The role of Achilles tendon properties in the mechanical function of the human triceps surae

Abstract

The mechanical output of the muscle-tendon unit (MTU) is in part governed by the viscoelastic nature of tendinous tissues. The tendon contributes to beneficial contractile conditions during various types of movement. Yet, knowledge about the modulation of muscle-tendon behaviour under different external constraints and with different tendon stiffness is scarce. Moreover, the role of human tendons has mainly been examined in the context of energy conservation or power amplification and has not been investigated during tasks requiring energy dissipation. Thus, the aim of the present thesis was to examine muscle-tendon interaction: during a landing task; under external constraints (i.e. loading and speed) during landing and running; and after a training-induced increase in tendon stiffness during landing and running.

We conducted a cross-sectional study (A) and a controlled longitudinal study (B), to investigate muscle-tendon interaction during a landing task (n=39 and n=21, respectively) and during running on a treadmill (n=16 and n=21, respectively). In study A, ankle and knee joint mechanics and gastrocnemius and soleus MTU length were derived from kinematic and kinetic data during both tasks. In addition, we synchronised ultrasound with these data to measure Achilles tendon and muscle fascicle length. Loading (+20% of body mass) was added to the subjects using weighted vests after completing the tasks unloaded. Running was performed at preferred speed and increased speed (+20%). In study B, the training group (n = 11) underwent 10 weeks of resistance training consisting of single-leg isometric plantar flexion contractions. Similar measurements as in study A were performed during unloaded landing and unloaded running at preferred speed, additionally including the assessment of plantarflexion force, tendon stiffness and strain, measured during isometric contractions. Repeated-measures ANOVAs were used to test differences in the variables of interest between conditions of task execution (study A) and between baseline and post-training tests (study B).

During landing in study A, the rapid MTU stretch was taken up by the Achilles tendon, while gastrocnemius and soleus fascicles lengthened actively at slower velocities than the MTU. Loading resulted in a greater tendon stretch and higher soleus muscle activity to compensate for the greater negative work during landing, whereas fascicle strains remained unchanged. During running, loading resulted in an increased Achilles tendon recoil – but not elongation -, whereas higher running speed resulted in greater gastrocnemius and soleus muscle activity. Fascicle length and velocity of either muscles were unchanged when imposing external constraints during running. In study B, Achilles tendon stiffness increased by 18%, without a significant reduction in tendon strain during isometric contractions. Increased resting pennation angle and muscle thickness (by 5% each) were accompanied by a 15% increase in plantarflexion strength in the training group but fascicle length was not altered by the training. During landing, longitudinal tendon strain remained similar after training, despite unchanged tendon force and increased tendon stiffness. Fascicle lengthening and velocity were reduced (by 27 and 21%, respectively) after training and, surprisingly, gastrocnemius fascicle length at touchdown was greater (8%). No differences were observed for soleus. During running, tendon elongation did not change after training but tendon recoil was reduced by 30%. Estimated tendon force was similar after training and neither gastrocnemius nor soleus fascicle shortening were affected. Altered gastrocnemius muscle mechanics were nevertheless indicated by greater changes in pennation angle and a higher architectural gear ratio measured during stance. None of the variables changed in the control group after the training duration.

The results showed that during landing, the rapid MTU stretch was buffered by the Achilles tendon to delimit muscle fascicle strains. Additional loading was taken up by the tendon and was met by increased soleus muscle activity, effectively preserving the contractile length and velocity of muscle fascicles. Similarly, fascicle behaviour was preserved during running with load and at increased speed. We observed different strategies to increase ankle joint work under the two constraints; higher elastic energy utilisation was favoured with added load, whereas increasing speed resulted in higher muscle activity. The training-induced increase in Achilles tendon stiffness also altered muscle-tendon behaviour during landing and running. During landing, the buffering action of the tendon was not limited despite similar forces and increased tendon stiffness. Mechanisms for the reduction in gastrocnemius lengthening and greater length at touch-down during landing remain to be determined. During running, gastrocnemius and soleus fascicle shortening patterns were preserved, despite a reduced tendon recoil. Increased gastrocnemius gear ratio during stance may explain asymmetrical changes in tendon stretch and recoil and may suggest that elastic energy was stored differently after training.

Within the limits of the experimental conditions of the present thesis, fascicle behaviour seems little affected by changes in external constraints (i.e. speed and load) or increased tendon stiffness during landing and running, whereas soleus seems less affected than gastrocnemius. Instead, most conditions were modulated by elastic energy storage or by muscle activity. We suggest that energy storage and contraction behaviour were influenced by changes in aponeurosis stiffness and can therefore not be fully explained by simple in series models.

Paper I: Werkhausen, A., Albracht, K., Cronin, N. J., Meier, R., Bojsen-Møller, J., & Seynnes, O. R. (2017). Modulation of muscle-tendon interaction in the human triceps surae during an energy dissipation task. The Journal of Experimental Biology, 220(22), 4141.

Paper II: Werkhausen, A., Albracht, K., Cronin, N. J., Paulsen, G., Bojsen-Møller, J., & Seynnes, O. R. (2018). Effect of Training-Induced Changes in Achilles Tendon Stiffness on Muscle–Tendon Behavior During Landing. Frontiers in Physiology, 9, 794.

Paper III: Werkhausen, A., Cronin, N. J., Albracht, K., Bojsen-Møller, J., & Seynnes, O. R.. Distinct muscle-tendon interaction during running at different speeds and in different loading conditions. In review Journal of Applied Physiology.

Paper IV: Werkhausen, A., Cronin, N. J., Albracht, K., Paulsen, G., Larsen, A.V., Bojsen-Møller, J., & Seynnes, O. R.. Training-induced increase in Achilles tendon stiffness affects tendon strain and muscle contraction behaviour during running. Submitted to PeerJ.