0
Research Papers

Strain Distribution of Intact Rat Rotator Cuff Tendon-to-Bone Attachments and Attachments With Defects

[+] Author and Article Information
Ryan C. Locke

Department of Biomedical Engineering,
University of Delaware,
5 Innovation Way,
Newark, DE 19716
e-mail: rlocke@udel.edu

John M. Peloquin

Department of Biomedical Engineering,
University of Delaware,
161 Colburn Lab 150 Academy Street,
Newark, DE 19716
e-mail: peloquin@udel.edu

Elisabeth A. Lemmon

Departments of Animal and Food Sciences
and Biomedical Engineering,
University of Delaware,
5 Innovation Way,
Newark, DE 19716
e-mail: blemmon@udel.edu

Adrianna Szostek

Departments of Animal and Food Sciences
and Biomedical Engineering,
University of Delaware,
5 Innovation Way,
Newark, DE 19716
e-mail: aszostek@udel.edu

Dawn M. Elliott

Mem. ASME
Department of Biomedical Engineering,
University of Delaware,
161 Colburn Lab 150 Academy Street,
Newark, DE 19716
e-mail: delliott@udel.edu

Megan L. Killian

Mem. ASME
Department of Biomedical Engineering,
University of Delaware,
5 Innovation Way,
Newark, DE 19716
e-mail: killianm@udel.edu

1Corresponding author.

Manuscript received August 14, 2017; final manuscript received September 14, 2017; published online October 16, 2017. Editor: Beth A. Winkelstein.

J Biomech Eng 139(11), 111007 (Oct 16, 2017) (6 pages) Paper No: BIO-17-1361; doi: 10.1115/1.4038111 History: Received August 14, 2017; Revised September 14, 2017

This study aimed to experimentally track the tissue-scale strains of the tendon–bone attachment with and without a localized defect. We hypothesized that attachments with a localized defect would develop strain concentrations and would be weaker than intact attachments. Uniaxial tensile tests and digital image correlation were performed on rat infraspinatus tendon-to-bone attachments with defects (defect group) and without defects (intact group). Biomechanical properties were calculated, and tissue-scale strain distributions were quantified for superior and inferior fibrous and calcified regions. At the macroscale, the defect group exhibited reduced stiffness (31.3±3.7 N/mm), reduced ultimate load (24.7±3.8 N), and reduced area under the curve at ultimate stress (3.7±1.5 J/m2) compared to intact attachments (42.4±4.3 N/mm, 39.3±3.7 N, and 5.6±1.4 J/m2, respectively). Transverse strain increased with increasing axial load in the fibrous region of the defect group but did not change for the intact group. Shear strain of the superior fibrous region was significantly higher in the defect group compared to intact group near yield load. This work experimentally identified that attachments may resist failure by distributing strain across the interface and that strain concentrations develop near attachment defects. By establishing the tissue-scale deformation patterns of the attachment, we gained insight into the micromechanical behavior of this interfacial tissue and bolstered our understanding of the deformation mechanisms associated with its ability to resist failure.

FIGURES IN THIS ARTICLE
<>
Copyright © 2017 by ASME
Your Session has timed out. Please sign back in to continue.

References

Thomopoulos, S. , Williams, G. R. , Gimbel, J. A. , Favata, M. , and Soslowsky, L. J. , 2003, “ Variation of Biomechanical, Structural, and Compositional Properties Along the Tendon to Bone Insertion Site,” J. Orthop. Res., 21(3), pp. 413–419. [CrossRef] [PubMed]
Szczesny, S. E. , and Elliott, D. M. , 2014, “ Interfibrillar Shear Stress Is the Loading Mechanism of Collagen Fibrils in Tendon,” Acta Biomater., 10(6), pp. 2582–2590. [CrossRef] [PubMed]
Lake, S. P. , Miller, K. S. , Elliott, D. M. , and Soslowsky, L. J. , 2009, “ Effect of Fiber Distribution and Realignment on the Nonlinear and Inhomogeneous Mechanical Properties of Human Supraspinatus Tendon Under Longitudinal Tensile Loading,” J. Orthop. Res., 27(12), pp. 1596–1602. [CrossRef] [PubMed]
Genin, G. M. , Kent, A. , Birman, V. , Wopenka, B. , Pasteris, J. D. , Marquez, P. J. , and Thomopoulos, S. , 2009, “ Functional Grading of Mineral and Collagen in the Attachment of Tendon to Bone,” Biophys. J., 97(4), pp. 976–985. [CrossRef] [PubMed]
Knese, K.-H. , and Biermann, H. , 1958, “ Die Knochenbildung an Sehnen Und Bandsätzen Im Bereich Ursprünglich Chondraler Apophysen,” Z. Zellforsch. Mikrosk. Anat., 49(2), pp. 142–187. [CrossRef] [PubMed]
Benjamin, M. , Toumi, H. , Ralphs, J. R. , Bydder, G. , Best, T. M. , and Milz, S. , 2006, “ Where Tendons and Ligaments Meet Bone: Attachment Sites (‘Entheses’) in Relation to Exercise and/or Mechanical Load,” J. Anat., 208(4), pp. 471–490. [CrossRef] [PubMed]
Fang, F. , and Lake, S. P. , 2016, “ Experimental Evaluation of Multiscale Tendon Mechanics,” J. Orthop. Res., 35(7), pp. 1353–1365. [CrossRef]
Deymier-Black, A. C. , Pasteris, J. D. , Genin, G. M. , and Thomopoulos, S. , 2015, “ Allometry of the Tendon Enthesis: Mechanisms of Load Transfer Between Tendon and Bone,” ASME J. Biomech. Eng., 137(11), p. 111005. [CrossRef]
Thomopoulos, S. , Marquez, J. P. , Weinberger, B. , Birman, V. , and Genin, G. M. , 2006, “ Collagen Fiber Orientation at the Tendon to Bone Insertion and Its Influence on Stress Concentrations,” J. Biomech., 39(10), pp. 1842–1851. [CrossRef] [PubMed]
Benjamin, M. , Kumai, T. , Milz, S. , Boszczyk, B. M. , Boszczyk, A. A. , and Ralphs, J. R. , 2002, “ The Skeletal Attachment of Tendons—Tendon ‘Entheses’,” Comp. Biochem. Physiol. A. Mol. Integr. Physiol., 133(4), pp. 931–945. [CrossRef] [PubMed]
Berenson, M. C. , Blevins, F. T. , Plaas, A. H. K. , and Vogel, K. G. , 1996, “ Proteoglycans of Human Rotator Cuff Tendons,” J. Orthop. Res., 14(4), pp. 518–525. [CrossRef] [PubMed]
Smith, L. J. , Deymier, A. C. , Boyle, J. J. , Li, Z. , Linderman, S. W. , Pasteris, J. D. , Xia, Y. , Genin, G. M. , and Thomopoulos, S. , 2016, “ Tunability of Collagen Matrix Mechanical Properties Via Multiple Modes of Mineralization,” Interface Focus, 6(1), p. 0070. [CrossRef]
Hu, Y. , Birman, V. , Demyier-Black, A. , Schwartz, A. G. , Thomopoulos, S. , and Genin, G. M. , 2015, “ Stochastic Interdigitation as a Toughening Mechanism at the Interface Between Tendon and Bone,” Biophys. J., 108(2), pp. 431–437. [CrossRef] [PubMed]
Deymier, A. C. , An, Y. , Boyle, J. J. , Schwartz, A. G. , Birman, V. , Genin, G. M. , Thomopoulos, S. , and Barber, A. H. , 2017, “ Micro-Mechanical Properties of the Tendon-to-Bone Attachment,” Acta Biomater., 56(1), pp. 25–35. [CrossRef] [PubMed]
Rossetti, L. , Kuntz, L. A. , Kunold, E. , Schock, J. , Müller, K. W. , Grabmayr, H. , Stolberg-Stolberg, J. , Pfeiffer, F. , Sieber, S. A. , Burgkart, R. , and Bausch, A. R. , 2017, “ The Microstructure and Micromechanics of the Tendon–Bone Insertion,” Nat. Mater., 16, pp. 664–670. [CrossRef] [PubMed]
Connizzo, B. K. , Adams, S. M. , Adams, T. H. , Jawad, A. F. , Birk, D. E. , and Soslowsky, L. J. , 2016, “ Multiscale Regression Modeling in Mouse Supraspinatus Tendons Reveals That Dynamic Processes Act as Mediators in Structure–Function Relationships,” J. Biomech., 49(9), pp. 1649–1657. [CrossRef] [PubMed]
Moffat, K. L. , Sun, W.-H. S. , Pena, P. E. , Chahine, N. O. , Doty, S. B. , Ateshian, G. A. , Hung, C. T. , and Lu, H. H. , 2008, “ Characterization of the Structure–Function Relationship at the Ligament-to-Bone Interface,” Proc. Natl. Acad. Sci., 105(23), pp. 7947–7952. [CrossRef]
Liu, Y. X. , Thomopoulos, S. , Birman, V. , Li, J.-S. , and Genin, G. M. , 2012, “ Bi-Material Attachment Through a Compliant Interfacial System at the Tendon-to-Bone Insertion Site,” Mech. Mater. Int. J., 44, pp. 83–92. [CrossRef]
Wopenka, B. , Kent, A. , Pasteris, J. D. , Yoon, Y. , and Thomopoulos, S. , 2008, “ The Tendon-to-Bone Transition of the Rotator Cuff: A Preliminary Raman Spectroscopic Study Documenting the Gradual Mineralization Across the Insertion in Rat Tissue Samples,” Appl. Spectrosc., 62(12), pp. 1285–1294. [CrossRef] [PubMed]
Galatz, L. M. , Ball, C. M. , Teefey, S. A. , Middleton, W. D. , and Yamaguchi, K. , 2004, “ The Outcome and Repair Integrity of Completely Arthroscopically Repaired Large and Massive Rotator Cuff Tears,” J Bone Jt. Surg. Am., 86(2), pp. 219–224. [CrossRef]
Kim, H. M. , Dahiya, N. , Teefey, S. A. , Middleton, W. D. , Stobbs, G. , Steger-May, K. , Yamaguchi, K. , and Keener, J. D. , 2010, “ Location and Initiation of Degenerative Rotator Cuff Tears,” J. Bone Joint Surg. Am., 92(5), pp. 1088–1096. [CrossRef] [PubMed]
Kim, H. M. , 2010, “ Relationship of Tear Size and Location to Fatty Degeneration of the Rotator Cuff,” J. Bone Jt. Surg. Am., 92(4), p. 829. [CrossRef]
Lehman, C. , Cuomo, F. , Kummer, F. J. , and Zuckerman, J. D. , 1995, “ The Incidence of Full Thickness Rotator Cuff Tears in a Large Cadaveric Population,” Bull. Hosp. Jt. Dis., 54(1), pp. 30–31. [PubMed]
Elia, F. , Azoulay, V. , Lebon, J. , Faraud, A. , Bonnevialle, N. , and Mansat, P. , 2017, “ Clinical and Anatomic Results of Surgical Repair of Chronic Rotator Cuff Tears at Ten-Year Minimum Follow-Up,” Int. Ortho, 41(6), pp. 1–8. [CrossRef]
Thomopoulos, S. , Williams, G. R. , and Soslowsky, L. J. , 2003, “ Tendon to Bone Healing: Differences in Biomechanical, Structural, and Compositional Properties Due to a Range of Activity Levels,” ASME J. Biomech. Eng., 125(1), pp. 106–113. [CrossRef]
Andarawis-Puri, N. , Ricchetti, E. T. , and Soslowsky, L. J. , 2009, “ Rotator Cuff Tendon Strain Correlates With Tear Propagation,” J. Biomech., 42(2), pp. 158–163. [CrossRef] [PubMed]
Bey, M. J. , Ramsey, M. L. , and Soslowsky, L. J. , 2002, “ Intratendinous Strain Fields of the Supraspinatus Tendon: Effect of a Surgically Created Articular-Surface Rotator Cuff Tear,” J. Shoulder Elbow Surg., 11(6), pp. 562–569. [CrossRef] [PubMed]
Andarawis-Puri, N. , Ricchetti, E. T. , and Soslowsky, L. J. , 2009, “ Interaction Between the Supraspinatus and Infraspinatus Tendons: Effect of Anterior Supraspinatus Tendon Full-Thickness Tears on Infraspinatus Tendon Strain,” Am. J. Sports Med., 37(9), pp. 1831–1839. [CrossRef] [PubMed]
Andarawis-Puri, N. , Kuntz, A. F. , Ramsey, M. L. , and Soslowsky, L. J. , 2010, “ Effect of Glenohumeral Abduction Angle on the Mechanical Interaction Between the Supraspinatus and Infraspinatus Tendons for the Intact, Partial-Thickness Torn, and Repaired Supraspinatus Tendon Conditions,” J. Orthop. Res., 28(7), pp. 846–851. [PubMed]
Andarawis-Puri, N. , Kuntz, A. F. , Kim, S.-Y. , and Soslowsky, L. J. , 2010, “ Effect of Anterior Supraspinatus Tendon Partial-Thickness Tears on Infraspinatus Tendon Strain Through a Range of Joint Rotation Angles,” J. Shoulder Elbow Surg., 19(4), pp. 617–623. [CrossRef] [PubMed]
Miller, R. M. , Fujimaki, Y. , Araki, D. , Musahl, V. , and Debski, R. E. , 2014, “ Strain Distribution Due to Propagation of Tears in the Anterior Supraspinatus Tendon,” J. Orthop. Res., 32(10), pp. 1283–1289. [CrossRef] [PubMed]
Reilly, P. , Amis, A. A. , Wallace, A. L. , and Emery, R. J. H. , 2003, “ Supraspinatus Tears: Propagation and Strain Alteration,” J. Shoulder Elbow Surg., 12(2), pp. 134–138. [CrossRef] [PubMed]
Schindelin, J. , Arganda-Carreras, I. , Frise, E. , Kaynig, V. , Longair, M. , Pietzsch, T. , Preibisch, S. , Rueden, C. , Saalfeld, S. , Schmid, B. , Tinevez, J.-Y. , White, D. J. , Hartenstein, V. , Eliceiri, K. , Tomancak, P. , and Cardona, A. , 2012, “ Fiji: An Open-Source Platform for Biological-Image Analysis,” Nat. Methods, 9(7), pp. 676–682. [CrossRef] [PubMed]
Bey, M. J. , Song, H. K. , Wehrli, F. W. , and Soslowsky, L. J. , 2002, “ Intratendinous Strain Fields of the Intact Supraspinatus Tendon: The Effect of Glenohumeral Joint Position and Tendon Region,” J. Orthop. Res., 20(4), pp. 869–874. [CrossRef] [PubMed]
Peloquin, J. M. , Santare, M. H. , and Elliott, D. M. , 2016, “ Advances in Quantification of Meniscus Tensile Mechanics Including Nonlinearity, Yield, and Failure,” ASME J. Biomech. Eng., 138(2), p. 021002. [CrossRef]
Carpenter, J. E. , Thomopoulos, S. , Flanagan, C. L. , DeBano, C. M. , and Soslowsky, L. J. , 1998, “ Rotator Cuff Defect Healing: A Biomechanical and Histologic Analysis in an Animal Model,” J. Shoulder Elbow Surg., 7(6), pp. 599–605. [CrossRef] [PubMed]
Galatz, L. M. , Charlton, N. , Das, R. , Kim, H. M. , Havlioglu, N. , and Thomopoulos, S. , 2009, “ Complete Removal of Load Is Detrimental to Rotator Cuff Healing,” J. Shoulder Elbow Surg., 18(5), pp. 669–675. [CrossRef] [PubMed]

Figures

Grahic Jump Location
Fig. 2

Biomechanical strength and AUC at ultimate stress decreased in tendon-to-bone attachments with defects. Structural properties of (a) ultimate load and (b) stiffness significantly decreased in the defect group compared to the intact group. (c) AUC at ultimate stress significantly decreased in the defect group, while other material properties of (d)–(f) Young’s modulus, strain at ultimate stress, and ultimate stress were not significantly different between groups. Black lines indicate significant difference (p < 0.05); data shown are mean ±95% confidence intervals.

Grahic Jump Location
Fig. 3

Near yield load, tissue-scale strain was heterogeneous and concentrated at attachment defects. Representative strain fields for (a), (c), and (e) intact and (b), (d), and (f) defect attachments are shown. Longitudinal (εxx; (a) and (b)), transverse (εyy; (c) and (d)), and shear (εxy; (e) and (f)) strain fields were generated near yield load. Strain magnitude is represented by the colored scale bars. Images shown are representative for each group. Coordinates for measured strain are shown in panel C. (a) and (b) T, tendon; B, bone. (b), (d), and (f) The defect is marked with a dashed white circle.

Grahic Jump Location
Fig. 4

Near yield load, transverse and shear strain were concentrated in the fibrous region of attachments with defects. Average Median tissue-scale (a) longitudinal strain (εxx), (b) transverse strain (εyy), and (c) shear strain (εxy) were compared between intact and defect groups for the fibrous and calcified regions of tendon-to-bone attachments. Black lines indicate significant difference (p < 0.05). Data shown are average median strain ±95% confidence intervals.

Grahic Jump Location
Fig. 5

Near yield, shear strain localizes near tendon-to-bone attachment defects. (a) Average median tissue-scale transverse and (b) shear strain for the superior and inferior fibrous regionswere compared. Black lines indicate significant difference (p < 0.05); data shown are average median strain ±95% confidence intervals.

Grahic Jump Location
Fig. 1

Study design. Infraspinatus attachments were divided into two experimental groups: intact and defect. For the defect group, a biopsy punch was used to create a superior-edge, partial-width, full-thickness tendon-to-bone attachment defect. Uniaxial tensile tests were performed with simultaneous image capture to obtain: biomechanical properties, qualitative tissue-scale strain fields, and quantitative regional tissue-scale strain of intact and defect groups. For regional tissue-scale strain, the average median strain was compared for fibrous, calcified, superior, and inferior regions within and between intact and defect groups. The white cylinder represents the biopsy punch used to create the defect. The dashed rectangle is a zoomed in depiction of the attachment. The dashed circle represents the superior edge defect. The dashed line separates superior from inferior, and the solid line separates the fibrous attachment from the calcified attachment; together creating the four quadrants. T, tendon; B, bone; M, muscle.

Tables

Errata

Discussions

Some tools below are only available to our subscribers or users with an online account.

Related Content

Customize your page view by dragging and repositioning the boxes below.

Related Journal Articles
Related eBook Content
Topic Collections

Sorry! You do not have access to this content. For assistance or to subscribe, please contact us:

  • TELEPHONE: 1-800-843-2763 (Toll-free in the USA)
  • EMAIL: asmedigitalcollection@asme.org
Sign In