Reduced Achilles Tendon Stiffness Disrupts Calf Muscle Neuromechanics in Elderly Gait

Abstract

Older adults walk slower and with a higher metabolic energy expenditure than younger adults. In this review, we explore the hypothesis that age-related declines in Achilles tendon stiffness increase the metabolic cost of walking due to less economical calf muscle contractions and increased proximal joint work. This viewpoint may motivate interventions to restore ankle muscle-tendon stiffness, improve walking mechanics, and reduce metabolic cost in older adults.

Keywords: Aging; Ankle exoskeleton; Biomechanics; Energy expenditure; Muscle mechanics; Stiffness.

Fig 1.

We propose the novel hypothesis that an age-related decline in Achilles tendon stiffness (k_t) increases the metabolic cost of walking due to less economical triceps surae muscle contractions and increased proximal joint work (D). Conceptually, in order for older adults to maintain tuned ankle neuromechanical function to the level of young adults during walking (in the presence of reduced k_t), they must operate at shorter triceps surae lengths and higher excitations (B); a metabolically costly adaptation that, due to reduced force-generating potential, yields lower force per unit activation (C). Upper limits on triceps surae muscle recruitment (i.e., 100% activation) impose a threshold above which age-related decreases in Achilles tendon stiffness cannot be surmounted via the local adaptive response of increased triceps surae activation (α). Thus, older adults exhibit characteristic compensatory redistributions of mechanical workload to muscles spanning the hip which, due to differences in anatomical architecture compared to those spanning the ankle, further increase the metabolic cost of walking (A).

Fig 2.

(A) Achilles tendon stiffness given as the association between Achilles tendon force and Achilles tendon length in young (gray) and older (black) adults adapted from Onambele et al. (2006). (B) Correlations between peak net ankle moment and gastrocnemius (GAS) and soleus (SOL) subtendon tissue displacement in n=9 young (gray, closed circles) and n=10 older (black, open circles) adults, adapted from Clark and Franz [2019]. (C) Illustrations depict the dependence of ankle muscle-tendon unit stiffness (k_mtu) on muscle activation (α), muscle stiffness (k_m), and Achilles tendon stiffness (k_t). (D) Illustration depicts the dependence of ankle joint stiffness (k_A) on muscle activation, net ankle moment (M_A) and ankle angle (θ_A). Plot shows ankle joint stiffness, given as the slope of net ankle moment and ankle angle, during isokinetic eccentric contractions of the triceps surae mucles at a matched activation of 75% MVIC, prescribed via biofeedback, in n=9 young (gray) and n=8 older (black) adults, adapted from Krupenevich et al. 2020.

Fig 3.

(A) Simulated gastrocnemius (GAS) and soleus (SOL) excitation (top) and fiber length (bottom) plotted over an average stance phase as a function of Achilles tendon stiffness, adapted from Orselli et al. (2017). The small arrows indicate reduced Achilles tendon stiffness (k_t), and large arrows indicate the direction of change in excitation and fiber length with reduced k_t. Thus, as k_t is reduced, GAS and SOL excitation increases, and fiber length decreases. (B) Average gastrocnemius fascicle length (adapted from Browne and Franz [2019]) and peak soleus activation reported as a percent of maximum voluntary isometric contraction (i.e., %MVC) (adapted from Franz and Kram [2013]) during walking in young (gray) and older (black) adults. (C) Soleus muscle stiffness, given by the relationship between soleus muscle force and soleus muscle length, in young adults during isokinetic eccentric contractions of the triceps surae mucles as a function of muscle activation (α - indicated with the large arrow from α =0% to α=75%) prescribed via biofeedback, adapted from Clark and Franz [2019]. (D) Model-predicted effects of peak Achilles tendon strain (ε_o) on gastrocnemius (GAS) and soleus (SOL) mass-normalized metabolic energy consumption. The small arrow indicates reduced k_t, and the large arrow indicates the direction of change in SOL and GAS metabolic energy with reduced k_t.

Fig 4.

Illustration of the proposed effect of elastic ankle exoskeleton assistance on mitigating age-related changes in triceps surae muscle length-tension behavior that arise from reduced Achilles tendon stiffness during walking. The left column illustrates the hypothesized effect of age-related reductions in Achilles tendon stiffness (k_t) on muscle length-tension behavior, where reduced k_t in older adults results in shorter fascicle lengths (l/l₀) and associated reductions in muscle force F/F_max). The center column illustrates the effect of exoskeleton assistance on muscle length-tension behavior, where τ_exo indicates the extensor torque applied about the ankle from the exoskeleton, k_exo indicates the rotational stiffness of the exoskeleton, and Δθ_A indicates the change in ankle angle. The exoskeleton behaves as a rotational spring (τ_exo=k_rot*Δθ_A), adding structural stiffness to the biological triceps surae muscle-tendon units. The right column illustrates the proposed effect of exoskeleton assistance in older adults. The exoskeleton acts to bypass age-related reductions in k_t via exoskeleton-applied torque (τ_exo), which effectively reduces the demand on the triceps surae muscle-tendon units and allows the triceps surae muscles to operate at a longer lengths (l/l₀) and lower activations (α).