Research Papers

Supraspinatus Tendons Have Different Mechanical Properties Across Sex

[+] Author and Article Information
K. A. Bonilla, A. M. Pardes

McKay Orthopaedic Laboratory,
University of Pennsylvania,
Philadelphia, PA 19104

B. R. Freedman

McKay Orthopaedic Laboratory,
University of Pennsylvania,
Philadelphia, PA 19104;
John A. Paulson School of Engineering
and Applied Sciences,
Harvard University,
Cambridge, MA 02138;
Wyss Institute for Biologically
Inspired Engineering,
Harvard University,
Cambridge, MA 02115

L. J. Soslowsky

McKay Orthopaedic Laboratory,
University of Pennsylvania,
Stemmler Hall, 3450 Hamilton Walk,
Philadelphia, PA 19104
e-mail: soslowsk@upenn.edu

1All authors contributed equally to this work.

2Corresponding author.

Manuscript received September 14, 2017; final manuscript received August 8, 2018; published online October 17, 2018. Assoc. Editor: Guy M. Genin.

J Biomech Eng 141(1), 011002 (Oct 17, 2018) (8 pages) Paper No: BIO-17-1411; doi: 10.1115/1.4041321 History: Received September 14, 2017; Revised August 08, 2018

Sex differences in the mechanical properties of different musculoskeletal tissues and their impact on tendon function and disease are becoming increasingly recognized. Tendon mechanical properties are influenced by the presence or absence of sex hormones and these effects appear to be tendon- or ligament-specific. The objective of this study was to determine how sex and hormone differences in rats affect supraspinatus tendon and muscle properties. We hypothesized that male supraspinatus tendons would have increased cross-sectional area but no differences in tendon material properties or muscle composition when compared to supraspinatus tendons from female or ovariectomized (OVX) female rats. Uninjured supraspinatus tendons and muscles from male, female, and OVX female rats were collected and mechanical and histological properties were determined. Our analysis demonstrated decreased dynamic modulus and increased hysteresis and cross-sectional area in male tendons. We found that male tendons exhibited decreased dynamic modulus (during low strain frequency sweep and high strain fatigue loading), increased hysteresis, and increased cross-sectional area compared to female and OVX female tendons. Despite robust mechanical differences, tendon cell density and shape, and muscle composition remained unchanged between groups. Interestingly, these differences were unique compared to previously reported sex differences in rat Achilles tendons, which further supports the concept that the effect of sex on tendon varies anatomically. These differences may partially provide a mechanistic explanation for the increased rate of acute supraspinatus tendon ruptures seen in young males.

Copyright © 2019 by ASME
Your Session has timed out. Please sign back in to continue.


Oliva, F. , Piccirilli, E. , Berardi, A. C. , Frizziero, A. , Tarantino, U. , and Maffulli, N. , 2016, “ Hormones and Tendinopathies: The Current Evidence,” Br. Med. Bull., 117(1), pp. 39–58. [CrossRef] [PubMed]
Frizziero, A. , Vittadini, F. , Gasparre, G. , and Masiero, S. , 2014, “ Impact of Oestrogen Deficiency and Aging on Tendon: Concise Review,” Muscles, Ligaments Tendons J., 4(3), pp. 324–328 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4241423/#__ffn_sectitle.
Pardes, A. M. , Freedman, B. R. , Fryhofer, G. W. , Salka, N. S. , Bhatt, P. R. , and Soslowsky, L. J. , 2016, “ Males Have Inferior Achilles Tendon Material Properties Compared to Females in a Rodent Model,” Ann. Biomed. Eng., 44(10), pp. 2901–2910. [CrossRef] [PubMed]
Vosseller, J. T. , Ellis, S. J. , Levine, D. S. , Kennedy, J. G. , Elliott, A. J. , Deland, J. T. , Roberts, M. M. , and O'Malley, M. J. , 2013, “ Achilles Tendon Rupture in Women,” Foot Ankle Int., 34(1), pp. 49–53. [CrossRef] [PubMed]
Pearson, S. J. , Burgess, K. E. , and Onambélé, G. L. , 2011, “ Serum Relaxin Levels Affect the In Vivo Properties of Some but Not All Tendons in Normally Menstruating Young Women,” Exp. Physiol., 96(7), pp. 681–688. [CrossRef] [PubMed]
Aagaard, K. E. , Abu-Zidan, F. , and Lunsjo, K. , 2015, “ High Incidence of Acute Full-Thickness Rotator Cuff Tears,” Acta Orthop., 86(5), pp. 558–562. [CrossRef] [PubMed]
Lee, H. , Petrofsky, J. S. , Daher, N. , Berk, L. , Laymon, M. , and Khowailed, I. A. , 2013, “ Anterior Cruciate Ligament Elasticity and Force for Flexion During the Menstrual Cycle,” Med. Sci. Monit., 19, pp. 1080–1088. [CrossRef] [PubMed]
Trobisch, P. D. , Bauman, M. , Weise, K. , Stuby, F. , and Hak, D. J. , 2009, “ Histologic Analysis of Ruptured Quadriceps Tendons,” Knee Surg. Sports Traumatol. Arthroscopy, 18(1), pp. 85–88. [CrossRef]
Circi, E. , Akpinar, S. , Balcik, C. , Bacanli, D. , Guven, G. , Akgun, R. C. , and Tuncay, I. C. , 2009, “ Biomechanical and Histological Comparison of the Influence of Oestrogen Deficient State on Tendon Healing Potential in Rats,” Int. Orthop., 33(5), pp. 1461–1466. [CrossRef] [PubMed]
Merrill, A. , Guzman, K. , and Miller, S. L. , 2008, “ Gender Differences in Glenoid Anatomy: An Anatomic Study,” Surg. Radiol. Anat., 31(3), pp. 183–189. [CrossRef] [PubMed]
Tang, C.-T. , and Simpson, S. , 2016, “ Shoulder,” Sex Differences in Sports Medicine, E. Casey , M. Rho , and J. M. Press , eds., Demos Medical Publishing, New York, pp. 31–44.
Karthikeyan, S. , Rai, S. B. , Parsons, H. , Drew, S. , Smith, C. D. , and Griffin, D. R. , 2014, “ Ultrasound Dimensions of the Rotator Cuff in Young Healthy Adults,” J. Shoulder Elbow Surg., 23(8), pp. 1107–1112. [CrossRef] [PubMed]
Vafadar, A. K. , Côté, J. N. , and Archambault, P. S. , 2015, “ Sex Differences in the Shoulder Joint Position Sense Acuity: A Cross-Sectional Study,” BMC Musculoskeletal Disord., 16(1), pp. 273–280.
Fedorowich, L. , Emery, K. , Gervasi, B. , and Côté, J. N. , 2013, “ Gender Differences in Neck/Shoulder Muscular Patterns in Response to Repetitive Motion Induced Fatigue,” J. Electromyogr. Kinesiol., 23(5), pp. 1183–1189. [CrossRef] [PubMed]
Wojtys, E. M. , Huston, L. J. , Boynton, M. D. , Spindler, K. P. , and Lindenfeld, T. N. , 2002, “ The Effect of the Menstrual Cycle on Anterior Cruciate Ligament Injuries in Women as Determined by Hormone Levels,” Am. J. Sports Med., 30(2), pp. 182–188. [CrossRef] [PubMed]
Bridgeman, J. T. , Zhang, Y. , Donahue, H. , Wade, A. M. , and Juliano, P. J. , 2010, “ Estrogen Receptor Expression in Posterior Tibial Tendon Dysfunction: A Pilot Study,” Foot Ankle Int., 31(12), pp. 1081–1084. [CrossRef] [PubMed]
Liu, S. H. , Al-Shaikh, R. , Panossian, V. , and Nelson, S. D. , 1996, “ Primary Immunolocalization of Estrogen and Progesterone Target Cells in the Human Anterior Cruciate Ligament,” J. Orthop. Res., 14(4), pp. 526–533. [CrossRef] [PubMed]
Huisman, E. S. , Andersson, G. , Scott, A. , Reno, C. R. , Hart, D. A. , and Thornton, G. M. , 2014, “ Regional Molecular and Cellular Differences in the Female Rabbit Achilles Tendon Complex: Potential Implications for Understanding Responses to Loading,” J. Anat., 224(5), pp. 538–547. [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 (Dordrecht), 35(6), pp. 2125–2136. [CrossRef]
Aydin, A. , Kenar, H. , Atmaca, H. , Alici, T. , Gacar, G. , Muezzinoglu, U. S. , and Karaoz, E. , 2013, “ The Short- and Long- Term Effects of Estrogen Deficiency on Apoptosis in Musculoskeletal Tissues: An Experimental Animal Model Study,” Arch. Iran. Med., 16(5), pp. 271–276. [PubMed]
Dehghan, F. , Muniandy, S. , Yusof, A. , and Salleh, N. , 2014, “ Sex-Steroid Regulation of Relaxin Receptor Isoforms (RXFP1 & RXFP2) Expression in the Patellar Tendon and Lateral Collateral Ligament of Female WKY Rats,” Int. J. Med. Sci., 11(2), pp. 180–191. [CrossRef] [PubMed]
Westh, E. , Kongsgaard, M. , Bojsen-Moller, J. , Aagaard, P. , Hansen, M. , Kjaer, M. , and Magnusson, S. P. , 2008, “ Effect of Habitual Exercise on the Structural and Mechanical Properties of Human Tendon, In Vivo, in Men and Women,” Scand. J. Med. Sci. Sports, 18(1), pp. 23–30. [CrossRef] [PubMed]
Lee, C.-Y. , Liu, X. , Smith, C. L. , Zhang, X. , Hsu, H.-C. , Wang, D.-Y. , and Luo, Z.-P. , 2004, “ The Combined Regulation of Estrogen and Cyclic Tension on Fibroblast Biosynthesis Derived From Anterior Cruciate Ligament,” Matrix Biol., 23(5), pp. 323–329. [CrossRef] [PubMed]
Seneviratne, A. , Attia, E. , Williams, R. J. , Rodeo, S. A. , and Hannafin, J. A. , 2004, “ The Effect of Estrogen on Ovine Anterior Cruciate Ligament Fibroblasts: Cell Proliferation and Collagen Synthesis,” Am. J. Sports Med., 32(7), pp. 1613–1618. [CrossRef] [PubMed]
Magrum, E. , Statuta, S. , Hryvniak, D. , and Wilder, R. , 2016, “ Running,” Sex Differences in Sports Medicine, E. Casey , M. Rho , and J. M. Press , eds., Demos Medical Publishing, New York, pp. 161–167.
Greenhalgh, A. , and Sinclair, J. , 2014, “ Comparison of Achilles Tendon Loading Between Male and Female Recreational Runners,” J. Human Kinet., 44(1), pp. 155–159.
Beynnon, B. D. , Vacek, P. M. , Newell, M. K. , Tourville, T. W. , Smith, H. C. , Shultz, S. J. , Slauterbeck, J. R. , and Johnson, R. J. , 2014, “ The Effects of Level of Competition, Sport, and Sex on the Incidence of First-Time Noncontact Anterior Cruciate Ligament Injury,” Am. J. Sports Med., 42(8), pp. 1806–1812. [CrossRef] [PubMed]
Burgess, K. E. , Pearson, S. J. , and Onambélé, G. L. , 2010, “ Patellar Tendon Properties With Fluctuating Menstrual Cycle Hormones,” J. Strength Cond. Res., 24(8), pp. 2088–2095. [CrossRef] [PubMed]
Wentorf, F. A. , Sudoh, K. , Moses, C. , Arendt, E. A. , and Carlson, C. S. , 2006, “ The Effects of Estrogen on Material and Mechanical Properties of the Intra- and Extra-Articular Knee Structures,” Am. J. Sports Med., 34(12), pp. 1948–1952. [CrossRef] [PubMed]
Ahmad, C. S. , Clark, M. , Heilmann, N. , Schoeb, J. S. , Gardner, T. R. , and Levine, W. N. , 2005, “ Effect of Gender and Maturity on Quadriceps-to-Hamstring Strength Ratio and Anterior Cruciate Ligament Laxity,” Am. J. Sports Med., 34(3), pp. 370–374. [CrossRef] [PubMed]
Sigward, S. M. , Pollard, C. D. , Havens, K. L. , and Powers, C. M. , 2012, “ Influence of Sex and Maturation on Knee Mechanics During Side-Step Cutting,” Med. Sci. Sports Exercise, 44(8), pp. 1497–1503. [CrossRef]
Wojtys, E. M. , Ashton-Miller, J. A. , and Huston, L. J. , 2002, “ A Gender-Related Difference in the Contribution of the Knee Musculature to Sagittal-Plane Shear Stiffness in Subjects With Similar Knee Laxity,” J. Bone Jt. Surg., 84A(1), pp. 10–16. [CrossRef]
Ro, D. H. , Lee, D. Y. , Moon, G. , Lee, S. , Seo, S. G. , Kim, S. H. , Park, I. W. , and Lee, M. C. , 2016, “ Sex Differences in Knee Joint Loading: Cross-Sectional Study in Geriatric Population,” J. Orthop. Res., 35(6), pp. 1283–1289. [CrossRef] [PubMed]
Kerrigan, D. C. , Todd, M. K. , and Croce, U. D. , 1998, “ Gender Differences in Joint Biomechanics During Walking: Normative Study in Young Adults,” Am. J. Phys. Med. Rehabil., 77(1), pp. 2–7. [CrossRef] [PubMed]
Murshed, K. A. , Çiçekcibaşi, A. E. , Karabacakoğlu, A. , Şeker, M. , and Ziylan, T. , 2005, “ Distal Femur Morphometry: A Gender and Bilateral Comparative Study Using Magnetic Resonance Imaging,” Surg. Radiol. Anat., 27(2), pp. 108–112. [CrossRef] [PubMed]
Hewett, T. E. , Myer, G. D. , and Ford, K. R. , 2004, “ Decrease in Neuromuscular Control About the Knee With Maturation in Female Athletes,” J. Bone Jt. Surg., 86A(8), pp. 1601–1608. [CrossRef]
Yamamoto, A. , Takagishi, K. , Osawa, T. , Yanagawa, T. , Nakajima, D. , Shitara, H. , and Kobayashi, T. , 2010, “ Prevalence and Risk Factors of a Rotator Cuff Tear in the General Population,” J. Shoulder Elbow Surg., 19(1), pp. 116–120. [CrossRef] [PubMed]
Keener, J. D. , Steger-May, K. , Stobbs, G. , and Yamaguchi, K. , 2010, “ Asymptomatic Rotator Cuff Tears: Patient Demographics and Baseline Shoulder Function,” J Shoulder Elbow Surg., 19(8), pp. 1191–1198. [CrossRef] [PubMed]
Yamaguchi, K. , Ditsios, K. , Middleton, W. D. , Hildebolt, C. F. , Galatz, L. M. , and Teefey, S. A. , 2006, “ The Demographic and Morphological Features of Rotator Cuff Disease: A Comparison of Asymptomatic and Symptomatic Shoulders,” J. Bone Jt. Surg., 88A(8), pp. 1699–1704. [CrossRef]
Milgrom, C. , Schaffler, M. , Gilbert, S. , and van Holsbeeck, M. , 1995, “ Rotator-Cuff Changes in Asymptomatic Adults,” J. Bone Jt. Surg. Br., 77(2), pp. 296–298 https://online.boneandjoint.org.uk/doi/abs/10.1302/0301-620X.77B2.7706351.
White, J. J. E. , Titchener, A. G. , Fakis, A. , Tambe, A. A. , Hubbard, R. B. , and Clark, D. I. , 2014, “ An Epidemiological Study of Rotator Cuff Pathology Using the Health Improvement Network Database,” Bone Jt. J., 96B(3), pp. 350–353. [CrossRef]
McFarland, E. G. , Campbell, G. , and McDowell, J. , 1996, “ Posterior Shoulder Laxity in Asymptomatic Athletes,” Am. J. Sports Med., 24(4), pp. 468–471. [CrossRef] [PubMed]
Voycheck, C. A. , Rainis, E. J. , McMahon, P. J. , Weiss, J. A. , and Debski, R. E. , 2010, “ Effects of Region and Sex on the Mechanical Properties of the Glenohumeral Capsule During Uniaxial Extension,” J. Appl. Physiol., 108(6), pp. 1711–1718. [CrossRef] [PubMed]
Abate, M. , Schiavone, C. , Di Carlo, L. , and Salini, V. , 2014, “ Prevalence of and Risk Factors for Asymptomatic Rotator Cuff Tears in Postmenopausal Women,” Menopause, 21(3), pp. 275–280. [CrossRef] [PubMed]
Rooney, S. I. , Baskin, R. , Torino, D. J. , Vafa, R. P. , Khandekar, P. S. , Kuntz, A. F. , and Soslowsky, L. J. , 2016, “ Ibuprofen Differentially Affects Supraspinatus Muscle and Tendon Adaptations to Exercise in a Rat Model,” Am. J. Sports Med., 44(9), pp. 2237–2245. [CrossRef] [PubMed]
Favata, M. , 2006, Scarless Healing in the Fetus: Implications and Strategies for Postnatal Tendon Repair, University of Pennsylvania, Pennsylvania, PA.
Pardes, A. M. , Beach, Z. M. , Raja, H. , Rodriguez, A. B. , Freedman, B. R. , and Soslowsky, L. J. , 2017, “ Aging Leads to Inferior Achilles Tendon Mechanics and Altered Ankle Function in Rodents,” J. Biomech., 60, pp. 30–38. [CrossRef] [PubMed]
Freedman, B. R. , Salka, N. S. , Morris, T. R. , Bhatt, P. R. , Pardes, A. M. , Gordon, J. A. , Nuss, C. A. , Riggin, C. N. , Fryhofer, G. W. , Farber, D. C. , and Soslowsky, L. , 2017, “ Temporal Healing of Achilles Tendons After Injury in Rodents Depends on Surgical Treatment and Activity,” J. Am. Acad. Orthop. Surg., 25(9), pp. 635–647. [CrossRef] [PubMed]
Fryhofer, G. W. , Freedman, B. R. , Hillin, C. D. , Salka, N. S. , Pardes, A. M. , Weiss, S. N. , Farber, D. C. , and Soslowsky, L. J. , 2016, “ Postinjury Biomechanics of Achilles Tendon Vary by Sex and Hormone Status,” J. Appl. Physiol. (1985), 121(5), pp. 1106–1114. [CrossRef] [PubMed]
Freedman, B. R. , Fryhofer, G. W. , Salka, N. S. , Raja, H. A. , Hillin, C. D. , Nuss, C. A. , Farber, D. C. , and Soslowsky, L. J. , 2017, “ Mechanical, Histological, and Functional Properties Remain Inferior in Conservatively Treated Achilles Tendons in Rodents: Long Term Evaluation,” J. Biomech., 56, pp. 55–60. [CrossRef] [PubMed]
Freedman, B. R. , Sarver, J. J. , Buckley, M. R. , Voleti, P. B. , and Soslowsky, L. J. , 2014, “ Biomechanical and Structural Response of Healing Achilles Tendon to Fatigue Loading Following Acute Injury,” J. Biomech., 47(9), pp. 2028–2034. [CrossRef] [PubMed]
Freedman, B. R. , Gordon, J. A. , Bhatt, P. R. , Pardes, A. M. , Thomas, S. J. , Sarver, J. J. , Riggin, C. N. , Tucker, J. J. , Williams, A. W. , Zanes, R. C. , Hast, M. W. , Farber, D. C. , Silbernagel, K. G. , and Soslowsky, L. J. , 2016, “ Nonsurgical Treatment and Early Return to Activity Leads to Improved Achilles Tendon Fatigue Mechanics and Functional Outcomes During Early Healing in an Animal Model,” J. Orthop. Res., 34(12), pp. 2172–2180. [CrossRef] [PubMed]
Fung, D. T. , Wang, V. M. , Laudier, D. M. , Shine, J. H. , Basta-Pljakic, J. , Jepsen, K. J. , Schaffler, M. B. , and Flatow, E. L. , 2009, “ Subrupture Tendon Fatigue Damage,” J. Orthop. Res., 27(2), pp. 264–273. [CrossRef] [PubMed]
Schiaffino, S. , Gorza, L. , Sartore, S. , Saggin, L. , Ausoni, S. , Vianello, M. , Gundersen, K. , and Lømo, T. , 1989, “ Three Myosin Heavy Chain Isoforms in Type 2 Skeletal Muscle Fibres,” J. Muscle Res. Cell Motil., 10(3), pp. 197–205. [CrossRef] [PubMed]
Smith, L. R. , and Barton, E. R. , 2014, “ SMASH–Semi-Automatic Muscle Analysis Using Segmentation of Histology: A MATLAB Application,” Skeletal Muscle, 4(1), p. 21. [CrossRef] [PubMed]
Freedman, B. R. , Gordon, J. A. , and Soslowsky, L. J. , 2014, “ The Achilles Tendon: Fundamental Properties and Mechanisms Governing Healing,” Muscles Ligaments Tendons J., 4(2), pp. 245–255 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4187594/. [PubMed]
Slauterbeck, J. , Clevenger, C. , Lundberg, W. , and Burchfield, D. M. , 1999, “ Estrogen Level Alters the Failure Load of the Rabbit Anterior Cruciate Ligament,” J. Orthop. Res., 17(3), pp. 405–408. [CrossRef] [PubMed]
Hansen, M. , Kongsgaard, M. , Holm, L. , Skovgaard, D. , Magnusson, S. P. , Qvortrup, K. , Larsen, J. O. , Aagaard, P. , Dahl, M. , Serup, A. , Frystyk, J. , Flyvbjerg, A. , Langberg, H. , and Kjaer, M. , 2009, “ Effect of Estrogen on Tendon Collagen Synthesis, Tendon Structural Characteristics, and Biomechanical Properties in Postmenopausal Women,” J. Appl. Physiol., 106(4), pp. 1385–1393. [CrossRef] [PubMed]
Shepherd, J. H. , and Screen, H. R. C. , 2013, “ Fatigue Loading of Tendon,” Int. J. Exp. Pathol., 94(4), pp. 260–270. [CrossRef] [PubMed]
Komi, P. , Fukashiro, S. , and Järvinen, M. , 1992, “ Biomechanical Loading of the Achilles Tendon During Normal Locomotion,” Clin. Sports Med., 11(3), pp. 521–531. [PubMed]
Kannus, P. , and Natri, A. , 1997, “ Etiology and Pathophysiology of Tendon Ruptures in Sports,” Scand. J. Med. Sci. Sports, 7(2), pp. 107–112 https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1600-0838.1997.tb00126.x. [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]
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]
Nakajima, T. , Rokuuma, N. , Hamada, K. , Tomatsu, T. , and Fukuda, H. , 1994, “ Histologic and Biomechanical Characteristics of the Supraspinatus Tendon: Reference to Rotator Cuff Tearing,” J. Shoulder Elbow Surg., 3(2), pp. 79–87. [CrossRef] [PubMed]
Itoi, E. , Berglund, L. J. , Grabowski, J. J. , Schultz, F. M. , Growney, E. S. , Morrey, B. F. , and An, K.-N. , 1995, “ Tensile Properties of the Supraspinatus Tendon,” J. Orthop. Res., 13(4), pp. 578–584. [CrossRef] [PubMed]
Elert, J. , Sterner, Y. , Nyberg, V. , and Gerdle, B. , 2000, “ Lack of Gender Differences in the Ability to Relax Between Repetitive Maximum Isokinetic Shoulder Forward Flexions: A Population-Based Study Among Northern Swedes,” Eur. J. Appl. Physiol., 83(4–5), pp. 246–256. [CrossRef] [PubMed]
Boyd, S. K. , Davison, P. , Müller, R. , and Gasser, J. A. , 2006, “ Monitoring Individual Morphological Changes Over Time in Ovariectomized Rats by In Vivo Micro-Computed Tomography,” Bone, 39(4), pp. 854–862. [CrossRef] [PubMed]
Bryant, A. L. , Clark, R. A. , Bartold, S. , Murphy, A. , Bennell, K. , Hohmann, E. , Marshall-Gradisnik, S. , Payne, C. , and Crossley, K. M. , 2008, “ Effects of Estrogen on the Mechanical Behavior of the Human Achilles Tendon In Vivo,” J. Appl. Physiol., 105(4), pp. 1035–1043. [CrossRef] [PubMed]
Burgess, K. E. , Pearson, S. J. , and Onambélé, G. L. , 2009, “ Menstrual Cycle Variations in Oestradiol and Progesterone Have No Impact on In Vivo Medial Gastrocnemius Tendon Mechanical Properties,” Clin. Biomech., 24(6), pp. 504–509. [CrossRef]
Kubo, K. , Miyamoto, M. , Tanaka, S. , Maki, A. , Tsunoda, N. , and Kanehisa, H. , 2008, “ Muscle and Tendon Properties During Menstrual Cycle,” Int. J. Sports Med., 30(2), pp. 139–143. [CrossRef] [PubMed]
Lujan, T. J. , Underwood, C. J. , Jacobs, N. T. , and Weiss, J. A. , 2009, “ Contribution of Glycosaminoglycans to Viscoelastic Tensile Behavior of Human Ligament,” J. Appl. Physiol. (1985), 106(2), pp. 423–431. [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]


Grahic Jump Location
Fig. 1

Pretest supraspinatus tendon. Tendons were secured in custom grips prior to undergoing ramp to failure or fatigue tensile testing. Verhoeff's stain was used to delineate the junction between the humeral head and tendon as well as 8 mm distally (concealed by grip). Dots were applied to the humeral head and tendon to permit optical tracking.

Grahic Jump Location
Fig. 2

Supraspinatus quasi-static and viscoelastic properties. Male tendons were significantly larger than female and OVX tendons and OVX tendons were significantly larger than female tendons (a). There were no significant differences in transition strain (b) or percent relaxation (c) across sex. Data represented as mean and standard deviation. Significant differences are indicated by solid bars (p < 0.05/3) and trends are indicated by dashed lines (p < 0.1/3).

Grahic Jump Location
Fig. 3

Toe and linear modulus and stiffness. There were no differences in toe or linear moduli across groups (a). Male supraspinatus tendons were stiffer than female and OVX tendons in toe and linear regions (b). Data represented as mean and standard deviation, n = 12/group. Significant differences are indicated by solid bars (p < 0.05/3) and trends are indicated by dashed lines (p < 0.1/3).

Grahic Jump Location
Fig. 4

Dynamic properties. Male supraspinatus tendons had significantly decreased |E|freq than female and OVX tendons (a). There was a trend toward an increase in tan(δ) in females compared to OVX at 10 Hz (b). Non-normal data sets include tan(δ) for females and OVX rats at 5 Hz and males at 10 Hz. Data represented as mean and standard deviation, n = 12/group. Significant differences are indicated by solid bars (p < 0.05/3) and trends are indicated by dashed lines (p < 0.1/3).

Grahic Jump Location
Fig. 5

Fatigue properties. Male supraspinatus tendons had significantly decreased |E|fat than female and OVX tendons (a) while females had decreased kfat compared to other groups (b). Hysteresis was greater in male tendons than female and OVX tendons (c). There were no significant differences in laxity at 50% fatigue life (d). Data represented as mean and standard deviation, n = 12/group. Significant differences are indicated by solid bars (p < 0.05/3) and trends are indicated by dashed lines (p < 0.1/3).

Grahic Jump Location
Fig. 6

Supraspinatus muscle fiber characterization. Male, female, and OVX fresh frozen muscle sections were stained for laminin (cell borders/red), MyHC type 2a (light gray/green), MyHC type 2b (dark gray/blue), MyHC type 2x (black/unstained), and MyHC type 1 fibers (not pictured) (a). Male fibers had increased average size compared to female fibers in deep (b) and superficial (c) muscle. There were no differences in regional distribution of fiber type across sex in deep (d) or superficial (e) muscle. Data represented as mean and standard deviation, n = 8/group. Significant differences are indicated by solid bars (p < 0.05/3) and trends are indicated by dashed lines (p < 0.1/3).

Grahic Jump Location
Fig. 7

Supraspinatus tendon histology. Supraspinatus tendons from male, female, and OVX (a) rats are pictured. There were no significant differences in cell density (b) or cell shape (c). Data represented as mean and standard deviation, n = 8/group.

Grahic Jump Location
Fig. 8

Tendon-specific sex differences in mechanical properties. Ratio of male to female means were taken for each parameter. Data that were significantly different between male and female supraspinatus or Achilles tendons are indicated by * and ‡, respectively. There were significant differences in dynamic and fatigue mechanical properties in both supraspinatus and Achilles tendons. Male supraspinatus tendons had higher stiffness while male Achilles tendons had lower elastic moduli compared to female tendons. No direct comparisons were made between supraspinatus and Achilles tendon property male:female ratio. Achilles tendon data referenced here has been previously published [3]. Dotted line represents a ratio of 1.0. CA: cross-sectional area, TM: toe modulus, LM: linear modulus, TS: toe stiffness, LS: linear stiffness, DM: |E|freq (1Hz), TD: tan(δ), H: hysteresis, SM: |E|fat, SS: kfat.



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