Asynchronous muscle and tendon adaptation after surgical tensioning procedures

Abstract

Background: Donor muscles are often highly stretched in tendon transfer surgery. Despite literature reports that showed adaptation of the serial sarcomere number to moderate stretch, little is known regarding adaptation to stretch outside of the physiological range (commonly seen in clinical tendon transfer). This study was performed to evaluate muscle-tendon-unit adaptation to tendon transfer surgery in an animal model.

Methods: Thirty-seven male New Zealand White rabbits were used for muscle analysis, and twenty-five of those rabbits were also used for biological analysis of the tendons after the experiment. The extensor digitorum muscle of the second toe was transferred at a specific sarcomere length of 3.7 microm, chosen to be near the end of the descending limb of the rabbit sarcomere length-tension curve. Animals were killed at five time points, at which complete muscle architectural analysis as well as measurements of tendon dimension, tendon water content, and tendon cytokine transcript levels were performed.

Results: As expected, a rapid increase in the serial sarcomere number (mean and standard error of the mean, 4658 +/- 154 in the transferred muscle compared with 3609 +/- 80 in the control muscle) was found one week after the surgery. From this time point until eight weeks, this increased serial sarcomere number paradoxically decreased, while the sarcomere length remained constant. Eventually, at eight weeks, it reached the same value (3749 +/- 83) as that in the control muscle (3767 +/- 61). Tendon adaptation was delayed relative to muscle adaptation, but it was no less dramatic. Tendon length increased by 1.43 +/- 0.74 mm over the eight-week time period, corresponding to a strain of 15.55% +/- 4.08%.

Conclusions: To our knowledge, this is the first report of biphasic adaptation of the serial sarcomere number followed by tendon adaptation, and it indicates that muscle adapts more quickly than tendon does. Taken together, these results illustrate a complex and unique interaction between muscles and tendons that occurs during adaptation to stretching during tendon transfer.

Fig. 1

A: Schematic diagram of the surgical procedure in this experiment. The tendon of the extensor digitorum muscle of the second toe (broken lines) was translocated (black solid lines) into the extensor retinaculum (arrowhead). B: An inclusive view of the surgical field after completion of the transfer. A laser diffraction device was applied intraoperatively to the most distal fiber bundle (circle) of the extensor digitorum to measure sarcomere length. Suture markers (arrows) were placed at the proximal end of the muscle and at the myotendinous junction to track the changes in the lengths of both the muscle and the tendon. C: Close-up view of the suture site shown by the broken line in B. The tendon was sutured to itself with at least seven knots after it was looped back around the extensor retinaculum (arrowhead). The scale bars represent 2 cm in B and C.

Fig. 2

Raw fiber length (A), sarcomere length (B), and serial sarcomere number (C) of the transferred muscle over the course of the experiment. The x axes denote the period after the operation. The horizontal solid and dashed lines represent the grand mean and the standard error of the mean, respectively, for the control-muscle values. #Significantly different (p < 0.05) compared with the corresponding control-muscle value. †Significantly different (p < 0.05) compared with the value in the one-day group.

Fig. 3

Elongation of the muscle-tendon unit expressed as absolute values (millimeters) (A) and elongation of the muscle (B) and the tendon (C) expressed as strain values (the length change divided by the initial length at the time of the surgery) over the course of the experiment. In A, the muscle length change (white bars) and the tendon length change (hatched bars) are stacked in one bar. The x axes denote the period after the operation. *P < 0.05. **P < 0.01. There were no differences between the values expressed by the absolute scale and those expressed by the strain scale.

Fig. 4

Expression levels of insulin-like growth factor-1 (IGF-1) (A) and transforming growth factor-β1 (TGF-β1) (B) mRNAs in the contralateral, control tendons (white bars) and the transferred tendons (gray bars) are presented as fold changes relative to 18S rRNA values. The x axes denote the period after the operation. #Significantly different (p < 0.05) compared with the corresponding control-tendon value. †A significant difference (p < 0.05) between the one-day and four-week groups of transferred tendons.

Fig. 5

Expression levels of interleukin-6 (IL-6) (A), IL-8 (B), and cyclooxygenase-2 (COX-2) (C) mRNAs in the contralateral, control tendons (white bars) and the transferred tendons (gray bars) are presented as fold changes relative to 18S rRNA values. The x axes denote the period after the operation. #Significantly different (p < 0.05) compared with the corresponding control-tendon value. ‡A significant difference (p < 0.05) between the one-day group and the other groups of transferred tendons.

Fig. 6

Expression levels of matrix metalloproteinase-1 (MMP-1) (A), MMP-3 (B), and MMP-13 (C) mRNAs in the contralateral, control tendons (white bars) and the transferred tendons (gray bars) are presented as fold changes relative to 18S rRNA values. The x axes denote the period after the operation. #Significantly different (p < 0.05) compared with the corresponding control-tendon value. †A significant difference (p < 0.05) between the transferred tendons at the two different time points.