METHODS

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Patients with COPD were recruited for this study. The diagnosis was based on smoking history and on pulmonary function tests showing irreversible bronchial obstruction defined by less than 12% and less than a 200-ml increase of initial FEV₁ after administration of salbutamol (400 μg via a metered dose inhaler) (22, 23). The training program conducted at our institution was developed in 3 alternate days each week for 12 weeks. Subjects were randomly assigned to endurance training alone, strength training alone, combined training modality (endurance and strength), or a control group.

The endurance training consisted of 40-minute leg exercises on a calibrated ergocycle. The work rate corresponding to 70% of the peak work rate achieved during the baseline incremental exercise test was selected as the target training intensity (24). The strength-training program included different exercises, which were performed with the following weight lifting procedures: (1) “chest pull” (mainly for strengthening of the latissimus dorsi), (2) “butterfly” (mainly for the pectoralis major muscle), (3) “neck press” (mainly for the triceps brachii and deltoid), (4) “leg flexion” (mainly for the biceps femoris and grastrocnemius), and (5) “leg extension” (mainly for the quadriceps femoris). The weight lifting exercises were performed with gymnastic apparatus. The patients performed four series of six to eight repetitions for each of the exercises included in the strength-training program at a workload of 70 to 85% of the one repetition maximum. This test was repeated each 2 weeks for new adjustment of the workload. The combined training modality included two series of six to eight repetitions of the five weight-lifting procedures plus 20 minutes of cycling.

Subjects were evaluated on 2 consecutive days at baseline, at the end of the 12-week training program, and at 12 weeks after training. Spirometry was measured with a pneumotachograph (25). Static lung volumes were determined in a constant-volume whole-body plethysmograph. Arterial blood was sampled at the radial artery while the patients breathed room air for at least 1 hour in the sitting position (26).

Weight-lifting capacity was measured as the heaviest weight that could be lifted once throughout the complete range of movement (one repetition maximum). Testing took place on 2 separate days, and the heaviest weight lifted was recorded as the pretraining value (12, 27). Progressive exercise testing was performed to a symptom-limited maximum on an electronically braked cycle ergometer. Patients began with a 3-minute period of unloaded pedaling at 60 rpm followed by 1-minute stepwise increments of 10 W. The concentrations of expired O₂ and CO₂ were analyzed breath by breath with a zirconium dioxide-cell O₂ analyzer and an infrared CO₂ analyzer, respectively (28). A submaximal endurance cycling test was performed on a calibrated cycle ergometer at 70% of the maximum power output achieved during the baseline incremental exercise test. Other measurements included the shuttle-walking test in which patients were requested to walk between two cones placed 10 m apart (the end point was when the patient was unable to maintain the required speed) (29), chronic breathlessness using the modified Baseline Dyspnea Index (30), and health-related quality of life using a Spanish-validated version of the Chronic Respiratory Questionnaire (31, 32). The analysis of variance for repeated measures was used for within-group and between-group comparisons. Additional information on the methods can be accessed in the online data supplement.

RESULTS

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Seventy-two patients with moderate to severe obstruction in a stable phase of COPD were studied (data of 18 control subjects are not shown). Of the 54 patients assigned to training interventions, seven patients (one in the strength group, two in the endurance group, and four in the combined group) failed to complete the program because of exacerbations of COPD requiring hospitalization (n = 4) or a lack of motivation for exercise training (n = 3). Baseline characteristics of the remaining 47 patients, who constituted the study population, are presented in Table 1

DISCUSSION

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This study confirms the beneficial effects of the three modalities of exercise training (strength, endurance, or combined) on dyspnea and quality of life in patients with COPD. Improvement of these parameters persisted at 3 months after the training intervention. Strength training was well tolerated and was superior to endurance to improve muscle strength. Endurance training was superior to strength to improve submaximal exercise tolerance, and the combined modality produced improvements in peripheral muscle strength and endurance comparable to those obtained by each modality alone. The combined group acquired most of the benefits of each intervention and seems an optimal strategy for patients with COPD. These results may therefore contribute to optimizing training and to provide guidance for the design of rehabilitation exercise programs.

Exercise intolerance is often the COPD patient's chief complaint. There is accumulating evidence that the skeletal muscles (most importantly, the muscles of deambulation) do not function normally and that this dysfunction contributes to exercise intolerance (7). In a recent study in which needle biopsies of the vastus lateralis before and after endurance training were obtained (33), patients with COPD showed a reduced ability to adapt to endurance training reflected in lower capacity to synthesize the antioxidant, reduced glutathione. The cause of physical impairment in COPD has received increasing attention. It has been shown that dynamic hyperinflation reduces the ability to increase tidal volume during exercise in patients with COPD and contributes importantly to dyspnea and exercise intolerance (34, 35). Reduced diaphragm pressure-generating capacity during exhaustive exercise in patients with COPD is secondary to the development of dynamic hyperinflation rather than to an inhibition of central drive (36). In addition, improvement in exercise endurance with hyperoxia has been explained by a combination of reduced ventilatory demand, a decrease in end-expiratory volume, and dyspnea alleviation (37). It has been recently suggested that the addition of domiciliary noninvasive positive pressure ventilation to an exercise-training program in severe COPD may produce greater benefits in exercise tolerance and quality of life than after training alone (38).

On the other hand, extensive deconditioning is a major contributor to the muscle dysfunction seen in COPD patients. In addition to using exercise training in motivating patients toward a higher level of activity and desensitization to dyspnea (39), rigorous programs of endurance training are primarily of value because they are capable of inducing physiologic changes in muscles of ambulation that improve exercise tolerance in patients with both moderate and severe COPD (40–43). The majority of established exercise programs are based on endurance training of the lower limbs with different exercise modalities, such as walking, treadmill, and stationary bicycle. Although exercise rehabilitation programs have systematically omitted activities of strength training primarily because of fear of an abrupt increase in heart rate and arterial pressure associated with isometric contractions in small muscle groups, recent studies (19–21), including these findings, have shown that strength training is beneficial and well tolerated as well. Moreover, in patients with mild COPD, Clark and colleagues (18) identified reduced isokinetic muscle function as compared with healthy subjects and showed that intervention with weight training was effective in countering this deficit.

Some aspects of this study deserve to be mentioned. Data based on small samples should be interpreted taking this limitation into account, and further studies with a larger number of patients in each training modality group will help to confirm these findings. In this respect, the absence of statistically significant differences in submaximal exercise capacity between the endurance-training group (33.6 minutes) and the combined training modality group (24 minutes) was probably caused by a type II error as a β level of 0.20 may not have been sufficiently high to show equivalence between treatment groups. Changes in muscle mass were not measured as opposed to the study of Bernard and colleagues (21). These authors showed that the addition of strength training to aerobic training was associated with significantly greater increases in the thigh muscle cross-sectional area measured by computed tomographic scanning than in the aerobic group, but in this study, a strength-training group was lacking.

After training, the improvement in the shuttle-walking test was only statistically significant in the strength-training group, whereas in the endurance- and combined-training modalities, improvements in the distance walked were not significant. However, between-group differences were not found. Atrophy of type II fibers have been shown in cross-sectional areas of muscle biopsies in patients with COPD (44). On the other hand, strength training in healthy subjects results in selective hypertrophy of type II fibers (12, 27), which are mainly recruited for explosive effort. Because of this effect, it may be possible that strength training might have a greater effect on the shuttle-walking test. It is incremental in nature and therefore more a measure of exercise capacity than of endurance. It has been shown, however, that assessing patient performance during a 6-minute walking test is improved when factors other than the distance walked (including endurance capacity, the pattern of heart rate, perceived symptoms, and impairment of oxygen transport) are also measured (45).

These results suggest that there is a certain degree of specificity in the training response as patients in the combined training modality improved muscle strength and endurance at comparable levels than in the training modalities of strength and endurance alone, but in a significantly higher magnitude in strength compared with the endurance-training modality alone as well as in endurance compared with the strength-training modality alone. Moreover, in the endurance-training modality, increases in the strength measures involving the upper extremities were lower compared with increases in the strength measures involving the lower extremities and also markedly lower (and probably with little clinical significance) than those obtained for the lower extremities in the strength-training group and in the combined-training modality. This may be explained by different factors, such as general improvement in muscle function after a regular program of endurance training, the effect of calisthenic exercises involving the upper extremities performed in the warm-up sessions (46), or isometric contractions of the muscles of the upper extremities when leaning arms against handlebars during cycling.

Although rehabilitation improves exercise tolerance and quality of life and may also benefit aspects of cognitive performance (47) in patients with COPD, it is not known whether these improvements are related to different modalities of exercise training. In the three training modalities tested in this study, improvements in different dimensions of the baseline dyspnea index and the chronic respiratory questionnaire were obtained. However, there were no differences when comparing increments in the scales of these instruments in each training modality. Bernard and colleagues (21) concluded that the addition of strength training to aerobic training achieved an increase in peripheral muscle strength but did not offer additional advantages as far as quality of life. Perhaps changes in peripheral muscle function in our study are not large enough to be reflected in the tests used, or perhaps these are not sensitive enough to capture said changes. Another possible explanation of the dissociation could be the relative specificity of the training stimulus so that greater function improvements take place in those tests using trained movements. This would imply that these movements should be similar to the most relevant activities in the patient's daily life. This way perhaps we could achieve greater improvement in quality of life. Another explanation could be lack of adjusting the training modality to individualized needs. It is likely that according to baseline characteristics (e.g., severe muscle atrophy) some patients with COPD could be benefited more by a program designed to improve strength and thus would gain more benefits in quality of life.

Exercise programs should be maintained because benefits disappeared if exercise is discontinued. However, benefits seem to continue for some time, regardless of whether follow-up training sessions are incorporated in the long-term management of patients with COPD. In a critical review and meta-analysis of studies evaluating the long-term effects of pulmonary rehabilitation (48), significant summary effect sizes (computed by pooling standardized mean differences as well as raw mean differences) were found up to 9 months after finishing pulmonary rehabilitation for maximal exercise capacity and 6-minute walking distance. In this critical review, however, patients with asthma and COPD were included. In our study, the comparisons between the end of 12 weeks of training and 3 months after the training intervention should be interpreted with caution. At 3 months after the training intervention, endurance parameters hardly varied in any of the training modality groups, whereas a greater loss in muscle strength was observed in the strength and combined training modality groups compared with the endurance-training group. There was no loss in strength in the endurance group because gain in strength during the training period was significantly lower than in the other two groups.

In summary, combined exercise training, including strength and endurance, seems more physiologically complete, achieving significant improvements in strength and endurance that were comparable to those obtained by each specific training program alone. These effects, however, were similar in respect to amelioration of dyspnea and benefits in quality of life. Three months after the training intervention, peripheral muscle strength seemed to diminish more rapidly than endurance gains, but the benefits of any training modality on endurance, breathlessness, and quality of life remained almost unchanged.