versus Immobilization in an Immature Rabbit Model
,” J. Orthop. Res.
, 9
, pp. 219
–227
.27.
Bey
, M. J.
, Song
, H. K.
, Wehrli
, F. W.
, and Soslowsky
, L. J.
, 2001, “A Non-Contact, Non-Destructive Method for Quantifying Intratissue Strains,” J. Biomech. Eng., in press.28.
Nigul
, I.
, and Nigul
, U.
, 1987
, “On the Algorithms of Evaluation of Fung’s Relaxation Function Parameters
,” J. Biomech.
, 20
, pp. 343
–352
.29.
Woo, S. L. Y., An, K. N., Frank, C. B., et al., 2000, “Anatomy, Biology, And Biomechanics Of Tendon and Ligament,” Orthopaedic Basic Science, 2nd edition, Buckwalter, J. A., Einhorn, T. A., and Simon, S. R., eds., American Academy of Orthopaedic Surgeons, pp. 581–616.
30.
Bateman, J. F., Lamande, S. R., and Ramshaw, J. A., 1996, “Collagen Superfamily,” Extracellular Matrix, vol 2, Comper, W. D., ed., Amsterdam, Overseas Publishers Association, pp. 23–67.
31.
Sakai
, H.
, Koibuchi
, N.
, Ohtake
, H.
, Tamai
, K.
, et al., 2001
, “Type I and Type III Procollagen Gene Expressions in the Early Phase of Ligament Healing in Rabbits: An In Situ Hybridization Study
,” J. Orthop. Res.
, 19
, pp. 132
–135
.32.
Amiel
, D.
, Woo
, S. L.
, Harwoon
, F. L.
, and Akeson
, W. H.
, 1982
, “The Effect of Immobilization on Collagen Turnover in Connective Tissue: A Biochemical-Biomechanical Correlation
,” Acta Scandinavica Orthopaedica
, 53
, pp. 325
–332
.33.
Fosang, A. J. and Hardingham, T. E., 1996, “Matrix Proteoglycans,” Extracellular Matrix, vol 2, Comper, W. D., ed., Amsterdam, Overseas Publishers Association, pp. 201–229.
34.
Mankin, H. J., Mow, V. C., Buckwalter, J. A., Iannotti, J. P., and Ratcliffe, A., 2000, “Articular Cartilage Structure, Composition, and Function,” Orthopaedic Basic Science, 2nd edition, Buckwalter, J. A., Einhorn, T. A., and Simon, S. R., eds., American Academy of Orthopaedic Surgeons, pp. 443–470.
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