Research Papers

Multiscale Poroviscoelastic Compressive Properties of Mouse Supraspinatus Tendons Are Altered in Young and Aged Mice

[+] Author and Article Information
Brianne K. Connizzo

Department of Biological Engineering,
Massachusetts Institute of Technology,
Cambridge, MA 02139

Alan J. Grodzinsky

Department of Biological Engineering,
Massachusetts Institute of Technology,
Cambridge, MA 02139;
Center for Biomedical Engineering,
Massachusetts Institute of Technology,
Cambridge, MA 02139;
Department of Electrical Engineering
and Computer Science,
Massachusetts Institute of Technology,
Cambridge, MA 02139;
Department of Mechanical Engineering,
Massachusetts Institute of Technology,
Cambridge, MA 02139
e-mail: alg@mit.edu

1Corresponding author.

Manuscript received August 7, 2017; final manuscript received December 4, 2017; published online February 15, 2018. Assoc. Editor: David Corr.

J Biomech Eng 140(5), 051002 (Feb 15, 2018) (8 pages) Paper No: BIO-17-1343; doi: 10.1115/1.4038745 History: Received August 07, 2017; Revised December 04, 2017

Rotator cuff disorders are one of the most common causes of shoulder pain and disability in the aging population but, unfortunately, the etiology is still unknown. One factor thought to contribute to the progression of disease is the external compression of the rotator cuff tendons, which can be significantly increased by age-related changes such as muscle weakness and poor posture. The objective of this study was to investigate the baseline compressive response of tendon and determine how this response is altered during maturation and aging. We did this by characterizing the compressive mechanical, viscoelastic, and poroelastic properties of young, mature, and aged mouse supraspinatus tendons using macroscale indentation testing and nanoscale high-frequency AFM-based rheology testing. Using these multiscale techniques, we found that aged tendons were stiffer than their mature counterparts and that both young and aged tendons exhibited increased hydraulic permeability and energy dissipation. We hypothesize that regional and age-related variations in collagen morphology and organization are likely responsible for changes in the multiscale compressive response as these structural parameters may affect fluid flow. Importantly, these results suggest a role for age-related changes in the progression of tendon degeneration, and we hypothesize that decreased ability to resist compressive loading via fluid pressurization may result in damage to the extracellular matrix (ECM) and ultimately tendon degeneration. These studies provide insight into the regional multiscale compressive response of tendons and indicate that altered compressive properties in aging tendons may be a major contributor to overall tendon degeneration.

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Buckwalter, J. A. , Heckman, J. D. , Petrie, D. P. , and AOA, 2003, “An AOA Critical Issue: Aging of the North American Population: New Challenges for Orthopaedics,” J. Bone Jt. Surg. Am., 85A(4), pp. 748–758. https://www.ncbi.nlm.nih.gov/pubmed/12672854
Millar, N. L. , Murrell, G. A. C. , and McInnes, I. B. , 2017, “Inflammatory Mechanisms in Tendinopathy—Towards Translation,” Nat. Rev. Rheumatol., 13(2), pp. 110–122. [CrossRef] [PubMed]
Soslowsky, L. J. , Thomopoulos, S. , Esmail, A. , Flanagan, C. L. , Iannotti, J. P. , Williamson, J. D. , and Carpenter, J. E. , 2002, “Rotator Cuff Tendinosis in an Animal Model: Role of Extrinsic and Overuse Factors,” Ann. Biomed. Eng., 30(8), pp. 1057–1063. [CrossRef] [PubMed]
Thomopoulos, S. , Parks, W. C. , Rifkin, D. B. , and Derwin, K. A. , 2015, “Mechanisms of Tendon Injury and Repair,” J. Orthop. Res., 33(6), pp. 832–839. [CrossRef] [PubMed]
Attia, M. , Scott, A. , Duchesnay, A. , Carpentier, G. , Soslowsky, L. J. , Huynh, M. B. , Van Kuppevelt, T. H. , Gossard, C. , Courty, J. , Tassoni, M.-C. , and Martelly, I. , 2012, “Alterations of Overused Supraspinatus Tendon: A Possible Role of Glycosaminoglycans and HARP/Pleiotrophin in Early Tendon Pathology,” J. Orthop. Res., 30(1), pp. 61–71. [CrossRef] [PubMed]
Thornton, G. M. , Shao, X. , Chung, M. , Sciore, P. , Boorman, R. S. , Hart, D. A. , and Lo, I. K. Y. , 2010, “Changes in Mechanical Loading Lead to Tendon-specific Alterations in MMP and TIMP Expression: Influence of Stress Deprivation and Intermittent Cyclic Hydrostatic Compression on Rat Supraspinatus and Achilles Tendons,” Br. J. Sports Med., 44(10), pp. 698–703. [CrossRef] [PubMed]
Thornton, G. M. , and Hart, D. A. , 2011, “The Interface of Mechanical Loading and Biological Variables as They Pertain to the Development of Tendinosis,” J. Musculoskeletal Neuronal Interact., 11(2), pp. 94–105. http://www.ismni.org/jmni/pdf/44/03THORNTON.pdf
Dourte, L. M. , Pathmanathan, L. , Mienaltowski, M. J. , Jawad, A. F. , Birk, D. E. , and Soslowsky, L. J. , 2013, “Mechanical, Compositional, and Structural Properties of the Mouse Patellar Tendon With Changes in Biglycan Gene Expression,” J. Orthop. Res., 31(9), pp. 1430–1437. [CrossRef] [PubMed]
Fang, F. , and Lake, S. P. , 2015, “Multiscale Strain Analysis of Tendon Subjected to Shear and Compression Demonstrates Strain Attenuation, Fiber Sliding, and Reorganization,” J. Orthop. Res., 33(11), pp. 1704–1712. [CrossRef] [PubMed]
Birk, D. E. , Zycband, E. I. , Woodruff, S. , Winkelmann, D. A. , and Trelstad, R. L. , 1997, “Collagen Fibrillogenesis In Situ: Fibril Segments Become Long Fibrils as the Developing Tendon Matures,” Dev. Dyn., 208(3), pp. 291–298. [CrossRef] [PubMed]
Birk, D. E. , Nurminskaya, M. V. , and Zycband, E. I. , 1995, “Collagen Fibrillogenesis In Situ: Fibril Segments Undergo Post-Depositional Modifications Resulting in Linear and Lateral Growth During Matrix Development,” Dev. Dyn., 202(3), pp. 229–243. [CrossRef] [PubMed]
Cribb, A. M. , and Scott, J. E. , 1995, “Tendon Response to Tensile Stress: An Ultrastructural Investigation of Collagen: Proteoglycan Interactions in Stressed Tendon,” J. Anat., 187(Pt. 2), pp. 423–428. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1167437/
Mow, V. C. , and Huiskes, R. , 2005, Basic Orthopaedic Biomechanics & Mechano-Biology, Lippincott Williams & Wilkins, Philadelphia, PA.
Scott, J. E. , Orford, C. R. , and Hughes, E. W. , 1981, “Proteoglycan-Collagen Arrangements in Developing Rat Tail Tendon. An Electron Microscopical and Biochemical Investigation,” Biochem. J., 195(3), pp. 573–581. [CrossRef] [PubMed]
Dunkman, A. A. , Buckley, M. R. , Mienaltowski, M. J. , Adams, S. M. , Thomas, S. J. , Satchell, L. , Kumar, A. , Pathmanathan, L. , Beason, D. P. , Iozzo, R. V. , Birk, D. E. , and Soslowsky, L. J. , 2013, “Decorin Expression Is Important for Age-Related Changes in Tendon Structure and Mechanical Properties,” Matrix Biol., 32(1), pp. 3–13. [CrossRef] [PubMed]
Nimer, E. , Schneiderman, R. , and Maroudas, A. , 2003, “Diffusion and Partition of Solutes in Cartilage Under Static Load,” Biophys. Chem., 106(2), pp. 125–146. [CrossRef] [PubMed]
Zhang, G. , Ezura, Y. , Chervoneva, I. , Robinson, P. S. , Beason, D. P. , Carine, E. T. , Soslowsky, L. J. , Iozzo, R. V. , and Birk, D. E. , 2006, “Decorin Regulates Assembly of Collagen Fibrils and Acquisition of Biomechanical Properties During Tendon Development,” J. Cell. Biochem., 98(6), pp. 1436–1449. [CrossRef] [PubMed]
Connizzo, B. K. , Yannascoli, S. M. , and Soslowsky, L. J. , 2013, “Structure-Function Relationships of Postnatal Tendon Development: A Parallel to Healing,” Matrix Biol., 32(2), pp. 106–116. [CrossRef] [PubMed]
Weiss, J. A. , and Maakestad, B. J. , 2006, “Permeability of Human Medial Collateral Ligament in Compression Transverse to the Collagen Fiber Direction,” J. Biomech., 39(2), pp. 276–283. [CrossRef] [PubMed]
Woo, S. L. , Debski, R. E. , Zeminski, J. , Abramowitch, S. D. , Saw, S. S. , and Fenwick, J. A. , 2000, “Injury and Repair of Ligaments and Tendons,” Annu. Rev. Biomed. Eng., 2, pp. 83–118. [CrossRef] [PubMed]
Ahmadzadeh, H. , Freedman, B. R. , Connizzo, B. K. , Soslowsky, L. J. , and Shenoy, V. B. , 2015, “Micromechanical Poroelastic Finite Element and Shear-Lag Models of Tendon Predict Large Strain Dependent Poisson's Ratios and Fluid Expulsion Under Tensile Loading,” Acta Biomater., 22, pp. 83–91. [CrossRef] [PubMed]
Atkinson, T. S. , Haut, R. C. , and Altiero, N. J. , 1997, “A Poroelastic Model That Predicts Some Phenomenological Responses of Ligaments and Tendons,” ASME J. Biomech. Eng., 119(4), pp. 400–405. [CrossRef]
Connizzo, B. K. , and Grodzinsky, A. J. , 2017, “Tendon Exhibits Complex Poroelastic Behavior at the Nanoscale as Revealed by High-Frequency AFM-Based Rheology,” J. Biomech., 54, pp. 11–18. [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]
Miller, K. S. , Connizzo, B. K. , Feeney, E. , and Soslowsky, L. J. , 2012, “Characterizing Local Collagen Fiber Re-Alignment and Crimp Behavior Throughout Mechanical Testing in a Mature Mouse Supraspinatus Tendon Model,” J. Biomech., 45(12), pp. 2061–2065. [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]
Connizzo, B. K. , Sarver, J. J. , Birk, D. E. , Soslowsky, L. J. , and Iozzo, R. V. , 2013, “Effect of Age and Proteoglycan Deficiency on Collagen Fiber Re-Alignment and Mechanical Properties in Mouse Supraspinatus Tendon,” ASME J. Biomech. Eng., 135(2), p. 021019. [CrossRef]
Fessel, G. , and Snedeker, J. G. , 2009, “Evidence Against Proteoglycan Mediated Collagen Fibril Load Transmission and Dynamic Viscoelasticity in Tendon,” Matrix Biol., 28(8), pp. 503–510. [CrossRef] [PubMed]
Miller, K. S. , Connizzo, B. K. , Feeney, E. , Tucker, J. J. , and Soslowsky, L. J. , 2012, “Examining Differences in Local Collagen Fiber Crimp Frequency Throughout Mechanical Testing in a Developmental Mouse Supraspinatus Tendon Model,” ASME J. Biomech. Eng., 134(4), p. 041004. [CrossRef]
Ansorge, H. L. , Adams, S. , Jawad, A. F. , Birk, D. E. , and Soslowsky, L. J. , 2012, “Mechanical Property Changes During Neonatal Development and Healing Using a Multiple Regression Model,” J. Biomech., 45(7), pp. 1288–1292. [CrossRef] [PubMed]
Fox, J. , Barthold, S. , Davisson, M. , Newcomer, C. , Quimby, F. , and Smith, A. , eds., 2017, The Mouse in Biomedical Research, 2nd ed., Vol. 4, Academic Press, Burlington, MA.
Connizzo, B. K. , Han, L. , Birk, D. E. , and Soslowsky, L. J. , 2016, “Collagen V-Heterozygous and -Null Supraspinatus Tendons Exhibit Altered Dynamic Mechanical Behaviour at Multiple Hierarchical Scales,” Interface Focus, 6(1), p. 20150043. [CrossRef] [PubMed]
Connizzo, B. K. , Sarver, J. J. , Han, L. , and Soslowsky, L. J. , 2014, “In Situ Fibril Stretch and Sliding Is Location-Dependent in Mouse Supraspinatus Tendons,” J. Biomech., 47(16), pp. 3794–3798. [CrossRef] [PubMed]
Azadi, M. , Nia, H. T. , Gauci, S. J. , Ortiz, C. , Fosang, A. J. , and Grodzinsky, A. J. , 2016, “Wide Bandwidth Nanomechanical Assessment of Murine Cartilage Reveals Protection of Aggrecan Knock-in Mice From Joint-Overuse,” J. Biomech., 49(9), pp. 1634–1640. [CrossRef] [PubMed]
Nia, H. T. , Gauci, S. J. , Azadi, M. , Hung, H.-H. , Frank, E. , Fosang, A. J. , Ortiz, C. , and Grodzinsky, A. J. , 2015, “High-Bandwidth AFM-Based Rheology Is a Sensitive Indicator of Early Cartilage Aggrecan Degradation Relevant to Mouse Models of Osteoarthritis,” J. Biomech., 48(1), pp. 162–165. [CrossRef] [PubMed]
Nia, H. T. , Han, L. , Li, Y. , Ortiz, C. , and Grodzinsky, A. , 2011, “Poroelasticity of Cartilage at the Nanoscale,” Biophys. J., 101(9), pp. 2304–2313. [CrossRef] [PubMed]
Han, B. , Nia, H. T. , Wang, C. , Chandrasekaran, P. , Li, Q. , Cherry, D. R. , Li, H. , Grodzinsky, A. J. , and Han, L. , 2017, “AFM-Nanomechanical Test: An Interdisciplinary Tool That Links the Understanding of Cartilage and Meniscus Biomechanics, Osteoarthritis Degeneration, and Tissue Engineering,” ACS Biomaterials Sci. Eng., 3(9), pp. 2033–2049. [CrossRef]
Nia, H. T. , Han, L. , Bozchalooi, I. S. , Roughley, P. , Youcef-Toumi, K. , Grodzinsky, A. J. , and Ortiz, C. , 2015, “Aggrecan Nanoscale Solid-Fluid Interactions Are a Primary Determinant of Cartilage Dynamic Mechanical Properties,” ACS Nano, 9(3), pp. 2614–2625. [CrossRef] [PubMed]
Peffers, M. J. , Thorpe, C. T. , Collins, J. A. , Eong, R. , Wei, T. K. J. , Screen, H. R. C. , and Clegg, P. D. , 2014, “Proteomic Analysis Reveals Age-Related Changes in Tendon Matrix Composition, With Age- and Injury-Specific Matrix Fragmentation,” J. Biol. Chem., 289(37), pp. 25867–25878. [CrossRef] [PubMed]
Riley, G. P. , Harrall, R. L. , Constant, C. R. , Chard, M. D. , Cawston, T. E. , and Hazleman, B. L. , 1994, “Glycosaminoglycans of Human Rotator Cuff Tendons: Changes With Age and in Chronic Rotator Cuff Tendinitis,” Ann. Rheum. Dis., 53(6), pp. 367–376. [CrossRef] [PubMed]
Esquisatto, M. A. M. , Joazeiro, P. P. , Pimentel, E. R. , and Gomes, L. , 2007, “The Effect of Age on the Structure and Composition of Rat Tendon Fibrocartilage,” Cell Biol. Int., 31(6), pp. 570–577. [CrossRef] [PubMed]
Moore, M. J. , and De Beaux, A. , 1987, “A Quantitative Ultrastructural Study of Rat Tendon From Birth to Maturity,” J. Anat., 153, pp. 163–169. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1261790/pdf/janat00179-0167.pdf [PubMed]
Strocchi, R. , De Pasquale, V. , Guizzardi, S. , Govoni, P. , Facchini, A. , Raspanti, M. , Girolami, M. , and Giannini, S. , 1991, “Human Achilles Tendon: Morphological and Morphometric Variations as a Function of Age,” Foot Ankle, 12(2), pp. 100–104. [CrossRef] [PubMed]
Butler, S. L. , Kohles, S. S. , Thielke, R. J. , Chen, C. , and Vanderby, R. , 1997, “Interstitial Fluid Flow in Tendons or Ligaments: A Porous Medium Finite Element Simulation,” Med. Biol. Eng. Comput., 35(6), pp. 742–746. [CrossRef] [PubMed]
Chen, C. T. , Malkus, D. S. , and Vanderby, R. , 1998, “A Fiber Matrix Model for Interstitial Fluid Flow and Permeability in Ligaments and Tendons,” Biorheology, 35(2), pp. 103–118. [CrossRef] [PubMed]
Fessel, G. , Cadby, J. , Wunderli, S. , van Weeren, R. , and Snedeker, J. G. , 2014, “Dose- and Time-Dependent Effects of Genipin Crosslinking on Cell Viability and Tissue Mechanics—Toward Clinical Application for Tendon Repair,” Acta Biomater., 10(5), pp. 1897–1906. [CrossRef] [PubMed]
Gautieri, A. , Passini, F. S. , Silván, U. , Guizar-Sicairos, M. , Carimati, G. , Volpi, P. , Moretti, M. , Schoenhuber, H. , Redaelli, A. , Berli, M. , and Snedeker, J. G. , 2017, “Advanced Glycation End-Products: Mechanics of Aged Collagen From Molecule to Tissue,” Matrix Biol., 59, pp. 95–108. [CrossRef] [PubMed]
Pang, X. , Wu, J. P. , Allison, G. T. , Xu, J. , Rubenson, J. , Zheng, M.-H. , Lloyd, D. G. , Gardiner, B. , Wang, A. , and Kirk, T. B. , 2016, “Three Dimensional Microstructural Network of Elastin, Collagen, and Cells in Achilles Tendons,” J. Orthop. Res., 35(6), pp. 1203–1214. https://www.ncbi.nlm.nih.gov/pubmed/27002477
Fang, F. , and Lake, S. P. , 2016, “Multiscale Mechanical Integrity of Human Supraspinatus Tendon in Shear After Elastin Depletion,” J. Mech. Behav. Biomed. Mater., 63, pp. 443–455. [CrossRef] [PubMed]
Fessel, G. , Wernli, J. , Li, Y. , Gerber, C. , and Snedeker, J. G. , 2012, “Exogenous Collagen Cross-Linking Recovers Tendon Functional Integrity in an Experimental Model of Partial Tear,” J. Orthop. Res., 30(6), pp. 973–981. [CrossRef] [PubMed]
Zhang, J. , and Wang, J. H.-C. , 2015, “Moderate Exercise Mitigates the Detrimental Effects of Aging on Tendon Stem Cells,” PLoS One, 10(6), p. e0130454. [CrossRef] [PubMed]
Yu, T.-Y. , Pang, J.-H. S. , Wu, K. P.-H. , Chen, M. J.-L. , Chen, C.-H. , and Tsai, W.-C. , 2013, “Aging Is Associated With Increased Activities of Matrix Metalloproteinase-2 and -9 in Tenocytes,” BMC Musculoskeletal Disord., 14, p. 2. [CrossRef]
Tsai, W.-C. , Chang, H.-N. , Yu, T.-Y. , Chien, C.-H. , Fu, L.-F. , Liang, F.-C. , and Pang, J.-H. S. , 2011, “Decreased Proliferation of Aging Tenocytes Is Associated With down-Regulation of Cellular Senescence-Inhibited Gene and Up-Regulation of p27,” J. Orthop. Res., 29(10), pp. 1598–1603. [CrossRef] [PubMed]
Torricelli, P. , Veronesi, F. , Pagani, S. , Maffulli, N. , Masiero, S. , Frizziero, A. , and Fini, M. , 2013, “In Vitro Tenocyte Metabolism in Aging and Oestrogen Deficiency,” Age, 35(6), pp. 2125–2136. [CrossRef] [PubMed]
Chen, C. T. , McCabe, R. P. , Grodzinsky, A. J. , and Vanderby, R. , 2000, “Transient and Cyclic Responses of Strain-Generated Potential in Rabbit Patellar Tendon Are Frequency and PH Dependent,” ASME J. Biomech. Eng., 122(5), pp. 465–470.


Grahic Jump Location
Fig. 1

(a) Testing setup for macroscopic compressive indentation of mouse supraspinatus tendon. Inset image shows dimensions of prepared tendon, and the expanded schematic depicts regional definition. (b) Indentation testing protocol, including preload, sequential compressive strain ramp-and-hold indentations, and dynamic frequency sweep.

Grahic Jump Location
Fig. 2

(a) Depiction of mouse supraspinatus tendon nanoindentation protocol, where the circles represent indentation regions. Nine indentations were performed within each region; solid lines mark the distance between indentation regions and the areas defined for pooled regional comparisons. (b) Depiction of indentation of mouse supraspinatus tendon using a probe tip having diameter (d) and AFM cantilever spring constant (k) (note: AFM cantilever is not to scale) (c) nanoindentation displacement–force protocol for each indentation consisted of an initial load-controlled ramp-and-hold pre-indentation of ∼3.5 μm followed by random binary sequence displacements of 8–12 nm amplitude. (d) Representative schematic of the magnitude and phase angle versus frequency for tendon, indicating the definitions of low and high frequency moduli values (EL and EH) as well as the angle and frequency of viscoelastic and (δv, fv) and poroelastic poroelastic peaks (δp, fp) (panels (b)–(d) adapted from Ref. [23]).

Grahic Jump Location
Fig. 3

In macroscale indentation testing, (a) equilibrium modulus was significantly higher in the aged tendons compared to both the young and mature tendons. (b) Similarly, the magnitude of the dynamic modulus was higher in aged tendons compared to mature tendons, particularly at the insertion site and the lowest frequency of the midsubstance. The young tendons were not significantly different from the aged group at any frequency in either regions, but were higher compared to the mature group at the highest frequency. (c) Finally, the phase angle of the dynamic modulus was higher in the young group compared to the mature group at the lowest frequency of the insertion site and compared to mature and aged tendons at low and high frequencies in the midsubstance. Data are presented as mean ±95% confidence interval and statistical significance is denoted by a solid line or star (*) symbol, while trends are denoted by a dashed line or hash (#) symbol.

Grahic Jump Location
Fig. 4

In nanoindentation testing: ((a), left) the low frequency, or equilibrium, modulus was significantly higher in the young and aged groups at the insertion site and in the mature and aged groups compared to the young group at the midsubstance. No significant differences were found in the ((a), right) high frequency, or instantaneous, modulus or the (b) self-stiffening ratio. Data are presented as mean ±95% confidence interval and statistical significance between groups is denoted by a solid line, while trends are denoted by a dashed line.

Grahic Jump Location
Fig. 5

Poroelastic properties were significantly altered in young and aged tendons when compared to the mature group (pooled comparisons ((a) and (c)), entire regional dataset ((b) and (d))). Specifically, the peak frequency ((a) and (b)) was higher in young and aged tendons at the midsubstance, and the peak phase angle (c) and (d) was higher in both groups in both regions of the tendon. Pooled data are presented as mean ±95% confidence interval, while entire dataset is presented as a single mean at each region. Statistical significance between groups is denoted by a solid line, while trends are denoted by a dashed line.

Grahic Jump Location
Fig. 6

Viscoelastic properties were altered only slightly with maturation and aging (pooled comparisons ((a) and (c)), entire regional dataset ((b) and (d))), with increased peak frequency (a) and (b) in young and aged tendons at the midsubstance. No differences were found in viscoelastic peak phase angle in either region of the tendon (c) and (d). Pooled data are presented as mean ±95% confidence interval, while entire dataset is presented as a single mean at each region. Statistical significance between groups is denoted by a solid line, while trends are denoted by a dashed line.

Grahic Jump Location
Fig. 7

Regional variation in each material parameter is shown here, where each bar represents the ratio of insertion to midsubstance properties; a value less than one indicates higher properties at the midsubstance, and a value greater than one indicates higher properties at the insertion site. A star (*) within the bar indicates a statistical significance between the insertion and midsubstance, while solid bars indicate significant differences between age groups. Many parameters were regionally different in the mature tendons (middle bars), but this regional heterogeneity was lost in the aged tendons (right bars), particularly in moduli (a)–(c) and poroelastic properties (e) and (f). Young tendons showed a loss of regional differences in poroelastic parameters (e) and (f) and a complete reversal of where higher properties appeared in the moduli values (a)–(c). Regional variations in viscoelastic parameters appeared to be constant across all age groups (g) and (h). Data are presented as mean ±95% confidence interval.




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