Muscle and Tendon Adaptation in Adolescence: Elite Volleyball Athletes Compared to Untrained Boys and Girls

Abstract

Though the plasticity of human tendons is well explored in adults, it is still unknown how superimposed mechanical loading by means of athletic training affects the properties of tendons during maturation. Due to the increased responsiveness of muscle to mechanical loading, adolescence is an important phase to investigate the effects of training on the mechanical properties of tendons. Hence, in the present study we compared vastus lateralis (VL) architecture, muscle strength of the knee extensor muscles and patellar tendon mechanical properties of male and female adolescent elite athletes to untrained boys and girls. Twenty-one adolescent volleyball athletes (A; 16.7 ± 1 years; 12 boys, 9 girls) and 24 similar-aged controls (C; 16.7 ± 1 years; 12 boys and girls, respectively) performed maximum isometric contractions on a dynamometer for the assessment of muscle strength and, by integrating ultrasound imaging, patellar tendon mechanical properties. Respective joint moments were calculated using an inverse dynamics approach and an electromyography-based estimation of antagonistic contribution. Additionally, the VL pennation angle, fascicle length and muscle-thickness were determined in the inactive state by means of ultrasound. Adolescent athletes produced significantly greater knee extension moments (normalized to body mass) compared to controls (A: 4.23 ± 0.80 Nm/kg, C: 3.57 ± 0.67 Nm/kg; p = 0.004), and showed greater VL thickness and pennation angle (+38% and +27%; p < 0.001). Tendon stiffness (normalized to rest length) was also significantly higher in athletes (A: 86.0 ± 27.1 kN/strain, C: 70.2 ± 18.8 kN/strain; p = 0.04), yet less pronounced compared to tendon force (A: 5785 ± 1146 N, C: 4335 ± 1015 N; p < 0.001), which resulted in higher levels of tendon strain during maximum contractions in athletes (A: 8.0 ± 1.9%, C: 6.4 ± 1.8%; p = 0.008). We conclude that athletic volleyball training provides a more efficient stimulus for muscle compared to tendon adaptation, which results in an increased demand placed upon the tendon by the working muscle in adolescent volleyball athletes. Besides implications for sport performance, these findings might have important consequences for the risk of tendon overuse injury.

The Free Achilles Tendon Is Shorter, Stiffer, Has Larger Cross-Sectional Area and Longer T2* Relaxation Time in Trained Middle-Distance Runners Compared to Healthy Controls

“…Young’s modulus (GPa) of the free Achilles tendon was calculated by obtaining the slope of the line fitted to the linear region of the tendon stress-strain curve measured at 25, 50, and 70% active muscle contraction conditions. Length normalised mechanical stiffness (kN/strain) was calculated as the product of free Achilles tendon mechanical stiffness and resting length ( Mersmann et al, 2017 ). Free Achilles tendon length calculated from freehand 3DUS data during resting scan was used as a reference measure in deformation and strain calculations.…”

Imbalances in the Development of Muscle and Tendon as Risk Factor for Tendinopathies in Youth Athletes: A Review of Current Evidence and Concepts of Prevention

“…Consequently, tendon strain during maximum contractions was not only increased chronically in comparison to controls, but also demonstrated significantly greater fluctuations during the period of investigation (Figure 2 ). In addition to the discordant changes of muscle strength and tendon stiffness that occur during a training process, results of a very recent study indicate that also the adaptive potential, at least in response to predominantly plyometric long-term loading, is lower with regard to tendon stiffness compared to muscle strength in both adolescent boys and girls (Mersmann et al, 2017b ). Though from this study it still remains an assumption that maturation contributed to the development musculotendinous imbalance in addition to the unfavorable type of loading, the increased stress and strain observed in the earlier study (Mersmann et al, 2014 ) in adolescent athletes compared to the adults, which were habitually subjected to intense plyometric loading as well, carefully suggest that the risk might be increased during adolescence.…”

“…However, the interplay of mechanical loading and changes of the hormonal milieu on muscle and tendon plasticity in general, and with regard to adolescence in particular, is still largely unknown. Similarly, though recent evidence demonstrated that an imbalanced musculotendinous adaptation can occur during adolescence (Mersmann et al, 2014 , 2016 , 2017a , b ), it is yet unclear how the likelihood of an imbalanced adaptation develops as a function of maturation and how it relates to specific types of loading.…”

“…The recommendations given in this chapter are based on our current knowledge on tendon adaptation, which is derived from studies on adults. Though it is known that the tendons of pre-pubertal children and adolescents are able to adapt to mechanical loading (Waugh et al, 2014 ; Mersmann et al, 2017b ), dose-response relationships specific for the immature tendinous system still need to be established in the future. However, as we are convinced that the basic mechanisms of mechanotransduction should not be profoundly different in children and adults, we can argue that it is likely that the characteristics of an effective stimulus for tendon adaptation (i.e., high strain magnitude and ~3 s strain duration applied with low frequency) is widely independent of age.…”

Muscle and Tendon Morphology in Early-Adolescent Athletes and Untrained Peers

“…However, there seems to be a disproportionate adaptation to athletic training, leading to a lower ratio of tendon to muscle CSA in athletes. This imbalance might contribute to the mismatch of muscle strength and tendon stiffness that has been reported earlier (Mersmann et al, 2017c;Charcharis et al, 2019), with potential implications for the risk of tendon injury (Simpson et al, 2016;Mersmann et al, 2019). Future research might clarify if mid-to late-adolescence is a period of pronounced tendon plasticity and if tendon adaptation can be promoted earlier during maturation by means of specific interventions.…”