Mechanical properties of the different rotator cuff tendons in the rat are similarly and adversely affected by age

Abstract

Rotator cuff tendon tears and tendinopathies are common injuries affecting a large portion of the population and can result in pain and joint dysfunction. Incidence of rotator cuff tears significantly increases with advancing age, and up to 90% of these tears involve the supraspinatus. Previous literature has shown that aging can lead to inferior mechanics, altered composition, and changes in structural properties of the supraspinatus. However, there is little known about changes in supraspinatus mechanical properties in context of other rotator cuff tendons. Alterations in tendon mechanical properties may indicate damage and an increased risk of rupture, and thus, the purpose of this study was to use a rat model to define age-related alterations in rotator cuff tendon mechanics to determine why the supraspinatus is more susceptible to tears due to aging than the infraspinatus, subscapularis, and teres minor. Fatigue, viscoelastic, and quasi-static properties were evaluated in juvenile, adult, aged, and geriatric rats. Aging ubiquitously and adversely affected all rotator cuff tendons tested, particularly leading to increased stiffness, decreased stress relaxation, and decreased fatigue secant and tangent moduli in geriatric animals, suggesting a common intrinsic mechanism due to aging in all rotator cuff tendons. This study demonstrates that aging has a significant effect on rotator cuff tendon mechanical properties, though the supraspinatus was not preferentially affected. Thus, we are unable to attribute the aging-associated increase in supraspinatus tears to its mechanical response alone.

Keywords: Aging; Fatigue; Quasi-static; Tendon; Tendon biomechanics; Viscoelasticity.

Figure 1:

Quasi-static viscoelastic mechanical testing protocol for LS, US, SS, IS, and TM. Preconditioning followed by stress relaxations and frequency sweeps at 3% and 6% strain, ending with a ramp to failure.

Figure 2:

Example peak strain vs cycles (% of failure, FL) curve. Fatigue parameters were calculated at breakpoints 1 (BP1), and breakpoints 2 (BP2)

Figure 3:

Cycles to failure was increase in US aged and IS geriatric animals (A). Cross sectional area (CSA) increased in US and IS geriatric groups (A, B). Data presented as mean +/− standard deviation, bars indicate significance (p<0.05).

Figure 4:

Linear stiffness increased in all tendons in aged animals (A), and toe stiffness increased in LS, US, and IS (B). Data presented as mean +/− standard deviation, bars indicate significance (p<0.05).

Figure 5:

Stress relaxation was significantly reduced compared to the juvenile animals in all tendons at 6% strain (A). No changes were found in tan(δ) at 6% strain (B) (only 10Hz shown). Dynamic modulus increased in LS at 6% strain in geriatric rats (C). Stress relaxation decreased in LS, SS, IS, and TM at 3% strain compared to juvenile animals (D). Tan(δ) showed no significant changes at 3% strain (E). Dynamic modulus decreased in SS geriatric tendons at 3% strain (F). Data presented as mean +/− standard deviation, bars indicate significance (p<0.05).

Figure 6:

Significant decrease was seen in LS, SS, and IS secant modulus at BP2 (A). BP2 Secant stiffness decreases in US and IS with age (B). Tangent modulus decreased in LS, US, and IS in aging tendons at BP2 (C). Secant modulus decreased in LS and IS with aging at BP1 (D). No differences were found in secant stiffness at BP1 (E). Tangent modulus significantly decreased at BP1 with aging in LS and IS (F). Data presented as mean +/− standard deviation, bars indicate significance (p<0.05).

Figure 7:

Hysteresis was significantly altered in all tendons with aging at BP2 (A). BP1 peak strain and laxity peaked in aging LS, SS, and IS tendons (B, C). LS and SS hysteresis increased with age at BP1 (D). IS peak strain increases in IS adult tendons at BP1 (E). Laxity at BP1 only peaked in LS aged tendons (F). Data presented as mean +/− standard deviation, bars indicate significance (p<0.05).