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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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Figures

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.

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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.

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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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