Plasticity of muscle architecture after supraspinatus tears

Abstract

Study design: Controlled laboratory study.

Objectives: To measure the architectural properties of rat supraspinatus muscle after a complete detachment of its distal tendon.

Methods: Supraspinatus muscles were released from the left humerus of 29 Sprague-Dawley rats (mass, 400-450 g), and the animals were returned to cage activity for 2 weeks (n=12), 4 weeks (n=9), or 9 weeks (n=8), before euthanasia. Measurements of muscle mass, pennation angle, fiber bundle length (sarcomere number), and sarcomere length permitted calculation of normalized fiber length, serial sarcomere number, and physiological cross-sectional area.

Results: Coronal oblique sections of the supraspinatus confirmed surgical transection of the supraspinatus muscle at 2 weeks, with reattachment by 4 weeks. Muscle mass and length were significantly lower in released muscles at 2 weeks, 4 weeks, and 9 weeks. Sarcomere lengths in released muscles were significantly shorter at 2 weeks but not different by 4 weeks. Sarcomere number was significantly reduced at 2 and 4 weeks, but returned to control values by 9 weeks. The opposing effects of smaller mass and shorter fibers produced significantly smaller physiological cross-sectional area at 2 weeks, but physiological cross-sectional area returned to control levels by 4 weeks.

Conclusions: Release of the supraspinatus muscle produced early radial and longitudinal atrophy of the muscle. The functional implications of these adaptations would be most profound at early time points (particularly relevant for rehabilitation), when the muscle remains smaller in cross-sectional area and, due to reduced sarcomere number, would be forced to operate over a wider range of the length-tension curve and at higher velocities, all adaptations resulting in compromised force-generating capacity. These data are relevant to physical therapy because they provide tissue-level insights into impaired muscle and shoulder function following rotator cuff injury.

Figure 1

Coronal oblique histological sections (stained with Masson's trichrome) of control and tear shoulders at 2 weeks and 4 weeks. The supraspinatus tendon (arrow) is intact in both control shoulders. While the supraspinatus tendon is detached on the tear side at 2 weeks, it has reattached to the humerus at 4 weeks. In this case, the tendon is qualitatively longer and thinner than on the control side.

Figure 2

Relative mass (A), muscle length (B), sarcomere length (C), serial sarcomere number (D), pennation angle (E), and physiological cross sectional area (PCSA) (F) from the supraspinatus muscles as a function of time. At 2 weeks, each variable (with the exception of pennation angle) was significantly reduced compared to the control side. At 4 weeks, mass, muscle length, and sarcomere number remain lower, but sarcomere length and PCSA have returned to control levels. At 9 weeks, only muscle mass and length remain less than control values. Data are presented as a percentage of the intact control shoulder (mean ± SE). * indicates significantly different (p<0.05) compared to 4 and 9 weeks, † indicates significantly different (p<0.05) from the control side.

Figure 3

Schematic representation of the time course of architectural changes in the detached supraspinatus muscle. When the supraspinatus muscle is acutely detached (A-B), the muscle retracts, muscle mass declines, sarcomere length shortens as the muscle recoils, sarcomere number declines, and physiological cross sectional area declines. When the supraspinatus muscle reattaches itself (B-C) in this model, the tendon becomes longer because the muscle cannot lengthen itself before reattaching. At this point, the muscle has the capacity to generate resisted tension which may explain why sarcomere length, sarcomere number, and PCSA return to control levels. The reduction in muscle length at this time point is likely due to a reduction in serial fiber number.