This study investigated the effectiveness of adding neuromuscular electrical stimulation (NMES) to endurance training (ET) and resistance training (RT) on exercise tolerance and balance in COPD patients. 42 patients were assigned randomly to the ET + RT + NMES group (
Chronic obstructive pulmonary disease (COPD) patients have demonstrated prominent balance impairment [
Exercise training, as a pillar of pulmonary rehabilitation, plays an essential role in improving muscle strength, exercise tolerance, and quality of life [
Despite the well-known positive effects of exercise training in patients with COPD, the best modality of exercise is still under discussion, and it depends on the physiologic requirement. In fact, various training modalities were used seeking additional benefits. Endurance training (ET) aimed to improve cardiorespiratory fitness, increase physical activity, and decrease dyspnea and fatigue [
Neuromuscular electrical stimulation (NMES), an emerging alternative, seems to be suitable for patients who are unable to exercise [
Recently, some studies focused on improving the balance and reducing the risk of falls [
Based on these research studies, we hypothesize that the combination of NMES, RT, and ET would improve balance, as well as the exercise tolerance in patients with COPD. We hypothesize that combined training (ET + RT + NMES) induces additional physiological adaptations than ET alone or RT alone or NMES alone.
The aim of our study was to compare the effect of adding NMES to RT and ET on exercise tolerance and balance in patients with COPD.
Forty-two male patients accepted to participate in the study. They were recruited from the department of physiology and lung function testing of Farhat Hached Hospital in Sousse in the period between 15/01/2016 and 15/09/2016. The criteria of inclusion were COPD diagnosed by pulmonary function testing, clinically stable, without other obstructive diseases, absence of heart diseases, absence of neuromuscular diseases, and fall in the past five years or recent near-fall. Individuals were excluded if they presented severe psychiatric, neurologic, or musculoskeletal conditions and/or instable cardiovascular diseases.
The patients were assigned randomly to the ET + RT + NMES group (
Flow diagram of subjects’ recruitment.
The patients were evaluated at the baseline and after 24 weeks of training (3 times a week for 90 minutes per session). On the first day, after obtaining written informed consent, measurements of pulmonary function at rest, weight, and height were done. On the following day, the subjects performed the six-minute walking test (6MWT). Spirometry, balance assessment, and maximal voluntary contraction (MVC) of the muscle quadriceps were also recorded.
All patients underwent pulmonary function testing with the measure of forced expiratory volume in 1 s (FEV1) and forced vital capacity (FVC). Testing was performed using Spirometry Zan 100 (Inspire Health GmbH, Germany) according to the European Respiratory Society recommendations [
The 6MWT evaluates the functional exercise capacity. The patient was invited to walk as far as possible along a flat corridor [
Patients began with a warm-up phase of the leg extensor muscle consisting of cycling for 5 min. Next, they performed three maximal voluntary contractions (MVC) separated by 5 min of rest to estimate the maximum voluntary force level (Globus Ergo system, TESYS 1000, Italy). Patients were required to sit with 90°hip flexion and 90°knee flexion. Stabilization straps were positioned across the chest, and the arms were crossed upon the chest.
The 1-RM test (kg) is used for assessing muscle strength. It is defined as the maximal weight that can be lifted once with the correct lifting technique (quadriceps, gluteus, hamstrings, and calf muscles).
Either group benefited three times a week for 24 weeks (72 sessions). The training session lasted 90 minutes. Each subject had to wear a pulse oximeter to control the saturation (SO2) and the heart rate (HR) during the training session.
A 5-minute warm-up, including exercises of stretching, was performed. Both groups received an individualized endurance training program which consisted of walking on the Ergo cycle for 45 minutes at 60–70% of the maximum HR reached at the end of 6MWT.
The training emphasized interval-type exercise; periods of high-intensity exercise were alternated with active recovery (10 min at 60–70% of the maximum HR alternated with 5 min of active recovery repeated over 45 min).
Both groups performed exercises for upper and lower limbs, two sets of 8–10 repetitions, with 1 minute break between exercises and two minutes between sets.
The RT is targeted to strengthen the lower and the upper limb muscles (biceps, triceps, deltoids, and pectoral muscles). The exercises consisted of leg extension, leg press, and leg curl. The training load of lower limb muscles started at 50% 1RM; then, it was set to increase to 80% 1RM. The load was set in kilograms (kg).
The NMES exercise consisted in completing three sessions a week for 24 weeks. During the NMES session, the subject was seated, and the foot was free with 60°leg flexion for maximal contraction to be produced. Quadriceps and calf muscles of both legs were stimulated electrically with two electrical stimulators (Globus 400) with four output channels. Sixteen self-adhesive (in both legs), rectangular, bipolar adhesive electrodes (5 × 5 cm2) were applied, and each of them was located on one of the anatomical motor points of the quadriceps and calf. The target muscles were vastus medialis, rectus femoris, and vastus lateralis muscles. Four electrodes were applied to the semitendinosus, and semimembranosus muscles’ motor points were previously determined, and the other electrodes were placed on the soleus and gastrocnemii (over both medial and lateral gastrocnemii) muscle motor points. This training was assessed with the following parameters: (1) symmetrical biphasic pulses fixed at 50 Hz frequency, (2) 400
Statistical analyses were realized using Statistica for Windows software (version 6.0, StatSoft, Inc., Tulsa). The normality was tested and determined using the Kolmogorov–Smirnov test.
A two-way analysis of variance (ANOVA) was used to compare baseline characteristics (anthropometric and pulmonary function) (2 groups (ET + RT and ET + NMES + RT) × 2 periods (before training and after training)).
6MWT parameters, MVC, and dynamic balance parameters (BBS and TUG) were analyzed by means of two-way ANOVA.
Static balance parameters (COP) were analyzed using a repeated-measure analysis of variance (ANOVA) with three factors: group (ET + RT and ET + RT + NMES), period (before and after), and vision (EO and EC). A post hoc test (Tukey) was performed to further analyze these results in detail. The level of significance was set at
The anthropometric characteristics and pulmonary function parameters of patients with COPD are provided in Table
Anthropometric characteristics and pulmonary function before and after the intervention.
Patient characteristics | Interventional group ( | Control group ( | |
---|---|---|---|
Gender (M/F) | 22/0 | 20/0 | – |
Age (years) | 63 ± 4 | 62 ± 6 | 0.53 |
Height (cm) | 166 ± 9 | 168 ± 7 | 0.46 |
Weight (kg) | 67 ± 15 | 67 ± 13 | 0.92 |
Body mass index, BMI (kg/m2) | 24.09 ± 5.97 | 25.14 ± 5.68 | 0.80 |
Current smoker/exsmoker | 0/22 | 0/20 | – |
Pack/years | 47 ± 6 | 49 ± 5 | 0.20 |
Dyspnea | 1.64 ± 0.72 | 1.60 ± 0.59 | 0.86 |
FEV1 (l) | 1.69 ± 0.53 | 1.73 ± 0.46 | 0.78 |
FEV1 (%) | 54.13 ± 19.85 | 54.80 ± 15.74 | 0.92 |
FVC (l) | 2.95 ± 0.78 | 3.16 ± 0.36 | 0.29 |
FVC (l) | 76.31 ± 12.77 | 80.1 ± 10.53 | 0.30 |
FEV1/FVC (%) | 57.12 ± 14.30 | 54.80 ± 6.69 | 0.11 |
Data are represented as mean ± standard deviation units. BW: body weight; BMI: body mass index; FEV1: forced expiratory volume in one second; FVC: forced vital capacity.
All statistical results of ANOVA analysis of 6MWT (6MWTD, SpO2 rest and peak, dyspnea rest and peak, and HR rest and peak), dynamic balance outcomes (TUG and BBS), MVC, and static balance (CoPML, CoPAP, and CoPV) were recapitulated in Tables
Statistical results of the ANOVA analysis of exercise tolerance, dynamic balance, and maximal voluntary contraction parameters (2-way ANOVA).
Parameters | 2-way ANOVA | |||||
---|---|---|---|---|---|---|
Group | Period | Group × period | ||||
F-value | F-value | F-value | ||||
6MWTD (m) | 5.83 | <0.01 | 173.49 | <0.001 | 5.95 | 0.024 |
SpO2 peak | 0.1 | 0.81 | 297.9 | <0.001 | 6.7 | 0.017 |
Dyspnea peak | 0.56 | 0.46 | 294.74 | <0.001 | 3.08 | 0.09 |
HR rest | 1.40 | 0.25 | 139.98 | <0.001 | 0.25 | 0.62 |
HR peak | 0.03 | 0.86 | 16.42 | 0.0006 | 0.31 | 0.58 |
TUG (s) | 4.82 | 0.04 | 399.68 | <0.001 | 4.72 | 0.04 |
BBS (score) | 0.91 | 0.1 | 305.60 | <0.001 | 13.07 | 0.002 |
MVC (N) | 4.10 | 0.05 | 431.61 | <0.001 | 9.97 | 0.005 |
6MWTD: six-minute walking test distance; SpO2: peripheral oxygen saturation; HR: heart rate; TUG: time up and go test; BBS: Berg Balance Scale; MVC: maximal voluntary contraction.
Statistical results of the ANOVA analysis of static balance parameters (3-way ANOVA).
Parameters | 3-way ANOVA | |||||
---|---|---|---|---|---|---|
CoPML (mm) | CoPAP (mm) | CoPv (mm/s) | ||||
F-value | F-value | F-value | ||||
Group | 7.49 | 0.01 | 4.25 | 0.05 | 19.19 | <0.001 |
Period | 458.23 | <0.001 | 139.4 | <0.001 | 619.91 | <0.001 |
Vision | 119.42 | <0.001 | 500.02 | <0.001 | 282.31 | <0.001 |
Group × period | 31.59 | <0.001 | 8.85 | <0.01 | 19.48 | <0.001 |
Group × vision | 0.70 | 0.41 | 0.00 | 0.98 | 4.08 | 0.05 |
Period × vision | 9.17 | <0.001 | 7.46 | <0.01 | 22.38 | <0.001 |
Group × period × vision | 0.09 | 0.76 | 0.08 | 0.77 | 0.055 | 0.81 |
CoPML: center of the pressure in the mediolateral direction; CoPAP: center of the pressure in the anterior-posterior direction; CoPv: oscillation velocity of the pressure center.
The post hoc test (Table
6MWT parameters and maximal voluntary contraction before and after the intervention.
Parameters | Intervention group ( | Control group ( | |
---|---|---|---|
6MWD | 418 ± 105 | 427 ± 61 | |
%SpO2 rest | 93 ± 2 | 93 ± 1 | |
%SpO2 peak | 88 ± 2 | 88 ± 1 | |
Dyspnea rest | 1.64 ± 0.72 | 1.60 ± 0.59 | |
Dyspnea peak | 4.18 ± 1.44 | 4.25 ± 0.85 | |
HR rest (bpm) | 82 ± 7 | 84 ± 6 | |
HR peak (bpm) | 118 ± 13 | 118 ± 8 | |
MVC (Newton meter) | 356 ± 31 | 355 ± 30 |
ET: endurance training; RT: resistance training; NMES: neuromuscular electrical stimulation; MVC: maximal voluntary contraction; SpO2: peripheral oxygen saturation; Borg: modified Borg dyspnea scale; HR: heart rate; bpm: beats per minute.
The post hoc test (Table
Mean values and standard deviations of static and dynamic balance outcomes before and after the intervention.
Intervention group: ET + RT + NMES | Control group: ET + RT | |||||||
---|---|---|---|---|---|---|---|---|
Before | After | Before | After | |||||
EO | EC | EO | EC | EO | EC | EO | EC | |
CoPML (mm) | 118.01 ± 13.77 | 146.69 ± 13.93 | 84.54 ± 10.22 | 103.67 ± 6.53 | 118.36 ± 16.96 | 144.01 ± 10.96 | 99.30 ± 12.76 | 116.78 ± 5.89 |
CoPAP (mm) | 175.03 ± 10.11 | 247.34 ± 14.72 | 160.49 ± 8.24 | 224.16 ± 17.18 | 178.16 ± 10.41 | 249.58 ± 19.59 | 169.55 ± 12.62 | 233.64 ± 14.42 |
CoPV (mm/s) | 10.03 ± 1.35 | 13.95 ± 0.96 | 7.48 ± 1.46 | 10.47 ± 0.91 | 10.83 ± 1.15 | 14.02 ± 1.27 | 9.40 ± 0.32 | 11.40 ± 0.82 |
TUG (s) | 13.57 ± 0.71 | 10.06 ± 0.48 | 13.75 ± 0.98 | 10.71 ± 0.70 | ||||
BBS (score) | 47.77 ± 4.49 | 53.68 ± 1.78 | 45.70 ± 1.79 | 55.10 ± 1.07 |
ET: endurance training; RT: resistance training; NMES: neuromuscular electrical stimulation; OE: open eyes; CE: closed eyes; CoPML: center of the pressure in the mediolateral direction; CoPAP: center of the pressure in the anterior-posterior direction; CoPv: oscillation velocity of the pressure center; TUG: time up and go; BBS: Berg Balance Scale.
The post hoc test demonstrated a significant decrease in CoPAP for the ET + RT + NMES group (
Concerning dynamic balance outcomes (Table
Our study aimed to compare two combined training modalities (RT + ET + NMES vs. RT + ET) on exercise tolerance and balance in patients with COPD.
The main finding suggests that combined training, including NMES, improved better the static and dynamic balance and exercise tolerance, as well as the lower limb strength, compared to training without NMES in patients with COPD.
As expected, the pulmonary characteristics have not changed after six months of training. These results are in agreement with previous studies [
The 6MWD increased significantly after the training program in favor of the ET + RT + NMES group. This could be explained by improved physiological conditions, a good exercise response, and a reduction of dyspnea [
Improvement in leg muscle strength in the ET + RT + NMES group could be explained by increasing capillarization and fiber-type plasticity [
The major finding of the current study is the improvement of static (CoPML, CoPAP, and CoPV) and dynamic (TUG and BBS) balance outcomes for the ET + RT + NMES group compared to the ET + RT group. These results could be explained by an increase of muscle strength [
Besides, NMES would improve the excitability and recruitment of muscle fibers and result in higher force and better coordination in the elderly [
The balance impairment is more critical in the medial-lateral (CoPML) direction in rest and during movements [
CoP improvement might be due to the improvement of the somatosensory function of the lower limbs by adding NMES. The exercise training could enhance the patients’ ability to integrate the somatosensory and vestibular inputs, becoming less reliant on the visual input while applying appropriate sensory strategies to control their posture and prevent falls [
Moreover, NMES proved its efficacy by activation of large and small motor units (MUs) [
Studies conducted in different diseases support our results. Amiridis et al. chose the ankle dorsiflexors to benefit from NMES combined with physical training. They reported that combined training reduced postural sway and improved the balance control in the anterior-posterior direction compared to the medial-lateral axis [
Concerning dynamic balance outcomes, a significant improvement was identified. BBS scores increased significantly in both groups. A better improvement in TUG scores was detected in the ET + RT + NMES group. Cho et al. showed that four weeks of treadmill training combined with NMES onto the gluteus medius and tibialis anterior muscles enhanced the BBS scores significantly. Thus, this combined training seems to be effective in improving balance performances, gait velocity, cadence, single support time, temporal asymmetry, and spatial asymmetry in stroke patients with chronic hemiparesis [
The main limitation of the study was the reduced number of patients. Given the heterogeneity of the response to NMES in the literature, emerging evidence suggested responders and nonresponder patients to NMES. Another limitation should be taken for consideration: the cardiopulmonary testing technique. The cardiopulmonary function could be evaluated by other techniques such as cardiopulmonary exercise testing and could give more measurements.
The combination of ET, RT, and NMES improves static and dynamic balance likewise in exercise tolerance in patients with COPD. This training program decreased the balance impairment and reduced dyspnea and fatigue. It could reduce the risk of falls and can be part of pulmonary rehabilitation for the patients with COPD.
The data used to support the findings of this study are included within the article.
The authors declare that there are no conflicts of interest regarding the publication of this paper.
The authors thank the patients for the invaluable contribution to this study.