Epidural Electrical Stimulation of the Lumbosacral Spinal Cord Improves Trunk Stability During Seated Reaching in Two Humans With Severe Thoracic Spinal Cord Injury

Megan Gill, Margaux Linde, Kalli Fautsch, Rena Hale, Cesar Lopez, Daniel Veith, Jonathan Calvert, Lisa Beck, Kristin Garlanger, Reggie Edgerton, Dimitry Sayenko, Igor Lavrov, Andrew Thoreson, Peter Grahn, Kristin Zhao, Megan Gill, Margaux Linde, Kalli Fautsch, Rena Hale, Cesar Lopez, Daniel Veith, Jonathan Calvert, Lisa Beck, Kristin Garlanger, Reggie Edgerton, Dimitry Sayenko, Igor Lavrov, Andrew Thoreson, Peter Grahn, Kristin Zhao

Abstract

Background: Quality of life measurements indicate that independent performance of activities of daily living, such as reaching to manipulate objects, is a high priority of individuals living with motor impairments due to spinal cord injury (SCI). In a small number of research participants with SCI, electrical stimulation applied to the dorsal epidural surface of the spinal cord, termed epidural spinal electrical stimulation (ES), has been shown to improve motor functions, such as standing and stepping. However, the impact of ES on seated reaching performance, as well as the approach to identifying stimulation parameters that improve reaching ability, have yet to be described. Objective: Herein, we characterize the effects of ES on seated reaching performance in two participants with chronic, complete loss of motor and sensory functions below thoracic-level SCI. Additionally, we report the effects of delivering stimulation to discrete cathode/anode locations on a 16-contact electrode array spanning the lumbosacral spinal segments on reach distance while participants were seated on a mat and/or in their wheelchair. Methods: Two males with mid-thoracic SCI due to trauma, each of which occurred more than 3 years prior to study participation, were enrolled in a clinical trial at Mayo Clinic, Rochester, MN, USA. Reaching performance was assessed, with and without ES, at several time points throughout the study using the modified functional reach test (mFRT). Altogether, participant 1 performed 1,164 reach tests over 26-time points. Participant 2 performed 480 reach tests over 17-time points. Results: Median reach distances during ES were higher for both participants compared to without ES. Forward reach distances were greater than lateral reach distances in all environments, mat or wheelchair, for both participants. Stimulation delivered in the caudal region of the array resulted in improved forward reach distance compared to stimulation in the rostral region. For both participants, when stimulation was turned off, no significant changes in reach distance were observed throughout the study. Conclusion: ES enhanced seated reaching-performance of individuals with chronic SCI. Additionally, electrode configurations delivering stimulation in caudal regions of the lumbosacral spinal segments may improve reaching ability compared to rostral regions.

Keywords: epidural spinal electrical stimulation; modified functional reach test; neuromodulation; neurorehabilitation; paralysis; reach distance; spinal cord injury; trunk stability.

Copyright © 2020 Gill, Linde, Fautsch, Hale, Lopez, Veith, Calvert, Beck, Garlanger, Edgerton, Sayenko, Lavrov, Thoreson, Grahn and Zhao.

Figures

Figure 1
Figure 1
Methods description. Panel (A) describes clinical trial timeline including enrollment, time of electrical stimulation (ES) implantation, 3 month break, and end of study. Training focus is described for each phase of the study as well as the environment of each modified functional reach test (mFRT). Panel (B) is a pictorial of forward and lateral reaching tasks performed on the mat or wheelchair. Panel (C) demonstrates the active electrodes used on the stimulating array for Caudal ES and Rostral ES.
Figure 2
Figure 2
Participant 1 reach distances for all conditions recorded over time. Number of mFRT trials recorded throughout the study demonstrating forward and lateral (right and left equally), through all ES conditions: NO ES and ES. Numbers display trials performed on mat and on wheelchair (A). The average of three trials per day for forward (B) and lateral reach (C) on mat and wheelchair. Solid vertical line indicates epidural stimulator implantation time point.
Figure 3
Figure 3
Participant 1 coefficient of variation (CV) of reach scores. The CV was calculated for all reach distances of NO ES (Blue) and ES (Red) for the right and left arm while seated on a mat or a wheelchair. Data represented in a scatter plot with line at the median value.
Figure 4
Figure 4
Participant 1 comparison of No ES to ES reach distances. Forward and lateral reach distances during No ES and ES conditions were compared for right and left sides while seated on the mat or the wheelchair. Dots represent the average of three trials for forward and lateral reach and solid horizontal line represents the median of all trials combined.
Figure 5
Figure 5
Participant 1 reach distance during three conditions (ES OFF, ES Rostral and ES Caudal) on mat and wheelchair. ES conditions for forward and lateral reach distances reported for right and left sides. Each data point indicates the average of three trials at each test date, blue represents ES off, red triangles represent Rostral ES usage, and red squares represent Caudal ES usage. Each reach direction, forward, lateral, right, and left were performed and reported for mat and wheelchair environments.
Figure 6
Figure 6
Participant 2 reach distances for all conditions recorded over time. Number of mFRT trials recorded throughout the study demonstrating forward and lateral (right and leftarm), through all ES conditions: NO ES and ES. Numbers display trials performed on mat (A). The average of three trials per day for forward (B) and lateral reach (C). Solid vertical line indicates ES implantation time point. Gray box represents when the participant exited the study.
Figure 7
Figure 7
Participant 2 coefficient of variation (CV) of reach scores. The CV was calculated for all reach distances of NO ES (Blue) and ES (Red) for the right and left arm while seated on a mat. Data represented in a scatter plot with line at the median value.
Figure 8
Figure 8
Participant 2 comparison of No ES to ES reach scores. mFRT scores for forward and lateral reach distances in No ES conditions were compared for right and left sides while seated on the mat. Dots represent average of three trials for forward and lateral reach and solid horizontal line represents the median of all trials combined.
Figure 9
Figure 9
Participant 2 reach distance during three conditions (ES OFF, Rostral ES and Caudal ES contacts) while seated on the mat. ES conditions for forward and lateral reach distances reported for right and left side. Each data point indicates the average of three trials at each test date, blue representing ES off, red triangles represent Rostral ES usage, and red squares represent Caudal ES usage.

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