Transcutaneous Electrical Spinal Stimulation Promotes Long-Term Recovery of Upper Extremity Function in Chronic Tetraplegia

Abstract

Upper extremity function is the highest priority of tetraplegics for improving quality of life. We aim to determine the therapeutic potential of transcutaneous electrical spinal cord stimulation for restoration of upper extremity function. We tested the hypothesis that cervical stimulation can facilitate neuroplasticity that results in long-lasting improvement in motor control. A 62-year-old male with C3, incomplete, chronic spinal cord injury (SCI) participated in the study. The intervention comprised three alternating periods: 1) transcutaneous spinal stimulation combined with physical therapy (PT); 2) identical PT only; and 3) a brief combination of stimulation and PT once again. Following four weeks of combined stimulation and physical therapy training, all of the following outcome measurements improved: the Graded Redefined Assessment of Strength, Sensation, and Prehension test score increased 52 points and upper extremity motor score improved 10 points. Pinch strength increased 2- to 7-fold in left and right hands, respectively. Sensation recovered on trunk dermatomes, and overall neurologic level of injury improved from C3 to C4. Most notably, functional gains persisted for over 3 month follow-up without further treatment. These data suggest that noninvasive electrical stimulation of spinal networks can promote neuroplasticity and long-term recovery following SCI.

Figures

Fig. 1.

Radiographic images of the injury location and decompression surgery of the cervical spine. (A) T2 weighted sagittal (top) and axial (bottom) magnetic resonance images of the subject’s cervical spine at 6 months post-injury. Arrows shows high intensity T2 signal of myelomalacia and atrophy at C3 and C4 spinal level. (B) Anteroposterior (top) and lateral (bottom) x-ray images of cervical vertebra showing laminectomy and arthrodesis surgery.

Fig. 2.

Schematic of the intervention showing electrical cervical spinal stimulation applied to the surface of the skin via electrodes placed midline at C3–4 and C6–7 bony landmarks. (Inset) Biphasic, rectangular, 1 ms pulses are delivered at a frequency of 30 Hz. Each pulse is filled with a carrier frequency of 10 kHz to permit stimulation intensities of 80–120mA to pass through the skin and reach the spinal cord without discomfort.

Fig. 3.

Bilateral manual muscle testing scores derived from Graded Redefined Assessment of Strength, Sensibility and Prehension (GRASSP) test throughout the study. Motor score is comprised of 10 muscles tested bilaterally (deltoid, triceps, biceps, wrist extensors, finger flexors, finger abductors, extensor digitorum, opponens pollicis, flexor pollicis longus, and first dorsal interossei). Strength was stable during baseline testing, increased 37 points during stimulation combined with physical therapy through week 9 (Stim + PT), and was maintained throughout three months of follow-up with no further treatment.

Fig. 4.

Total GRASSP test scores improve markedly during treatment with stimulation and physical therapy (Stim + PT). The total score combines all domains of the test including strength, sensation, qualitative and quantitative prehension. Improvements were sustained throughout three months of follow-up with no further treatment. Please see Fig. 5 for results from individual test domains.

Fig. 5.

Subscores of the Graded Redefined Assessment of Strength, Sensation and Prehension (GRASSP) test reported at the conclusion of each phase of the study. Improvement (Δ) during stimulation combined with physical therapy (stim + PT) exceeded the minimal detectable difference (MDD) for all subscores of the GRASSP test except fingertip sensation (strength: Δ37 vs. MDD 7; sensation: Δ−2 vs. MDD 4; qualitative prehension: Δ6 vs. MDD 5; and quantitative prehension: Δ11 vs. MDD 6.

Fig. 6.

Lateral pinch strength improved in both the right and left hands during stimulation combined with physical therapy. During four weeks of stimulation combined with physical therapy, pinch strength improved 2-to 7-fold in the presence of stimulation for the left and right hand, respectively. Physical therapy alone (PT only) resulted in no further improvement, but all gains were maintained during three months of follow-up. Each data point is the average of three maximal contractions performed on a given day, and error bars are standard deviation.

Fig. 7.

Following four weeks of stimulation combined with physical therapy, normal light touch and pin prick sensations expanded from the C4 to the T10 dermatome. After an additional four weeks of physical therapy only, altered sensation returned below T4, but remained constant at this level throughout the three-month follow-up period.

Fig. 8.

Integrated EMG of stimulus-evoked response recorded from right opponens pollicis muscle (right panel). Spinal evoked potentials were elicited by monophasic, rectangular, 1 ms single pulses filled with a 10 kHz waveform, delivered at 1 Hz. Stimulation intensity was 90 mA applied over the C3–4 spinous processes. The polysynaptic, late EMG responses (left panels) increased gradually over four weeks of stimulation combined with physical therapy, reduced after physical therapy only, but returned with five days of additional stimulation and therapy treatment.