Tendon properties remain altered in a chronic rat rotator cuff model

Abstract

Background: Chronic rotator cuff tears are often associated with pain or poor function. In a rat with only a detached supraspinatus tendon, the tendon heals spontaneously which is inconsistent with how tears are believed to heal in humans.

Questions/purposes: We therefore asked whether a combined supraspinatus and infraspinatus detachment in the rat would fail to heal and result in a chronic injury in the supraspinatus tendon.

Methods: We acutely detached the supraspinatus and infraspinatus tendons in a rat model. At 4, 8, and 16 weeks post-detachment, biomechanical testing, collagen organization, and histological grading were evaluated for the detached supraspinatus and infraspinatus tendons and compared to controls.

Results: In the detached supraspinatus tendon, area and percent relaxation were increased at all time points while the modulus and stiffness were similar to those of controls at 4 and 8 weeks. Collagen disorganization increased at late time points while cellularity increased and cells were more rounded in shape. In the detached infraspinatus tendon, area and percent relaxation were also increased at late time points. However, the modulus values initially decreased followed by an increase in both modulus and stiffness at 16 weeks compared to control. In the detached infraspinatus, we also observed a decrease in collagen organization at all time points and increased cellularity and a more rounded cell shape.

Conclusions: Due to the ongoing changes in mechanics, collagen organization and histology in the detached supraspinatus tendon compared to control animals at 16 weeks, this model may be useful for understanding the human chronic tendon tear.

Clinical relevance: This rat rotator cuff chronic model can be used to test hypotheses regarding injury and repair mechanisms that cannot be addressed in human patients or in cadaveric studies.

Fig. 1

The study design is shown as a graph.

Fig. 2A–D

Geometric and biomechanical properties (n = 12–13) of the time-matched controls and detached supraspinatus tendons are shown at each time point (mean and standard deviation). Comparisons are of detached tendons to time matched controls (p < 0.1 shown). Both (A) area and (B) percent relaxation remained increased from time matched controls, even at the 16-week time point. No differences were seen in (C) modulus or (D) stiffness.

Fig. 3

Collagen angular deviation (n = 3–5) of the time matched controls and detached supraspinatus tendons is shown at each time point (mean and standard deviation). Comparisons are of detached tendons to time matched controls (p < 0.1 shown). Tendon angular deviation remains increased, or decreased organization, even at late time points, suggesting the tendon is not healing.

Fig. 4A–D

(A) Cellularity and (B) cell shape grades for detached supraspinatus are shown; (C) cellularity and (D) cell shape grades for infraspinatus tendons are shown as median and interquartile range due to the nonparametric nature of the data. Comparisons are of detached tendons to time matched controls. Both the supraspinatus and infraspinatus tendons remain altered from controls.

Fig. 5A–B

Representative supraspinatus H&E samples at 16 weeks (200×) are shown. The 16 week uninjured control (A) shows long, spindle shaped fibroblasts aligned between collagen fibers where the 16 week detached supraspinatus tendon (B) shows increased cellularity, more rounded cells and a random distribution of fibroblasts throughout the ECM.

Fig. 6A–B

(A) Modulus and (B) stiffness (n = 12–13) of the time-matched controls and detached infraspinatus tendons are shown at each time point (mean and standard deviation). Comparisons are of detached tendons to time matched controls, p < 0.1 shown. Unlike the supraspinatus tendon, the infraspinatus is seen to have increased modulus and stiffness at the 16 week time point suggesting that the tendon is healing.