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* From the Lung function and Exercise Laboratory (Ms. Vivodtzev, and Drs. Pépin, Lévy, and Wuyam), Hospital A Michallon, Grenoble, France; and the Pulmonary Rehabilitation Center (Drs. Vottero, Mayer, and Porsin) Les Rieux, Nyons, France.
Correspondence to: Bernard Wuyam, MD, PhD, EFCR, BP 217 X, 38043 Grenoble, France; e-mail: BWuyam{at}chu-grenoble.fr
Abstract
Study objectives: Low body weight in COPD patients is associated with worsening dyspnea, reduced leg strength, and poor prognosis. Classical rehabilitation strategies are then limited by reduced exercise tolerance. Thus, we proposed to evaluate whether electrostimulation (ES) was a beneficial technique in the rehabilitation programs for severely deconditioned COPD patients after an acute exacerbation.
Design: Randomized, controlled study.
Setting: Pulmonary rehabilitation center.
Patients: Seventeen patients with severe COPD (mean [ ± SD] FEV1, 30 ± 3% predicted) and low body mass index (BMI) [18 ± 2.5 kg/m2].
Methods: Patients were randomly assigned either to usual rehabilitation (UR) alone or to a UR-plus-ES program for 4 weeks. Quadriceps muscle strength, total muscle mass (MM), exercise capacity, and health-related quality of life were measured before and after rehabilitation.
Results: The training with ES plus UR induced a significant twofold improvement in the mean number of maximal voluntary contraction (MVC) compared to UR alone (97 ± 71 vs 36 ± 34 contractions, respectively; p = 0.03) and resulted in a more significant improvement in dyspnea when performing daily tasks (decrease in the dyspnea domain score of the 28-item Maugeri Foundation Respiratory Failure questionnaire, –1.7 ± 1.0 vs –0.2 ± 1.2 points, respectively; p = 0.05). There was also a significant increase in walking distance (63 ± 40 m; p = 0.01) and BMI (0.6 ± 0.5 kg/m2; p = 0.02) after training in the ES + UR group. A significant relationship was found between changes in MVC and changes in MM after training in the ES + UR group (r = 0.94; p = 0.03).
Conclusions: The combination of ES and UR was associated with greater improvement in quadriceps strength and dyspnea during the performance of daily tasks than UR alone in severely disabled COPD patients with low BMI. In this population, ES has been revealed as a useful procedure, complementing the usual pulmonary rehabilitation.
Key Words: COPD • electrical stimulation • malnutrition • nutrition • pulmonary exercise • pulmonary rehabilitation
Exercise training is a major component of pulmonary rehabilitation in patients with chronic pulmonary disease, and positive effects on exercise tolerance are now well-documented.1 However, standard rehabilitation that essentially includes aerobic training with cycle or treadmill walk exercise is harder to perform in patients with major muscle deconditioning. In patients with severe COPD who have chronic resting breathlessness, repeated exacerbations, and associated loss of muscle mass (MM), not all are capable of exercising2 and exercise training is thus not always possible to perform.3 The improvement observed after exercise training is smaller in patients with severe dyspnea compared to patients with low-to-moderate dyspnea.45
The understanding of the mechanisms of muscle dysfunction and their reversibility with rehabilitation is an important parameter to consider in COPD patients. Among the muscular abnormalities affecting COPD patients, peripheral muscle weakness67 is now recognized as an independent factor of comorbidity and of increased use of health-care resources8 in COPD patients.9101112 In addition, a low body weight in COPD patients is associated with the worsening of dyspnea, the deterioration of both generic and disease-specific health-related quality-of-life scores,13 and a lower exercise tolerance despite a similar degree of lung function impairment.14 In a careful study of how a reduction in fat-free mass (FFM) [ie, presumably a consequence of muscle wasting] impacts on the strength and endurance of leg (and arm) muscles, Franssen et al15 showed that leg strength only was significantly reduced in FFM-depleted COPD patients compared with nondepleted patients, although endurance (both for arms and legs) was similar in these subgroups of patients. This suggests that weakness rather than endurance may be an appropriate outcome to monitor in nutritionally depleted COPD patients.
Neuromuscular electrostimulation (ES) could be an alternative strategy with which to increase the muscle work performed in severely disabled underweight patients. Numerous investigations since the 1980s have shown its muscular benefits in healthy humans16171819 or in patients with muscle weakness associated with atrophy and intact innervation.20 More recent studies2122 have shown an interesting beneficial effect of ES in patients with chronic heart failure in terms of strength and endurance improvement, as well as central circulatory adaptations and enhanced aerobic capacity. Finally, preliminary results have been provided by several studies232425 in the rehabilitation COPD patients. Until now, however, a limited number of patients have been studied, and most of them were capable of performing cycle exercise and had normal body mass index (BMI), reflecting a limited disability. Thus, we prospectively studied the effects of 1 month of rehabilitation on muscle function, exercise tolerance, and health-related quality of life in 17 hospitalized COPD patients with very low BMI, who were randomly allocated to receive or not to receive ES treatment after an acute exacerbation.
Materials and Methods
Subjects
The following procedures were performed in accordance with the standards of the Committee on Human Experimentation at our institution, which approved the study. The criteria for participation in the study were as follows: (1) experiencing severe bronchial obstruction (ie, COPD and/or bronchiectasis) but with no evidence of cardiovascular, renal, or hepatic diseases; (2) FEV1 
50% predicted with an FEV1/FVC ratio of < 70%; (3) disability and malnutrition as established by a BMI of < 22 kg/m2; (4) quadriceps muscle atrophy (ie, isometric maximal voluntary contraction [MVC] of < 50% predicted26); (5) the inability to perform cycle exercise or extremely limited (ie, < 3 to 5 min) exercise tolerance at the lowest workloads (ie, < 20 W); (6) the ability to perform experimental maneuvers; (7) all patients were recruited after a sojourn in an ICU and/or after an acute exacerbation that required hospitalization, while they were subsequently admitted for 1 month as inpatients in the pulmonary rehabilitation center (Clinique "Les Rieux"; Nyons, France); (8) no acute respiratory failure at the time of the study; and (9) a signed informed consent form. Seventeen patients were thus randomly allocated to receive the usual rehabilitation (UR) [based on segmental exercises] associated with quadriceps ES (ie, the ES + UR group; n = 9) or to UR alone (ie, the control group; n = 8). Anthropometric data are shown in Table 1
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Measurements
Pulmonary Function Tests:
All measurements were made according to the recommendations of the European Respiratory Society.27 Pulmonary function tests included FEV1 and FVC using a spirometer (Masterscreenbody type B/IEC-601–1; Jaeger; Wurzburg, Germany) and a calibrated pneumotachograph. Subjects were asked to perform three maximal forced expiratory maneuvers (Labman software, version 3.43; Jaeger; Wurzburg, Germany). Measurements of arterial blood gases (ie, PaO2 and PaCO2) and pH were measured at rest while patients breathed room air using a blood gas analyzer (system 625; Radiometer ABL; Copenhagen, Denmark).
Quality-of-Life Questionnaire:
The 28-item Maugeri Foundation Respiratory Failure questionnaire (MRF-28) was chosen to assess patients’ health-related quality of life. It is a self-administered disease-specific questionnaire28 that has been validated in French29 and is particularly close to the lifestyle of COPD patients. The following three domains were investigated: daily activity (ie, sensation of dyspnea in daily tasks); cognitive function (ie, loss of memory and concentration capacity); and invalidity. For each of the 28 items, patients have to answer either "true" or "false." The score is determined as a percentage of the ratio number of "true" responses/total number of responses (ie, 28). A high score on the MRF-28 indicates a high degree of disability.
Quadriceps Muscle Strength:
Subjects were studied while they were seated on a dynamometer at 90° knee and hip flexion with the arms stretched down along their body. The legs were fixed on the chair with belts around the thighs. Quadriceps strength was measured with a strain gauge tensiometer (Dempo Technologies Co; Trevisio, Italy) linked to a digital recorder. The strain gauge transducer is designed to measure strength with a reliability of measurement of within ± 0.1% in the range of 0 to 200 kg. The signal induced was then recorded and analyzed using specific software (Ergo Meter No. 10085, DC: 6V1W; Globus Italia srl; Trevisio, Italy). Patients achieved knee extension with their two legs against resistance for 3 s. Each subject made several attempts, which were separated by a 3-min resting period (the number of attempts varied from five to seven). A maximal test was accepted if the strength obtained varied minimally (ie, < 5%) during the plateau of the strength curve on the three best different trials. The MVC was reported as the maximal value obtained.
Quadriceps Muscle Composition:
Six patients in the ES + UR group and five patients in the UR group agreed to undergo anthropometric measurements. All measurements of the circumference of the legs were performed while subjects were in a resting state. Measurements consisted of a corrected thigh circumference (CTC) determination of quadriceps skin fold thickness (QST), CTC, and total MM. All skin fold measurements were performed with the patient in a standing position, and QST was calculated with the following equation: (anterior thigh skin fold thickness + posterior thigh skin fold thickness)/2. CTC, corrected arm circumference, corrected calf circumference, and total MM were determined according to the criteria of Lee et al.30 In our laboratory, the mean between-session coefficient of variation of total MM calculated with this technique was 1.9% (range, 0.1 to 4.7%; n = 12 [unpublished data]).
6-Min Walking Distance Test.
The 6-min walking distance test was performed in a corridor that was 30 m long, following the American Thoracic Society guidelines.31 Patients were asked to walk as fast as possible for 6 min. Only standardized phrases of encouragement were used during the test.31 Oxygen desaturation was monitored throughout the test using a pulse oximeter connected to an oximeter carried on the subjects’ back. Identical procedures were used before and after training. Measurements included walking distance, rest, and 6-min pulse oximetric saturation (SpO2), end-test dyspnea (modified Borg scale of 1 to 10), and the presence or absence of desaturation to an SpO2 of 88% at the end of the test.32 Supplemental O2 was provided to each patient by nasal prongs in order to maintain the mean arterial oxygen saturation at > 90% with the flow usually used by the patients during the performance of their daily activities (ES + UR patients, 3.5 ± 2 L/min; UR patients, 3.0 ± 2 L/min).
Training Protocol
The UR program consisted of 4 days per week of active limb mobilizations (ALMs), which were performed with the patient in lying down on a physiotherapist table. The strongest patients also performed slow walking on a treadmill and 5 to 10 min of arm-lifting exercise with a 2.5-kg workload. All of the exercises were supervised by a physical therapist in a group session. In addition, patients were enrolled in health education sessions 1 day per week.
The ES program consisted of electrically induced contractions of the quadriceps, performed four times a week using an electrostimulator (Sport 400; Compex Medical SA; Ecublens, Switzerland) with three surface patch electrodes applied to each quadriceps (one patch, 8 x 4 cm; two patches, 4 x 4 cm). The patients stretched their legs out on the bed. ES was performed for > 30 min on both legs simultaneously. A symmetrical, biphasic, square-pulsed current was used. Each session comprised a 5-min warm-up period at a 5-Hz pulse width with 400 µs of continuous electrical current. Then, during the following 25 min, the stimulator generated electrical impulses at 35-Hz width for 400 µs lasting for 7 s alternated with a resting current of 5-Hz width for 400 µs lasting 8 s. The intensity applied was set as the maximal tolerable intensity by the patient and was increased by 1 to 5 mA each day. This was a strategy that allowed better tolerance to long stimulating exposures in patients with severe COPD. The initial and final mean intensities were 21 ± 6 and 46 ± 24 mA, respectively.
Statistical Analysis
All data were expressed as the mean ± SD. The level of significance for all tests was set at p < 0.05. The effect of training on muscle and functional parameters were analyzed using the Wilcoxon test for within-group comparisons. The data at baseline and the changes made after training were analyzed using the Mann-Whitney U test for between-group comparisons. Relations between changes in muscle strength and changes in walking distance, quality of life, or MM after training were analyzed using Spearman correlation tests.
Results
Patients Studied
As a whole group (n = 17), patients exhibited severe chronic bronchial obstruction (mean FEV1, 30 ± 3% predicted) and severe disability and malnutrition considering their very low mean BMI (18 ± 2.5 kg/m2) [Table 1]. Both groups showed a marked decrease in muscle strength (ES + UR group, 24 ± 18% predicted; UR group, 22 ± 11% predicted26), MM (ES + UR group 49 ± 14% predicted; UR group, 58 ± 8% predicted30), and 6 min-walking distance (ES + UR group, 42 ± 14% predicted; UR group, 39 ± 21% predicted33) [Table 2
]. No significant difference was found between groups in anthropometric and lung function variables (Table 1), and in muscle and exercise functional parameters (Table 2) at baseline.
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Respective Effects of Rehabilitation in ES + UR vs UR Patients
Lung Function and BMI:
No significant change in lung function in either group was observed at the beginning or the end of the treatment period, which suggests that airway obstruction was a fixed determinant of exercise limitation. A small but significant improvement in BMI was observed in ES + UR patients (0.6 ± 0.5 kg/m2; p < 0.02) [Table 2].
Muscle Parameters:
After the 4-week rehabilitation period, MVC increased significantly in both groups (Fig 1
, top, A) but a twofold greater improvement was observed in ES + UR patients (97 ± 71 contractions; increase, 35%) and UR patients (36 ± 34 contractions; increase, 14%; p = 0.03) [Table 2]. The application of ES was associated with an improvement in CTC (35.1 ± 6.7 vs 34.1 ± 6.5 cm, respectively; p = 0.04; increase, 3 ± 3%) without significant modification in QST, which was related to an increased MM (16.9 ± 4.8 vs 15.9 ± 4.5 kg, respectively; p = 0.035 increase, 6 ± 4%) [Table 2].
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Health-Related Quality of Life:
No between-group difference was found at baseline in health-related quality of life as assessed by the MRF-28. After training, a significant decrease in the score of the "dyspnea in daily tasks" domain of the MRF-28 was reported in the ES + UR group compared to that in UR group (–1.7 ± 1.0 vs –0.2 ± 1.2, respectively; p = 0.05) [Fig 2
]. The mean variation in MRF-28 score after training in ES + UR patients was 43 ± 12% vs 58 ± 13%, respectively (p = 0.035), and 53 ± 24% vs 53 ± 24%, respectively, in UR patients (p = 0.85).
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This study sought to evaluate whether ES was a useful additive strategy to UR (ie, ALM) in severely deconditioned COPD patients with low BMIs who were unable to perform cycle ergometry. Our results showed that ES was feasible to perform and was well-tolerated by these patients. The main result of this study was that the combination of ES and UR enabled improvements in quadriceps muscle strength and dyspnea in the performance of daily tasks to a greater extent than UR alone.
Effects of ES on Muscle Strength
Compared to UR alone, training with ES plus UR was associated with a greater improvement in quadriceps isometric muscle strength (35% vs 14%, respectively; p = 0.03). One limitation of our study would be that the tester was not blinded during effort-dependent measurements. However, identical encouragement was used for patients in both groups before and after training, and the maximal strength value was accepted only if the percentage of variation of the three successive strength measurements performed by the patient was < 5%. Thus, the probability for an overestimation of the posttraining measurements was very low. Our results are in accordance with those of other previous randomized controlled studies that have reported significant increase in peripheral muscle strength in stable COPD patients. After a 6-week ES training period in COPD patients (FEV1, 38% predicted), Bourjeily-Habr et al23 reported a significant improvement in isokinetic leg extension peak torque (+ 39%) compared to that in a sham ES group. Neder et al24 also showed an increase in the isokinetic measurement of the quadriceps extension (+ 42%) compared to that in an untrained control group. Neither of these studies, however, was performed in similarly disabled COPD patients after exacerbation. In a third study,25 which was performed in an ICU that investigated the additional effect of ES with ALM, an increase in muscle strength was also suggested (clinical score of strength: after ES + ALM treatment, 2.16 ± 1.02; after ALM treatment, 1.25 ± 0.75; p = 0.02). This was translated into a decrease in the number of days needed to go from bed to chair, and thus the time to leave the ICU. No direct evaluations of peripheral muscle strength and/or exercise performance were performed, however, in that study.25
Using similar isometric measurements, the muscle strength increase observed in our study was of greater magnitude than that previously reported by Neder et al24 using ES alone (+ 35% vs + 18%, respectively). This was observed despite a shorter period of training (4 weeks in the present study vs 6 weeks in the study by Neder et al24) and with a lower mean maximal intensity having been achieved by the end of the training period (electrical intensity increased from 21 ± 6 to 46 ± 24 mA in our study, although it increased from 10 to 20 mA to 100 mA in the study by Neder et al,24 and from 56.7 ± 7.0 to 95.0 ± 4.2 mA in the study by Bourjeily-Habr et al23). There were several explanations for that. We used a lower intensity but a longer contraction time during the ES sessions. Thus, the contraction/relaxation time ratio in our protocol was twofold higher than those used for the ES protocols in the studies by Bourjeily-Habr et al23 and Neder et al24 (50% vs 13% and 10 to 25%, respectively). Moreover, the reduced leg adipose tissue observed in the present subgroup of patients (QST, 1.07 ± 0.67 mm) [Table 2] may have been a favorable factor in face of the low intensity used, thus reducing the electrical impedance to muscle activation. Finally, since sensory discomfort is related to electrically induced current intensity,34 lower intensity may have promoted an acceptable clinical tolerance of ES.
Mechanisms of Change in Muscle Strength
The mechanisms for improvements in muscle strength observed after any form of training can be peripheral or central in nature. Although low-frequency ES acts by the direct stimulation of muscle fibers, as reflected by changes in size3536 and/or biological profile3738 after chronic stimulation, the hypothesis of an increase in strength due to changes in central neural activation levels must be considered in the present study. After bed rest, using the twitch interpolation technique, Kawakami et al39 have shown that muscle strength deficit can be of central origin (ie, a decreased ability to activate motor units). This situation might have been reversed by voluntary and active mobilization.40 When specifically looking for the benefits of ES, one limitation of our study is that we did not have a sham ES group, nor did we record EMG data during ES sessions. Thus, one can speculate as to whether voluntary assistance during or in anticipation of ES may thus be a confounding factor for the increase in strength brought about by the procedure. No specific instruction was given to patients to add volitional muscle contraction simultaneously with ES. Whether contractions were in phase with ES (and presumably due to ES) could easily be checked by the physiotherapist in these thin patients, and no clear or overt cocontraction (which could be volitionally performed) was detected. Furthermore, a similar ALM program was performed in each group. Thus, although we cannot exclude that subconscious voluntary assistance had occurred, we think that this is unlikely to explain the whole difference observed between the ES + UR and UR groups in the present study. As can be seen in Figure 3, a close correlation between the increase in muscle strength and the increase in MM was observed after training in the ES + UR group. The gain in strength, however, seemed to be of greater magnitude when using ES in addition to UR (ie, a greater gain in strength per unit of gain in MM) than in the UR group. The limited resolution of anthropometric measurements and/or the limited number of observations may act as confounding factors for this between-group difference, however. Although the correlation between MM and strength observed in the ES + UR group would seem to support the hypothesis of muscle hypertrophy obtained with ES, additional factors such as central activation improvement (due to active and volitional contraction associated with ES) and/or improvement in excitation-transmission coupling may have also played a role. Additional observations may attempt to clarify this issue.
Effects of ES on Exercise Capacity
Gains in quadriceps muscle strength, however, do not translate into short-term improvements in exercise capacity, as reflected by the 6-min walking distance evaluation. Although a significant (and clinically noticeable41) increase in the walking distance was observed in the ES + UR group (63 ± 40 m; p = 0.01), the between-group difference in walking distance improvement was not significant (p = 0.12). A lower increase in walking distance was observed in the UR alone group (30 ± 38 m; p = 0.08). We cannot exclude the possibility that the lack of significance may be attributed to a ß-type error and insufficient statistical power due to the small number of patients tested. Larger trials may be mandatory for definitive conclusions to be achieved on the positive effect of ES on exercise capacity and tolerance in patients with similarly severe COPD, which has been previously suggested by authors in steady-state patients with COPD.2324
Other studies4243 have led to similar conclusions in patients with moderate-to-severe COPD using different forms of peripheral muscle training. Van’t Hul et al,44 for instance, investigated the impact of strength on the exercise capacity of COPD patients. As an example, endurance work correlates with MVC in patients with moderate COPD, but not in those with severe COPD. This may also suggest that, among the factors involved in the walking exercise performance, an increase in quadriceps muscle strength might have a variable impact on walking performance. Additionally, the quadriceps muscle only, as the main muscle involved in static upright maintenance of the body, was trained in the present study. The weakness of untrained lower-limb muscles might have restrained the improvement in walking performance observed.
Finally, in our study, we did not report minute ventilation measurements. Others, (Bourjeily-Habr et al23) observed a small but significant decrease in dead space ventilation and perceived exertion during exercise (Borg scale) in the ES group after training. Thus, a decrease in ventilatory requirement during walking exercise after training could also be present in our study. Further studies are needed to determine the real impact of changes in muscle strength on walking performances and especially via a decrease in exercise-induced ventilation at a given submaximal exercise level.
Effects of ES on Quality of Life and BMI
The greater decrease after training in the score on the domain of dyspnea in daily tasks, as assessed by the MRF-28 in the ES + UR group compared to the UR group (p = 0.05), is in accordance with the previous results observed in steady-state COPD patients24 and would confirm the greater improvement induced by ES training in the dyspnea domain of health related-quality of life in COPD.
Interestingly, in our study, increased muscle function was associated with a 3% increase in BMI in ES + UR patients. In a 2003 study45 investigating the prognostic value of nutritional depletion in patients with COPD treated by long-term oxygen therapy, the authors showed that BMI was the most powerful predictor of duration and rate of hospitalization, independent of blood gas levels and respiratory function. Furthermore, an increase in BMI from < 20 to 20 kg/m2 to < 24 kg/m2 would induce an increase in 5-year survival rates from 24 to 34% (p < 0.001) in these COPD patients who were receiving long-term oxygen therapy.45 In this respect, a mean rise in BMI of 0.6 ± 0.5 kg/m2 as observed in the present study after a 4-week training program may have a real clinical interest. In comparison, 8 weeks of nutritional supplementation therapy (based on a mean intake of 2,812 ± 523 kJ/24 h) had induced an increase in FFM of 1.1 ± 2.0 kg (p < 0.001) in depleted patients with COPD.46
In summary, ES can improve quadriceps muscle strength and dyspnea in performing daily tasks, independently of volitional exercise and without an increase in self-perceived dyspnea during the training session, to a greater extent than that reported with UR, in severely deconditioned and malnourished patients with COPD. Clinical interest in ES is probably essentially directed toward disabled patients who are unable to perform usual exercise on a regular basis, as is required in rehabilitation programs. In this context, ES may be a useful alternative in the rehabilitation of disabled patients with severe COPD.
Footnotes
Abbreviations: ALM = active limb mobilization; BMI = body mass index; CTC = corrected thigh circumference; ES = electrostimulation; FFM = fat-free mass; MM = muscle mass; MRF-28 = 28-item Maugeri Foundation Respiratory Failure questionnaire; MVC = maximal voluntary contraction; QST = quadriceps skin fold thickness; SpO2 = pulse oximetric saturation; UR = usual rehabilitation
This research was supported by grants from the Association pour le Traitement, la Rééducation et la Réadaptation des Insuffisants Respiratoires (ATRIR), "Bourse André Dion," Nyons, France.
Received for publication July 19, 2005. Accepted for publication December 9, 2005.
References
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  A. L. Ries, G. S. Bauldoff, B. W. Carlin, R. Casaburi, C. F. Emery, D. A. Mahler, B. Make, C. L. Rochester, R. ZuWallack, and C. Herrerias Pulmonary Rehabilitation: Joint ACCP/AACVPR Evidence-Based Clinical Practice Guidelines Chest, May 1, 2007; 131(5_suppl): 4S - 42S. [Abstract] [Full Text] [PDF]
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) and walking distance (bottom, B; 
) measured before (pre) and after (post) the 4-week rehabilitation programs in ES + UR patients (black points) and in UR patients (white points). * = p < 0,05; ** = p < 0.01. Between-group comparisons were analyzed at baseline (not significant [NS]) and between changes after and before training (MVC, p = 0.03; walking distance, p = 0.12).
). The Spearman correlation coefficient were r = 0.94 (p = 0.03) and r = 0.30 (p = 0.54), respectively.