Diabetes alters mechanical properties and collagen fiber re-alignment in multiple mouse tendons

Abstract

Tendons function to transfer load from muscle to bone through their complex composition and hierarchical structure, consisting mainly of type I collagen. Recent evidence suggests that type II diabetes may cause alterations in collagen structure, such as irregular fibril morphology and density, which could play a role in the mechanical function of tendons. Using the db/db mouse model of type II diabetes, the diabetic skin was found to have impaired biomechanical properties when compared to the non-diabetic group. The purpose of this study was to assess the effect of diabetes on biomechanics, collagen fiber re-alignment, and biochemistry in three functionally different tendons (Achilles, supraspinatus, patellar) using the db/db mouse model. Results showed that cross-sectional area and stiffness, but not modulus, were significantly reduced in all three tendons. However, the tendon response to load (transition strain, collagen fiber re-alignment) occurred earlier in the mechanical test, contrary to expectations. In addition, the patellar tendon had an altered response to diabetes when compared to the other two tendons, with no changes in fiber re-alignment and decreased collagen content at the midsubstance of the tendon. Overall, type II diabetes alters tendon mechanical properties and the dynamic response to load.

Figure 1

(A) Cross-sectional area and (B) transition strain are significantly reduced in the diabetic supraspinatus (SST), Achilles (ACH), and patellar (PT) tendons.

Figure 2

(A) Stiffness at the insertion site is significantly reduced in the diabetic tendons for all three tendons. (B) Modulus is also significantly reduced with diabetes in the Achilles tendon. Midsubstance results show no differences between the groups in stiffness or modulus in any tendon.

Figure 3

(A) The Achilles tendons had significantly more collagen at the midsubstance than at the insertion site but there was no difference due to diabetes. The patellar tendons had increased collagen at the midsubstance in the non-diabetic group, which was not present in the diabetic group. In addition, the patellar tendon midsubstance in the diabetes group was significantly lower than the non-diabetic group. (B) GAG content was not different in any group between the non-diabetic and diabetic groups. However, the supraspinatus non-diabetic tendons had more GAGs at the insertion than the midsubstance and the Achilles tendons in both groups had more GAGs at the midsubstance than the insertion site.

Figure 4

At the insertion site, diabetic supraspinatus tendons re-aligned during preconditioning and in the linear region, while only in the linear region in the non-diabetic group. At the midsubstance, there was no difference between the diabetic and non-diabetic groups with re-alignment occurring in the linear region in both groups. Results here show are representative samples showing the population statistics, where the bold lines represent a significant change in circular variance during the region shown on the y-axis.

Figure 5

At the insertion site, diabetic Achilles tendons re-aligned during preconditioning while the non-diabetic tendons re-aligned during the toe region of the test. At the midsubstance, both groups re-aligned during the preconditioning and linear region of the mechanical test. Results here show are representative samples showing the population statistics, where the bold lines represent a significant change in circular variance during the region shown on the y-axis.

Figure 6

In the patellar tendons, there were no significant differences in re-alignment between the non-diabetic and diabetic tendons at either location. Results here show are representative samples showing the population statistics, where the bold lines represent a significant change in circular variance during the region shown on the y-axis.

Figure 7

Summary of findings for significant changes with diabetes are shown here where a down arrow indicates that the diabetes group was significantly less than the control group in that parameter and a change in re-alignment is noted by ‘Earlier’, meaning that the diabetes group re-aligned earlier in the mechanical test.