Abstract

Tendon mechanical properties respond to altered load in adults, but how load history during growth affects adult tendon properties remains unclear. To address this question, we adopted an avian model in which we altered the mechanical load environment across the growth span. Animals were divided at 2 weeks of age into three groups: (1) an exercise control group given the opportunity to perform high-acceleration movements (EXE, n = 8); (2) a sedentary group restricted from high-intensity exercise (RES, n = 8); and (3) a sedentary group also restricted from high-intensity exercise and in which the gastrocnemius muscles were partially paralyzed using repeated bouts of botulinum toxin-A injections (RES-BTX, n = 8). Video analysis of bird movement confirmed the restrictions eliminated high-intensity exercise and did not alter time spent walking and sitting between groups. At skeletal maturity (33–35 weeks) animals were sacrificed for analysis, consisting of high-field MRI and material load testing, of both the entire free Achilles tendon and the tendon at the bone-tendon junction. Free tendon stiffness, modulus, and hysteresis were unaffected by variation in load environment. Further, the bone-tendon junction cross-sectional area, stress, and strain were also unaffected by variations in load environment. These results suggest that: (a) a baseline level of low-intensity activity (standing and walking) may be sufficient to maintain tendon growth; and (b) if this lower threshold of tendon load is met, non-mechanical mediated tendon growth may override the load-induced mechanotransduction signal attributed to tendon remodeling in adults of the same species. These results are important for understanding of musculoskeletal function and tendon health in growing individuals.

Highlights

  • Tendon mechanical properties change in response to variations in mechanical load history

  • The spring-like characteristics of the free tendon and the bone-tendon junction were unaffected both after restricting high-intensity exercise and after restricting high-intensity exercise and additional chronic administration of botulinum toxin across the growth period. These results suggest that tendon properties, at least in the bird species studied here, may be resilient to variations in load level during the growth period

  • Modulus and cross sectional area values of the free tendon in all groups are very close to the values reported for comparable control animals in a previous study of adult guinea fowl

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Summary

Introduction

Tendon mechanical properties change in response to variations in mechanical load history. A comparison of adolescent athletes to non-athletes provided indirect evidence that longterm training during growth may result in increased patellar tendon stiffness (Mersmann et al, 2017a; Charcharis et al, 2019). A similar comparison between pre-adolescent athletes and non-athletes, found no differences in Achilles tendon stiffness (Pentidis et al, 2019). Short-term (10-week) resistance training interventions in both typically developing preadolescent children (Waugh et al, 2014) and in children with cerebral palsy (Kalkman et al, 2019) have been shown to increase Achilles tendon stiffness. We are not aware of any longer-term intervention studies of tendon adaptation in human children, but a 1-year longitudinal study tracking adolescent volleyball athletes undergoing strenuous training and minimally active control subjects found no significant between-group differences in the changes in patellar tendon stiffness (Mersmann et al, 2016). In others by these authors (for a review, see Mersmann et al, 2017b), it is proposed that tendon has a slower and less pronounced response to altered load during growth compared to muscle, a phenomenon that may lead to an imbalance in the development of muscle and tendon strength

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