Case Report: Endurance Electrical Stimulation Training Improves Skeletal Muscle Oxidative Capacity in Chronic Spinal Cord Injury

Abstract

Objective:

To describe the use of a novel neuromuscular electrical stimulation (NMES) endurance exercise protocol and its effects on skeletal muscle oxidative capacity.

Design:

Case report, pre/post intervention.

Setting:

University-based trial.

Participant:

A 39-year-old man who suffered a motor complete spinal cord injury (C5–6, ASIA Impairment Scale grade A).

Intervention:

Twenty-four weeks of endurance NMES that consisted of progressive increases in the twitch frequency, duration of sessions, and sessions per week.

Main Outcome Measure:

Mitochondrial capacity was measured, in vivo, as the rate of recovery of muscle oxygen consumption using near-infrared spectroscopy.

Results:

The rate of recovery of muscle oxygen consumption increased approximately 3-fold from 0.52 to 1.43, 1.46, and 1.40/min measured on 3 separate occasions during week 12 of training, and 1.57/min after 24 weeks of NMES endurance training.

Conclusion:

The findings of this study suggest that NMES endurance training using twitches can increase mitochondrial capacity to comparable levels measured in nonparalyzed muscles of sedentary able-bodied controls.

Spinal cord injury (SCI) results in changes to the musculature below the level of injury, including atrophy, increased intramuscular fat, and reduced skeletal muscle mitochondrial function.^1,2 These changes have been associated with an increased risk of cardiovascular disease, metabolic diseases, osteoporosis, and obesity. It is known that neuromuscular electrical stimulation (NMES) training can prevent muscle atrophy and cause muscle hypertrophy³ and can improve lipid profiles and bone density in persons with SCI. NMES therapies for persons with SCI typically include resistance exercise or functional electrical stimulation (FES) exercises, such as cycling and rowing. However, most electrical stimulation training programs involve a resistance training stimulation protocol designed to induce muscle hypertrophy. The effects of endurance electrical stimulation training of paralyzed human skeletal muscle are unclear. Further, improving skeletal muscle mitochondrial function through NMES training could lead to health benefits in persons with SCI.

Methods

This case study describes the use of a novel method of NMES training and measuring skeletal muscle mitochondrial capacity using near-infrared spectroscopy (NIRS). A 39-year-old man suffered a complete SCI (C5–6, ASIA Impairment Scale grade A) as a result of traumatic injury secondary to a motor vehicle collision 20 years prior to this study. The participant (height, 195cm; weight, 108kg) had no history of orthopedic injuries that would make NMES training unsafe. The Institutional Review Board at the University of Georgia approved this study, and the participant gave written informed consent prior to beginning this study.

Endurance NMES training

Twenty-four weeks of endurance NMES was performed using twitch electrical stimulation (pulse duration/interval =200/50μs). This stimulation protocol was designed to provide an endurance training stimulus in contrast to previously used resistance training NMES.^3,4 The NMES current amplitude was set to 175mA, and the current was kept the same for every training session. NMES training began with 10 minutes of twitch stimulation at 2Hz for the first 2 weeks. Initially, the training was performed twice per week, with at least 2 days of rest between sessions. After the first 2 weeks, the duration of each training session was progressively increased up to 75 minutes. The frequency of training sessions was also progressively increased from 2 to 5 sessions per week. Finally, the stimulation frequency (ie, number of twitch contractions per second, or hertz) was also increased progressively from 2 up to 7Hz.

A Theratouch 4.7 NMES unit^a was attached to the quadriceps muscles using 2 commercial electrodes (Superstim^a 7.62×12.7cm). One electrode was placed distally over the skin of the vastus medialis, approximately 1 to 2cm above the patella; another electrode was placed proximally and about 24cm above the patella over the vastus lateralis. The participant was trained in his wheelchair with both legs extended (0° flexion).

NIRS measurements of mitochondrial capacity

Skeletal muscle mitochondrial capacity was assessed using the rate of recovery of muscle oxygen consumption (mVo₂) after electrical stimulation using NIRS.^5,6 mVo₂ was measured as the change in the NIRS signal during arterial occlusions using linear regression. Repeated arterial occlusions were performed after 15 seconds of electrical stimulation at 4Hz and were fit to a mono-exponential curve. A rate constant (k) was calculated, which is proportional to the mitochondria’s oxidative capacity. NIRS signals were corrected for changes in blood volume, as previously described.⁶ Corrected oxygenated hemoglobin/myoglobin (O₂Hb) and deoxygenated hemoglobin/myoglobin (HHb) were subtracted to produce the NIRS difference signal (Hb = O Hb–HHb), which doubles the change in the NIRS signal during arterial occlusion. NIRS signals were normalized using an ischemic calibration to control for adipose tissue thickness.^6,7 NIRS data were collected at 10Hz using an Oxymon Mk III.^b NIRS testing occurred prior to beginning NMES training, on 3 separate days immediately after week 12 of training, and again after week 24 of training.

Results

The number of contractions performed increased from 1200 per training session and 2400 per week to 31,500 contractions per session and 157,500 per week (145 total sessions). Because of time constraints with the training protocol, no increases in training intensity occurred after week 12 of training (fig 1). Prior to NMES training, the rate of recovery of mVo₂ was .52/min (time constant, 115s). After 12 weeks of training, the rate of recovery of mVo₂ was 1.43, 1.46, and 1.40/min (time constant, 41, 41, and 42s, respectively), measured on 3 separate occasions (1d apart). The coefficient of variation of the 3 week 12 measurements was 2.5%. The rate of recovery of mVo₂ measured after week 24 of training was 1.5/min (time constant, 38s). Pre-, week 12, and week 24 NIRS recovery rates are shown in figure 2.

Fig 1.

NMES training progression. The number of twitch contractions (sum of both legs) is plotted for each training session. Because of time constraints, no increases in training intensity occurred after week 12 of training.

Fig 2.

Rate of recovery of mVo₂ after electrical stimulation. Measurements were made prior to beginning NMES training, on 3 separate days within 1 week after 12 weeks of training, and after 24 weeks of training. Solid lines indicate SCI and able-bodied results from a previous study.⁸ Abbreviation: AB, able-bodied.

Discussion

This case study documented a 3-fold increase in muscle oxidative capacity, measured by the increase in the rate of recovery of mVo₂, in response to a 6-month NMES endurance exercise program. Prior to beginning the NMES exercise program, the participant had approximately one third the mitochondrial capacity of that previously reported in able-bodied participants using NIRS.⁶ The baseline NIRS rate constant for this participant (.52/min) was similar to SCI participants using magnetic resonance spectroscopy (~.64/min)² and NIRS (.70/min).⁸ We found good reproducibility between the 3 trials performed after 12 weeks of the training program (coefficient of variation, 2.5%). The leveling-off of mitochondrial capacity after 12 weeks of training suggests that training adaptations equilibrated to the endurance training stimulus. Further increases in mitochondrial capacity may require greater increases in training intensity, which was not practical in this study. Improving mitochondrial function in people with SCI may have significant health outcomes, especially considering the high prevalence of cardiovascular and metabolic diseases.^9–11

The 3-fold improvement in mitochondrial capacity with twitch endurance training in this case study is substantially larger than reported using traditional FES exercise programs.^12,13 Chilibeck et al¹⁴ reported a 56% increase in citrate synthase activity after 8 weeks (3d/wk) of FES cycling exercise. Similarly, Martin et al¹ reported an approximately 1-fold increase in succinate dehydrogenase activity in both type I and type II fibers after 6 months of NMES training of the tibialis anterior muscle. Kjaer et al¹⁵ found that citrate synthase activity from muscle biopsies of the vastus lateralis doubled after 3 months of FES cycling, but no further improvements were found after 3 months.

Study limitations

The limitations of this study are that only 1 participant was tested and that no statistical analyses were performed because of the sample size. Therefore, the results of this case report should be considered exploratory.

Conclusions

An NMES endurance training protocol that consisted of progressive increases in the twitch frequency and duration of exercise resulted in a substantial improvement in skeletal muscle mitochondrial capacity in a person with chronic SCI. This training protocol is cost-efficient in that it only requires a commercially available NMES unit and is practical for clinical use. The findings suggest that NMES endurance training using twitches may increase mitochondrial capacity to levels measured in non-paralyzed muscles of able-bodied controls. Future studies are warranted to investigate the impact of improving mitochondrial capacity on the health and wellness of people with SCI, including cardiovascular and metabolic diseases. Moreover, studies should be performed to optimize electrical stimulation training programs to improve health in people with SCI.

Suppliers

1. Rich-Mar Corp, 4120 S Creek Rd, Chattanooga, TN 37406.

2. Artinis Medical Systems, Sint Walburg 4 6671 AS Zetten, The Netherlands.

List of abbreviations:

FES

functional electrical stimulation

mVo₂

muscle oxygen consumption

NIRS

near-infrared spectroscopy

NMES

neuromuscular electrical stimulation

SCI

spinal cord injury