Fascicles and the interfascicular matrix show adaptation for fatigue resistance in energy storing tendons

Chavaunne T Thorpe,Graham P Riley,Helen L Birch,Peter D Clegg,Hazel R.C Screen

doi:10.1016/j.actbio.2016.06.012

Abstract

Tendon is composed of rope-like fascicles, bound together by interfascicular matrix (IFM). Our previous work shows that the IFM is critical for tendon function, facilitating sliding between fascicles to allow tendons to stretch. This function is particularly important in energy storing tendons, which experience extremely high strains during exercise, and therefore require the capacity for considerable inter-fascicular sliding and recoil. This capacity is not required in positional tendons. Whilst we have previously described the quasi-static properties of the IFM, the fatigue resistance of the IFM in functionally distinct tendons remains unknown. We therefore tested the hypothesis that fascicles and IFM in the energy storing equine superficial digital flexor tendon (SDFT) are more fatigue resistant than those in the positional common digital extensor tendon (CDET). Fascicles and IFM from both tendon types were subjected to cyclic fatigue testing until failure, and mechanical properties were calculated. The results demonstrated that both fascicles and IFM from the energy storing SDFT were able to resist a greater number of cycles before failure than those from the positional CDET. Further, SDFT fascicles and IFM exhibited less hysteresis over the course of testing than their counterparts in the CDET. This is the first study to assess the fatigue resistance of the IFM, demonstrating that IFM has a functional role within tendon and contributes significantly to tendon mechanical properties. These data provide important advances into fully characterising tendon structure-function relationships. Statement of SignificanceUnderstanding tendon-structure function relationships is crucial for the development of effective preventative measures and treatments for tendon injury. In this study, we demonstrate for the first time that the interfascicular matrix is able to withstand a high degree of cyclic loading, and is specialised for improved fatigue resistance in energy storing tendons. These findings highlight the importance of the interfascicular matrix in the function of energy storing tendons, and potentially provide new avenues for the development of treatments for tendon injury which specifically target the interfascicular matrix.

Highlights

IntroductionEnergy storing tendons, such as the human Achilles and patellar tendons, play an important role in locomotory efficiency, decreasing the energetic cost associated with movement [1, 2]
Energy storing tendons, such as the human Achilles and patellar tendons, play an important role in locomotory efficiency, decreasing the energetic cost associated with movement [1, 2].To enable this function, energy storing tendons have distinct mechanical properties, such as greater extensibility and elasticity leading to improved energy storage and return, when compared to tendons that are purely positional in function, such as the anterior tibialis tendon [1, 3,4,5]
Fascicle hysteresis was significantly greater in the common digital extensor tendon (CDET) than in the superficial digital flexor tendon (SDFT) at all time points that were assessed (p < 0.01)

Summary

Introduction

Energy storing tendons, such as the human Achilles and patellar tendons, play an important role in locomotory efficiency, decreasing the energetic cost associated with movement [1, 2]. To enable this function, energy storing tendons have distinct mechanical properties, such as greater extensibility and elasticity leading to improved energy storage and return, when compared to tendons that are purely positional in function, such as the anterior tibialis tendon [1, 3,4,5]. Fascicles are bound together by the interfascicular matrix (IFM), which is the largest hierarchical level of ground substance, and is referred to as the endotenon. The IFM is rich in glycoproteins, elastin and collagens [9,10,11]

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