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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.

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Figures

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.

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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).

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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).

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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).

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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.

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