Effects of percutaneously-implanted epidural stimulation on cardiovascular autonomic function and spasticity after complete spinal cord injury: A case report

Abstract

Importance: There is a revived interest to explore spinal cord epidural stimulation (SCES) to improve physical function after spinal cord injury (SCI). This case report highlights the potential of eliciting multiple functional improvements with a single SCES configuration, a strategy which could improve clinical translation.

Objective: To determine whether SCES intended to facilitate walking also acutely yields benefits in cardiovascular autonomic regulation and spasticity.

Design: Case report from data collected at two timepoints 15 weeks apart from March to June 2022 as part of a larger clinical trial.

Setting: Research lab at Hunter Holmes McGuire VA Medical Center.

Participant: 27-year-old male, 7 years post a C8 motor complete spinal cord injury.

Intervention: A SCES configuration intended to enhance exoskeleton-assisted walking training applied for autonomic and spasticity management.

Main outcomes and measures: The primary outcome was cardiovascular autonomic response to a 45-degree head-up-tilt test. Systolic blood pressure (SBP), heart rate (HR), and absolute power of the low-frequency (LF) and high-frequency (HF) components of a heart-rate variability analysis were collected in supine and tilt with and without the presence of SCES. Right knee flexor and knee extensor spasticity was assessed via isokinetic dynamometry with and without SCES.

Results: At both assessments with SCES off, transitioning from supine to tilt decreased SBP (assessment one: 101.8 to 70 mmHg; assessment two: 98.9 to 66.4 mmHg). At assessment one, SCES on in supine (3 mA) increased SBP (average 117 mmHg); in tilt, 5 mA stabilized SBP near baseline values (average 111.5 mmHg). At assessment two, SCES on in supine (3 mA) increased SBP (average 140 mmHg in minute one); decreasing amplitude to 2 mA decreased SBP (average 119 mmHg in minute five). In tilt, 3 mA stabilized SBP near baseline values (average 93.2 mmHg). Torque-time integrals at the right knee were reduced at all angular velocities for knee flexors (range: -1.9 to -7.8%) and knee extensors (range: -1 to -11.4%).

Conclusions and relevance: These results demonstrate that SCES intended to facilitate walking may also enhance cardiovascular autonomic control and attenuate spasticity. Using one configuration to enhance multiple functions after SCI may accelerate clinical translation.

Clinical trial registration: https://clinicaltrials.gov/ct2/show/, identifier NCT04782947.

Keywords: autonomic nervous system; exoskeleton; percutaneous epidural stimulation; rehabilitation; spasticity; spinal cord injury.

FIGURE 1

(A) Longitudinal and (B) axial T2 MRIs highlighting the level of injury in a person with C8 complete motor and sensory SCI that were captured prior to implantation. (C) Leads placements with inter-pulse generator as captured by dual energy x-ray absorptiometry of the spine region. The black rectangle denotes the placement of the cathode at 0 and the right rectangle denotes the placement of the anode at 3. These configurations (–0 and +3) yielded rhythmic locomotor-like activity. The leads were staggered where the left lead covered the mid-line of T11 vertebral body to proximal border of L1 and the right lead extended from the T11/T12 inter-vertebral space to the mid-line of L1 vertebral body.

FIGURE 2

Supine rhythmic electromyography (EMG) activities of the left and right rectus femoris (RF) and medical gastrocnemius muscles initiated when the stimulation parameters were set at a frequency of 25 Hz, pulse duration of 250 μs and amplitude of the current that progressed from 5.0–7.0 mA after configuring the cathode at –0 and the anode at +3. The rhythmicity pattern resulted in periods of EMG bursts that followed by periods of relaxation in three out of the four muscle groups and was less obvious in the right rectus femoris muscle. The EMGs presented are rectified and bandpass filtered at 10–990 Hz. RF, rectus femoris; MG, medial gastrocnemius; mV, millivolts; mA, milliamps; sec, seconds.

FIGURE 3

Fourteen weeks of exoskeleton walking training. Each week consisted of an average of three sessions per week. Circles represent time (minutes) for average total walk time and uptime. Triangles represent average total number of steps achieved throughout each week of training. During this period, exoskeleton was set at a variable assist mode to enable stepping with SCES on during 60 min of EAW.

FIGURE 4

Raw EMG activities of the left and right vastus lateralis muscles for 5 min with SCES off in supine position (pink), followed by 5 min in supine and 10 min tilt with SCES on (both green). The participant was then tilted back to supine position and the SCES remained on for another 5 min (green) followed by another 5 min with the SCES off (pink). The EMG activities were captured only during the second assessment period. min, minutes; mV, millivolts; mA, milliamps; SCES, spinal cord epidural stimulation.

FIGURE 5

Cardiovascular autonomic response to EAW enhancement SCES during a 45-degree head-up-tilt. Assessment 1 was captured 15 weeks before assessment 2. Both assessments followed the same protocol. The participant was initially in supine lying for 5 min followed by an attempt to perform a head-up tilt using a motorized tilting table for 10 min. The tilting maneuver was discontinued if systolic blood pressure (SBP) dropped by 40 mm Hg from resting baseline. This is followed by repeating the same protocol with SCES on after a 30-min washout period. The SCES was turned on 3–5 min in supine lying before performing the head-up tilt maneuver. A similar timeline was repeated in assessment 2. Triangles and circles represent 1-min averages of SBP and heart rate (HR), respectively. Low-frequency (LF) and high-frequency (HF) components of a heart rate variability analysis are presented for the entire corresponding supine or head-up tilt period.

FIGURE 6

Torque-time integral (Nm.s/s) measured for knee extensor (A) and flexor (B) muscle groups using isokinetic dynamometer. The examined leg was moved across different angular velocities (5–270 deg.sec^{– 1}) and the resistance to passive movement was reported as area under the curve after accounting for the duration (s) of each curve. The task was administered initially with SCES off (open diamond) before a washout period of 30 min in which SCES was turned on (closed diamond).