Functionally distinct tendon fascicles exhibit different creep and stress relaxation behaviour

Abstract

Most overuse tendinopathies are thought to be associated with repeated microstrain below the failure threshold, analogous to the fatigue failure that affects materials placed under repetitive loading. Investigating the progression of fatigue damage within tendons is therefore of critical importance. There are obvious challenges associated with the sourcing of human tendon samples for in vitro analysis so animal models are regularly adopted. However, data indicates that fatigue life varies significantly between tendons of different species and with different stresses in life. Positional tendons such as rat tail tendon or the bovine digital extensor are commonly applied in in vitro studies of tendon overuse, but there is no evidence to suggest their behaviour is indicative of the types of human tendon particularly prone to overuse injuries. In this study, the fatigue response of the largely positional digital extensor and the more energy storing deep digital flexor tendon of the bovine hoof were compared to the semitendinosus tendon of the human hamstring. Fascicles from each tendon type were subjected to either stress or strain controlled fatigue loading (cyclic creep or cyclic stress relaxation respectively). Gross fascicle mechanics were monitored after cyclic stress relaxation and the mean number of cycles to failure investigated with creep loading. Bovine extensor fascicles demonstrated the poorest fatigue response, while the energy storing human semitendinosus was the most fatigue resistant. Despite the superior fatigue response of the energy storing tendons, confocal imaging suggested a similar degree of damage in all three tendon types; it appears the more energy storing tendons are better able to withstand damage without detriment to mechanics.

Shear load transfer in high and low stress tendons

“…more fascicles per transverse unit length) compared to fascicles in the low stress tendon (C. T. Thorpe, Klemt, et al 2013; Shepherd et al 2014). Although the differences seen in the fascicles per transverse unit length may be a result of either fascicle size or packing, qualitative analysis of the images supported a difference in fascicle packing (Fig.…”

“…L.-Y. Woo et al 1981; Blanton and Biggs 1970; Benedict, Walker, and Harris 1968; Shepherd et al 2014). This study indicates that differences in mechanical behavior between high and low stress tendons are also present when lacerations increase internal shear.…”

“…Interestingly, it has been reported that stress relaxation is greater in bovine digital extensor, a largely positional tendon, than the deep digital flexor, a more energy storing tendon (Shepherd et al 2014), indicating not only a difference in mechanical strength but also in time-dependent adaptation to loading between tissue types. Although there has been little investigation into why these differences are present, it has been shown that inter-fascicular binding is greater in the flexor tendon and that fascicles in the bovine deep digital flexor tendon are less linearly oriented along the length of the tendon than fascicles in the digital extensor tendon (Shepherd et al 2014). The difference in angulation of fascicles has also been confirmed by demonstrating a greater helical pitch angle in equine energy storing (superficial digital flexor) tendons than positional tendons (common digital extensor) (C.…”

Molecular level detection and localization of mechanical damage in collagen enabled by collagen hybridizing peptides

“…These results support previous studies on fatigue damage in tendon that demonstrated low-level fatigue damage, indicated by changes in material behaviour and tissue morphology, after only 160 cycles of creep-fatigue loading that reached peak strains of 6–7% (ref. 32) and reductions in modulus and failure stress for tendon subjected to 300 cycles of creep-fatigue loading to 25 or 60% of the tissue tensile failure stress5259. This evidence of low-cycle fatigue damage in tendon, CF-CHP binding accumulation with repeated subfailure loading, and collagen molecular damage in the absence of fiber-scale tissue disruption suggest that subfailure damage may initiate as collagen triple helix unfolding long before progressing to disruption or damage of structures at larger physical scales, and collagen unfolding may even precede detectable changes in tissue material behaviour.…”

The (dys)functional extracellular matrix

“…Repeated subrupture loading results in collagen fibril kinking [102], which can affect cell morphology and matrix degradation [103]. These mechanisms of microdamage accumulation may be tendon type [104] and age specific [105]. …”