FES-rowing: a well-tolerated and highly beneficial exercise for a patient with Brown-Sequard syndrome

Abstract

Context:

Brown-Séquard Syndrome (BSS) is a rare neurological condition associated with Spinal Cord Injury (SCI). Hemisection of the spinal cord causes paralysis of the homolateral side, and thermoalgesic dysfunction on the opposite side. Cardiopulmonary and metabolic alterations have been reported. For all these patients, regular physical activity is highly recommended and functional electrical stimulation (FES) may be a good option, especially for those with paraplegia. However, to our knowledge, the effects of FES have primarily been studied in those with complete SCI and data regarding application and effects in patients with incomplete lesions (with sensory feedback) is lacking. The present case report therefore evaluated the feasibility and effectiveness of a 3-month FES-rowing program in a patient with BSS.

Methods:

Knee extensor muscle strength and thickness, walking and rowing capacities as well as quality of life were evaluated before and after 3 months of FES-rowing (two sessions per week) in a 54 year old patient with BSS.

Results:

The individual had excellent tolerance and adherence to the training protocol. All measured parameters were greatly improved after 3 months: on average, + 30% rowing capacity, + 26% walking capacity, + 24.5% isometric strength, + 21.9% quadriceps muscle thickness, + 34.5% quality of life.

Conclusion:

FES-rowing appears to be well tolerated and highly beneficial for a patient with incomplete SCI and could therefore be considered as an appealing exercise option for these patients.

Introduction

Spinal cord injury (SCI) is a traumatic injury of the nervous system inducing neurological deficits that can lead to muscle paralysis, loss of upper/lower-limb functionality, and reduced physical function. Among people with spinal cord injuries, ∼2–4% are affected by Brown-Séquard Syndrome (BSS): a hemisection of the spinal cord with ipsilateral weakness or paralysis, and loss pain sensation on the opposite side (1). For these patients, as for all SCI patients, regular physical activity is highly recommended, and moderate to high intensities are associated with greater benefits (2). However, reaching such intensities can be difficult for these patients because of the small muscle mass that can be engaged for voluntary exercise (3). One solution is to activate/assist lower limb muscles by using functional electrical stimulation (FES). Briefly, this technique consists of applying electric current to activate the damaged or disabled neuromuscular system in a coordinated manner in order to generate muscular contractions and produce a functionally useful movement (4). Although FES-cycling is the most developed method and has demonstrated numerous beneficial effects, FES-rowing might be even more efficient since it requires coordinated voluntary work of the upper limbs with electrically induced contractions of the lower limbs to produce the rowing movement (5,6). Several recent studies have demonstrated large benefits in cardiorespiratory and muscular function in patients with SCI (3).

However, in able-bodied subjects, electrical stimulation is often associated with discomfort limiting the stimulation intensity and therefore the effectiveness of training (7). Although it is less of a problem in patients with complete SCI and no sensory feedback, it could be an issue for patients with BSS. Defining the feasibility, tolerance and effectiveness of a FES-rowing program would therefore be of great interest and might open new avenues for physical exercise and rehabilitation for these patients. This was the aim of the present case report. The effects of 3 months of FES-rowing were evaluated with respect to rowing exercise capacity, muscle strength and thickness, 6-min walk test performance, and quality of life in a patient with Brown-Séquard Syndrome (incomplete SCI).

Material and methods

Subject. A 54-years-old man (182 cm, 66 kg, 4 h of swimming per week) with Brown-Sequard Syndrome developed 27 years prior following both cervical spinal extradural empyema and incomplete spinal cord injury (C4/C5, ASIA D) participated in the study. He presented paralysis of the left lower limb, thermoalgesic dysfunction on the right side and difficulties regarding left-hand’s fingers extension. Due to the left lower limb’s paralysis, the participant’s ambulation was slow but did not require any assistance nor induce any alteration in daily living activities or independence. The participant was medically stable with no contraindications to FES-rowing exercise (i.e. excessive spasticity, rotator cuff tears, cardiac pacemaker or implantable electric devices). Inclusion criteria were: adult with BSS, available and motivated to participate to a 3-month FES-rowing training protocol (two sessions per week). Exclusion criteria: uncontrolled high blood pressure, limited passive range of motion, cardiopulmonary disease, cardioactive medications, diabetes, neurological disorders (other than BSS), lower extremity contractures, or rotator cuff tears that would limit the ability to row.

Before injury, the participant was physically active (swimming and running for ∼ 5–6 h per week) but he had never rowed. The study was conducted according to the declaration of Helsinki, and approval for the project was obtained from the local Institutional Review Board. The participant read/signed a written informed consent document describing the procedure and potential risks of the study.

Experimental design. After 3 familiarization sessions to learn the FES-rowing technique, the participant underwent 3 months of training (2 sessions per week) preceded and followed by testing described below.

Training protocol. Each training session was composed of 38 min of FES-rowing as described on Fig. 1: (i) 5 min of warm-up, (ii) alternation of rowing at 50% of peak rowing power (during 4 min, five times) and rowing power and at 70% (for 2 min, 4 times), (iii) 5 min of recovery. FES (50 Hz with a pulse width of 400 μs) was applied simultaneously on both quadriceps at maximal tolerated intensity to assist the drive phase of the rowing stroke. The training took place on a hybrid rowing machine assisted by functional electrical stimulation (Werize Rower – Kurage, Lyon, France), equipped with a high-back seat combined with adjustable seat belts to stabilize the trunk and prevent loss of balance. Electrical stimulation was achieved with a Motimove unit (3F-Fit Fabricando Faber, Serbia) attached to 5 × 9 cm self-adhesive electrodes (Compex SA, Ecublens, Switzerland) placed over the motor points of the rectus femoris and the vastus lateralis muscles of both legs.

Figure 1.

Schematic view of a training session.

Testing procedures

To assess the effects of the training protocol, tests were conducted before (M0) and after 3 months (M3). Tests were performed at approximately the same time of the day for each session. At each testing time point (M0, M3), the subject came for two testing sessions: Session 1: peak rowing power; Session 2: knee extensor muscles’ architecture and strength, 6-min Walking test and Quality of Life questionnaire. Testing sessions were separated by 72 h to avoid fatigue effects.

Peak rowing power: Peak exercise power was assessed using an incremental rowing test performed with lower limb stimulation. The test started at a load of 20 W and increased by 10 W every minute until the subject could not maintain the required intensity. Heart rate was monitored continuously during testing (heart rate monitor, Garmin, Taiwan). This test was performed at the end of each month to readjust training intensities.

Knee extensor muscles’ strength: Isometric knee extensor muscles’ strength was measured using maximal voluntary contractions (MVC) performed on an isokinetic ergometer (Biodex Medical Systems Inc., Shirley, NY, USA). The participant’s trunk was firmly held with straps and the leg was fixed to the dynamometer lever-arm with a knee joint angle of 90°. Measurements were made for both legs. For each leg, two measurements were performed, and the average value is presented here.

Muscle architecture: Muscle architecture was evaluated using real-time B-mode ultrasonography (Z.one ultra sp 4.2, Zonare Medical Systems, USA) with a 50 mm, 12-MHz linear-array probe. Measurements were performed on the right and left quadriceps muscles after subject was in the supine position for 20 min (8). Scans were taken in the midsagittal plane, at 39% of the Rectus Femoris (RF) and Vastus Lateralis (VL) muscle length measured from the superior border of the patella to the anterior superior iliac spine (9). Position was recorded to ensure that the same region of muscle was scanned for all sessions (10). For each testing session, three scans were recorded per muscle and averaged to account for error (10). Care was taken to apply minimal pressure during the muscle scan to avoid compression (10). The investigator was the same for each test.

6-min walking test (6-MWT): Walking capacity was evaluated via the 6-min walk test using the protocol described by Kervio et al. (11). The participant was asked to cover as much distance as possible in 6 min. Slow down and stops were allowed, and the total distance walked was measured at the end of 6 min.

Quality of life: Quality of Life and general health (physical and mental scores) were evaluated using the Short-form 36 health survey questionnaire (SF-36 questionnaire) (12).

Results are presented as percent change between M0 and M3 (((Value at M3 – Value at M0)/Value at M0) × 100).

Results

The FES-rowing training protocol was extremely well accepted and tolerated by our participant as demonstrated by its adherence to the training, oral feedbacks and by the absence of any adverse event/major discomfort associated with the stimulation. In addition, testing results revealed significant effectiveness of the training protocol. Indeed, peak exercise power measured each month increased progressively from 100 W at the beginning of the study to 130 W after 3 months (+ 30%). In addition, the average power developed during each training session increased by 51.2% over the 3 month-period (from 43 to 65 W, Fig. 2). Muscle strength increased by 22% (from 99.3 to 121.2 N·m) in the right leg and by 27% (from 89.9 to 114.0 N·m) in the left (injured) leg (Fig. 3(a)). Muscle thickness was also greatly improved: + 18.6% (from 12.9 to 15.3 mm) and +27.8% (from 13.3 to 17.0 mm) for the right and left RF respectively, + 9.6% (from 18.8 to 20.6 mm) and +31.9% (from 9.4 to 12.4 mm) for the right and left VL respectively (Fig. 3(b)). The total distance covered in 6 min also increased from 301 to 379 m between M0 and M3. Lastly, the physical score obtained from the SF-36 Questionary was increased by 34.5% (from 42.3 to 56.9) whereas the mental score was unchanged (−0.3%, from 73.9 to 73.7) between M0 and M3.

Figure 2.

Average power developed during training sessions over the 3 months period.

Figure 3.

Knee extensor muscles isometric torque (panel A) and thickness (panel B) measured on the left leg (black symbols) and right leg (white symbols) at the beginning (M0) and at the end (M3) of the study. KE, Knee extensors; RF, Rectus Femoris muscle; VL, Vastus Lateralis Muscle.

Discussion

This preliminary case report aimed to evaluate the feasibility and effectiveness of a 3-month FES-rowing program in a patient with Brown-Sequard Syndrome (BSS), characterized by left hemiplegia and incomplete sensation. We found here that exercise with FES-rowing was feasible, well tolerated and induced beneficial effects in a patient with BSS.

More specifically, our results showed a significant improvement in quadriceps muscle strength, increasing by 27% for the injured leg after only 3 months of FES-rowing. Previously, a study showed a 151% increase of the evoked torque after one year of training with FES and 20% of this increase was obtained after the first 3 months of rowing (5). These improvements could be attributed to central and/or peripheral adaptations to training. Our methodology did not allow us to investigate central adaptations, but we observed large peripheral adaptations as demonstrated by increases in knee extensor muscle thickness. These results are similar to those obtained previously in SCI patients after FES-rowing (5) and FES-cycling (13–15), and suggest that FES-rowing can promote significant muscle hypertrophy. One concern with FES is that the discomfort associated with stimulation could prevent the participant from using intensities sufficient to obtain benefits. Our results reveal that it was not the case.

We also assessed the impact of the FES-rowing program on walking capacity. The 6-min walk test evaluates physical performances related to activities of daily living (11). The participant demonstrated a 26% increase in the distance walked which may result in better autonomy and also increased quality of life (16). Indeed, we found a large increase in the “Physical score” of the SF-36 questionnaire. Similar improvements in walking ability have been reported after four weeks of FES-cycling in incomplete SCI (17). Such results are not surprising according to Mian et al. (18) who demonstrated a significant correlation between maximal isometric strength and 6-MWT distance.

Conclusion

This case report demonstrates that the FES-rowing training program can be extremely well tolerated and can induce several beneficial effects. These benefits include improvements in quadriceps muscle strength and thickness, walking capacity, and quality of life. These results are of particular interest since they suggest that the FES-rowing induced benefits previously demonstrated in people with SCI could also be obtained in patients with incomplete lesions. This might therefore open new exercise avenues for this population. However, our study is a case report with no control group; the results should be interpreted with caution, but indicate a larger scale study should be pursued.

Disclaimer statements

Contributors None.

Conflicts of interest Authors have no conflict of interests to declare.

Funding Statement

None.