Gait Rehabilitation Using Functional Electrical Stimulation Induces Changes in Ankle Muscle Coordination in Stroke Survivors: A Preliminary Study

ORIGINAL RESEARCH published: 20 December 2018 doi: 10.3389/fneur.2018.01127 Gait Rehabilitation Using Functional Electrical Stimulation Induces Changes in Ankle Muscle Coordination in Stroke Survivors: A Preliminary Study Jessica L. Allen 1*, Lena H. Ting 2,3 and Trisha M. Kesar 2 1 Department of Chemical and Biomedical Engineering, West Virginia University, Morgantown, WV, United States, 2 Division of Physical Therapy, Department of Rehabilitation Medicine, Emory University School of Medicine, Atlanta, GA, United States, 3 Wallace H. Coulter Department of Biomedical Engineering, Emory University and Georgia Institute of Technology, Atlanta, GA, United States Edited by: Ping Zhou, University of Texas Health Science Center at Houston, United States Reviewed by: Svetlana Pundik, Case Western Reserve University, United States Andrew Earl Ekelem, Vanderbilt University, United States *Correspondence: Jessica L. Allen Specialty section: This article was submitted to Stroke, a section of the journal Frontiers in Neurology Received: 07 September 2018 Accepted: 07 December 2018 Published: 20 December 2018 Citation: Allen JL, Ting LH and Kesar TM (2018) Gait Rehabilitation Using Functional Electrical Stimulation Induces Changes in Ankle Muscle Coordination in Stroke Survivors: A Preliminary Study. Front. Neurol. 9:1127. doi: 10.3389/fneur.2018.01127 Frontiers in Neurology | www.frontiersin.org Background: Previous studies have demonstrated that post-stroke gait rehabilitation combining functional electrical stimulation (FES) applied to the ankle muscles during fast treadmill walking (FastFES) improves gait biomechanics and clinical walking function. However, there is considerable inter-individual variability in response to FastFES. Although FastFES aims to sculpt ankle muscle coordination, whether changes in ankle muscle activity underlie observed gait improvements is unknown. The aim of this study was to investigate three cases illustrating how FastFES modulates ankle muscle recruitment during walking. Methods: We conducted a preliminary case series study on three individuals (53–70 y; 2 M; 35–60 months post-stroke; 19–22 lower extremity Fugl-Meyer) who participated in 18 sessions of FastFES (3 sessions/week; ClinicalTrials.gov: NCT01668602). Clinical walking function (speed, 6-min walk test, and Timed-Up-and-Go test), gait biomechanics (paretic propulsion and ankle angle at initial-contact), and plantarflexor (soleus)/dorsiflexor (tibialis anterior) muscle recruitment were assessed pre- and post-FastFES while walking without stimulation. Results: Two participants (R1, R2) were categorized as responders based on improvements in clinical walking function. Consistent with heterogeneity of clinical and biomechanical changes commonly observed following gait rehabilitation, how muscle activity was altered with FastFES differed between responders. R1 exhibited improved plantarflexor recruitment during stance accompanied by increased paretic propulsion. R2 exhibited improved dorsiflexor recruitment during swing accompanied by improved paretic ankle angle at initial-contact. In contrast, the third participant (NR1), classified as a non-responder, demonstrated increased ankle muscle activity during inappropriate phases of the gait cycle. Across all participants, there was a positive relationship between increased walking speeds after FastFES and reduced SOL/TA muscle coactivation. 1 December 2018 | Volume 9 | Article 1127 Allen et al. FastFES Changes Ankle Muscle Activity Conclusion: Our preliminary case series study is the first to demonstrate that improvements in ankle plantarflexor and dorsiflexor muscle recruitment (muscles targeted by FastFES) accompanied improvements in gait biomechanics and walking function following FastFES in individuals post-stroke. Our results also suggest that inducing more appropriate (i.e., reduced) ankle plantar/dorsi-flexor muscle coactivation may be an important neuromuscular mechanism underlying improvements in gait function after FastFES training, suggesting that pre-treatment ankle muscle status could be used for inclusion into FastFES. The findings of this case-series study, albeit preliminary, provide the rationale and foundations for larger-sample studies using similar methodology. Keywords: walking, functional electrical stimulation (FES), electromyography (EMG), neuromechanics, biomechanics, gait rehabilitation INTRODUCTION whether abnormal muscle activation patterns underlying gait deficits are restored following rehabilitation. FastFES, the combination of fast treadmill training and functional electrical stimulation (FES) of ankle muscles, is a novel post-stroke gait intervention that has been shown to improve walking speed, endurance, and energy efficiency poststroke (14–16). FastFES targets paretic propulsion by using electrical stimulation to augment force generation of ankle plantarflexor muscles during terminal stance of walking (17). In addition, FastFES includes stimulation of paretic ankle dorsiflexor muscles during swing to correct foot-drop. Following 12-weeks of the FastFES intervention, increases in paretic propulsion were observed when walking without stimulation, and maintained 3 months post-training (14). This improved ability to generate propulsion from the paretic limb following FastFES was accompanied by increased walking speeds and function (14, 15, 18). Nevertheless, as is common with a majority of gait interventions, there was considerable interindividual variability in the magnitude of FastFES-induced gait improvements, such that not all participants who underwent the intervention improved walking function (18). We posit that identifying neuromechanical mechanisms underlying improved walking function after FastFES can help identify candidates who are most likely to benefit, reducing variability in response to FastFES. Because the FastFES gait intervention specifically aims to improve paretic ankle muscle recruitment, presumably changes in paretic ankle muscle recruitment drive the training-induced gait improvements. However, FastFES-induced changes in ankle muscle activation have not been assessed previously. It is currently unknown whether ankle muscle activity is actually changed after FastFES. Indirectly, predictions from gait simulations based solely on measured biomechanics suggest that improved plantarflexor recruitment underlies the increases in propulsion and walking speed observed after FastFES (19). But, direct evidence for improved plantarflexor muscle activity after FastFES through EMG recordings has not yet been demonstrated. Further, whether dorsiflexor recruitment is also altered by FastFES is also unknown. Long-term use of dorsiflexor stimulation alone to prevent foot-drop post-stroke has previously been shown to improve voluntary recruitment of the dorsiflexor Characterizing changes in muscle coordination after poststroke gait rehabilitation may help identify neuromuscular mechanisms drivi (...truncated)