Mechanical and energetic determinants of impaired gait following stroke: segmental work and pendular energy transduction during treadmill walking

Abstract

Systems biology postulates the balance between energy production and conservation in optimizing locomotion. Here, we analyzed how mechanical energy production and conservation influenced metabolic energy expenditure in stroke survivors during treadmill walking at different speeds. We used the body center of mass (BCoM) and segmental center of mass to calculate mechanical energy production: external and each segment's mechanical work (Wseg). We also estimated energy conservation by applying the pendular transduction framework (i.e. energy transduction within the step; Rint). Energy conservation was likely optimized by the paretic lower-limb acting as a rigid shaft while the non-paretic limb pushed the BCoM forward at the slower walking speed. Wseg production was characterized by greater movements between the limbs and body, a compensatory strategy used mainly by the non-paretic limbs. Overall, Wseg production following a stroke was characterized by non-paretic upper-limb compensation, but also by an exaggerated lift of the paretic leg. This study also highlights how post-stroke subjects may perform a more economic gait while walking on a treadmill at preferred walking speeds. Complex neural adaptations optimize energy production and conservation at the systems level, and may fundament new insights onto post-stroke neurorehabilitation.This article has and associated First Person interview with the first author of the paper.

Keywords: Energetics; Gait; Mechanics; Oxygen consumption; Rehabilitation; Stroke.

Conflict of interest statement

Competing interestsThe authors declare no competing or financial interests.

© 2020. Published by The Company of Biologists Ltd.

Figures

Fig. 1.

Changes in mechanical work and cost of transport following chronic neural adaptations to loss of upper-motor neuron control. (A) Stroke causes loss of upper-motor neuron control over voluntary movements, leading to weakness, abnormal tonus and spasticity at the most affected side and movement compensations at the least affected side (Balbinot and Schuch, 2019). (B) The balance between energy production and conservation maintains a functional post-stroke gait. Ep, BCoM potential energy; Ek, BCoM kinetic energy.

Fig. 2.

Metabolic and mechanical energy production was greater for stroke subjects. (A) A familiarization session was conducted to determine the PWS during level walking. (B) Based on the PWS, subjects were asked to walk on a treadmill at two or three different speeds below the PWS and one or two speeds slightly above the PWS. (C) During each walking speed, bilateral three-dimensional (3D) kinematics and VO2 consumption were acquired following 3 min of walking acclimation. (D) The kinematic model included 11 body segments: arm (two), forearm (two), trunk (one), thigh (two), shank (two) and foot (2). (E) Increased cost of transport was evident following stroke. (F–H) External mechanical work (Wext) was greater for stroke survivors. Data are Mean±s.d., two-way ANOVAs (speed and lesion) followed by Tukey’s post-hoc test, *P<0.05 between groups as indicated, nStroke=7, nControl=10 for C and nStroke=6, nControl=10 for mechanical work variables; Wv, vertical external mechanical work; Wf, forward external mechanical work.

Fig. 3.

Post-stroke gait displayed a substantial reduction of energy recovery within the stride. (A) BCoM, Ep and Ek for a control participant, the stride cycle is defined as the time period of contact of the heel strike to next contact of the same limb; note the accumulation of energy recovery when exchanging Ep to Ek with both limbs (grey). (B) For post-stroke participants the stride cycle is defined as the time period from contact of paretic limb with the treadmill to the next contact of the same limb. During the initial contact of the paretic limb with the treadmill, stroke survivors used the paretic limb as a rigid shaft while pushing off using the non-paretic lower limb (green); but a substantial reduction of energy recovery occurred when exchanging Ep to Ek using the paretic limb to push off (red). Note that this transduction seems to occur more briefly and with a reduced increase in Ek. (C–F) Stroke survivors showed relative maintenance of energy recovery while walking at 40% of PWS. A substantial reduction of the energy transduction within the step (ΔRint) accumulated from 0–25%, 25–50% and 50–75% of the stride was evident for stroke survivors walking at the PWS. (G) Rint during the full stride was substantially reduced for stroke participants at the PWS; note that stroke participants maintain a relatively constant energy recovery, regardless of speed, whereas the control group shows the expected increase in energy recovery at PWS. Data are Mean±s.d.; two-way ANOVA (speed and lesion) followed by Tukey’s post-hoc test, *P<0.05 between groups as indicated, nStroke=6, nControl=10. Rint, energy transduction within the step.