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(Chest. 2003;124:1357-1364.)
© 2003 American College of Chest Physicians

Comparison of Specific Expiratory, Inspiratory, and Combined Muscle Training Programs in COPD*

Paltiel Weiner, MD; Rasmi Magadle, MD; Marinella Beckerman, MD; Margalit Weiner, PhD and Noa Berar-Yanay, MD

* From the Department of Medicine A, Hillel Yaffe Medical Center, Hadera, Israel.

Correspondence to: Paltiel Weiner, MD, Department of Medicine A, Hillel Yaffe Medical Center, Hadera, Israel 38100; e-mail: weiner{at}hillel-yaffe.health.gov.il


   Abstract
TOP
 Abstract
Introduction
 Patients and Methods
 Results
 Discussion
 References
 
Background: Respiratory muscle weakness may contribute to dyspnea and exercise limitation in patients with significant COPD. In an attempt to reduce the severity of breathlessness and to improve exercise tolerance, inspiratory muscle training has been applied in many COPD patients. On the other hand, there is a paucity of data related to expiratory muscle performance and training in COPD.

Methods: Thirty-two patients with significant COPD (ie, mean FEV1, 37% of predicted) were recruited for the study. The patients were randomized into four groups: eight patients were assigned to receive specific expiratory muscle training (SEMT); eight patients received specific inspiratory muscle training (SIMT); eight patients received SEMT and SIMT (ie, the SEMT + SIMT group); and eight patients who were assigned to a control group received training with very low load. All patients trained daily, six times a week, with each session consisting of one half hour of training, for 3 months. Spirometry, respiratory muscle strength and endurance, 6-min walk test distance, the perception of dyspnea, and the Mahler baseline dyspnea index (BDI) were measured before and following training.

Results: Training caused a statistically significant specific increase in the expiratory muscle strength and endurance (in the SEMT and SEMT + SIMT groups) and in the inspiratory muscle strength and endurance (in the SIMT and SEMT + SIMT groups). There was significant increase in the distance walked in 6 min in the SEMT, SIMT, and SEMT + SIMT groups. However, the increase in the SIMT and SEMT + SIMT groups was significantly greater than that in the SEMT group. There was a statistically significant increase in the BDI, and a decrease in the mean Borg score during breathing against resistance in the SIMT and SEMT + SIMT groups, with no changes in the SEMT and control groups.

Conclusions: The inspiratory and expiratory muscles can be specifically trained with improvement of both muscle strength and endurance. The improvement in the inspiratory muscle performance is associated with an increase in the 6-min walk test distance and the sensation of dyspnea. There is no additional benefit gained by combining SIMT with SEMT, compared to using SIMT alone.

Key Words: exercise performance • expiratory and inspiratory muscle training • sensation of dyspnea


   Introduction
TOP
 Abstract
 Introduction
Patients and Methods
 Results
 Discussion
 References
 
Patients with significant COPD have respiratory and peripheral muscle weakness, but it does not affect all muscles to a similar extent.1 Respiratory muscle weakness may contribute to dyspnea and to exercise performance.2 3 Therefore, trying ventilatory muscle training in these patients was a rational decision designed to enhance respiratory muscle function, and, potentially, to reduce the severity of breathlessness and to improve exercise tolerance.

Inspiratory muscle training was extensively investigated in patients with COPD. It has been shown, in studies in which the training stimulus was adequate,3 4 5 6 7 that in most COPD patients dyspnea and functional exercise capacity may improve as a result of such training. The joint committee of the American College of Chest Physicians/American Association of Cardiovascular and Pulmonary Rehabilitation8 declared that when the stimulus or load placed on the respiratory muscles during training is sufficient to augment inspiratory muscle strength, there is an associated increase in exercise capacity and decrease in dyspnea.

The expiratory muscles (ie, abdominal muscles and the internal intercostal muscles) were investigated to a much lesser extent in COPD patients. These muscles have been found to be recruited in such patients both at rest and during loaded breathing.9 The significance of this activation has not been well-defined. However, there are several reports showing that expiratory muscle strength2 10 and endurance11 also can be impaired in COPD patients.

The expiratory muscles were specifically trained in several settings other than COPD. Such training tended to enhance expiratory muscle strength and to improve cough efficacy in severely disabled multiple sclerosis patients,12 to improve the perception of dyspnea (POD) in children with neuromuscular disease,13 and to reduce the sensation of respiratory effort during exercise in healthy subjects.14 When patients with COPD were nonspecifically trained with normocapnic hyperpnea,15 the strength of both the inspiratory and expiratory muscles was increased, with beneficial effects on exercise performance and quality of life. In the present study, we wanted to compare the effects of specific expiratory muscle training (SEMT), specific inspiratory muscle training (SIMT), and the combination of both, on respiratory muscle performance, exercise performance, and the sensation of dyspnea in patients with significant COPD.


   Patients and Methods
TOP
 Abstract
 Introduction
 Patients and Methods
Results
 Discussion
 References
 
Subjects
Thirty-two patients (26 men and 6 women) with spirometric evidence of significant chronic air-flow limitation (ie, FEV1 of < 50% of predicted and FEV1/FVC ratio of < 70% of predicted) in whom COPD had been diagnosed, according to the criteria of the American Thoracic Society,16 were recruited for the study. They were all observed during a 4-week run-in period, in which their regular treatment was maintained, to verify stability in their clinical and functional status. Their characteristics are summarized in Table 1 . The results of individual pulmonary function tests are summarized in Table 2 . Patients with cardiac disease, poor compliance, a requirement for supplemental oxygen therapy, or CO2 retention were excluded from the study.


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  		Table 1.. Characteristics of Patients With COPD*

 

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  		Table 2.. Individual Pulmonary Function Tests of Patients With COPD*

 
Study Design
All tests were performed before the training period and within 1 week after its completion. The patients were randomized into the following four groups: eight patients were assigned to receive SEMT; eight patients were assigned to receive SIMT; eight patients were assigned to receive a combination of SEMT and SIMT (ie, the SEMT + SIMT group); and eight patients who were assigned to a control group received training with a very low load.

In all patients, we performed several practice tests before obtaining the baseline value in order to correct possible training and learning effects. All the data were collected by the same collector, who was blinded to the training group as well as to the patients themselves, who also were blinded to the mode of treatment. The study protocol was approved by the institutional ethics committee, and informed consent was obtained from all the subjects.

Tests
Spirometry: The FVC and FEV1 were measured three times on a computerized spirometer (Compact; Vitalograph; Buckingham, UK), and the results of the best trial are reported.

6-Min Walk Test: The distance that the patient was able to walk in 6 min was determined in a measured corridor, as described for the 12-min walk test by McGavin and coworkers.17 The patients were instructed to walk at their fastest pace and to cover the longest possible distance over 6 min under the supervision of a physiotherapist. The test was performed twice, and the best result is reported.

Respiratory Muscle Strength: Respiratory muscle strength was assessed by measuring the maximal inspiratory pressure (PImax) and the maximal expiratory pressure (PEmax) at residual volume and total lung capacity, respectively, as previously described by Black and Hyatt.18 Mouth pressures were measured with a mouthpiece (model 1002; Vacumed; Ventura, CA) that has a small air leak to prevent pressure generation by glottis closure and is connected to a pressure transducer, and the data were recorded on a strip chart recorder. The value obtained from the best of at least three efforts was used.

Respiratory Muscle Endurance: To determine inspiratory muscle endurance, a device similar to that proposed by Nickerson and Keens19 was used. Subjects inspired through a two-way valve (Hans-Rudolph; Kansas City, MO), the inspiratory port of which was connected to a chamber and plunger to which weights could be added externally. Inspiratory elastic work then was increased by the progressive addition of weights of 25 to 100 g at 2-min intervals, as previously described by Martyn and coworkers,20 until the subjects were exhausted and could no longer inspire. The pressure achieved with the heaviest load (tolerated for at least 60 s) was defined as the peak inspiratory pressure (PImpeak).

To determine expiratory muscle endurance the subjects inspired through a two-way Hans-Rudolph valve whose inspiratory port was open to room air with no load and the expiratory port was connected to the expiratory port of a threshold muscle trainer (Threshold Inspiratory Muscle Trainer; Health-Scan; Cedar Grove, NJ). The expiratory load was then increased by the progressive addition of 10 to 20 cm H2O at 2-min intervals until the subjects were exhausted and could no longer continue. The pressure achieved with the highest load (tolerated for at least 60 s) was defined as the peak expiratory pressure (PEmpeak).

Dyspnea: Dyspnea was assessed using the following two techniques:

  1. Dyspnea in daily activities was assessed with the Mahler baseline dyspnea index (BDI).21
  2. The POD also was measured while the subject breathed through the same device proposed by Nickerson and Keens.19 The subjects breathed against progressive resistance, at 1-min intervals, in order to achieve mouth pressures of 0 (ie, no resistance), 5, 10, 20, and 30 cm H2O. In a protocol similar to the one previously described by our group,22 after breathing for 1 min at each inspiratory load the subjects rated the sensation of difficulty in breathing (ie, dyspnea) using a modified Borg scale.23 This is a linear scale of numbers ranking the magnitude of difficulty in breathing ranging from 0 (none) to 10 (maximal).

Training Protocol
Subjects in all groups trained daily, six times a week, with each session consisting of 1 h, for 3 months. The SEMT group received one half hour of SEMT plus one half hour of SIMT with a low load (7 cm H2O). The SIMT group received one half hour of SIMT plus one half hour of SEMT with a low load. The SEMT + SIMT group received one half hour of SEMT plus one half hour of SIMT, and the control group one half hour of SEMT with a low load plus one half hour of SIMT with a low load.

The training was performed using a threshold inspiratory muscle trainer (Threshold Inspiratory Muscle Trainer; Healthscan). The subjects started breathing at a resistance equal to 15% of their PImax or PEmax for 1 week. The resistance then was increased incrementally 5 to 10% each session, to reach 60% of their PImax or PEmax at the end of the first month of training. SEMT and SIMT then were continued at 60% of the PImax or PEmax and was adjusted weekly to the new PImax or PEmax achieved. Low load was defined as a fixed resistance of 7 cm H2O.

Data Analysis
The results are expressed as the mean ± SEM. Correlations were assessed by calculating Spearman correlation coefficients. Comparisons of lung function, respiratory muscle strength and endurance, the results of a 6-min walk test, and the rating of dyspnea within and between the four groups were carried out using the two-way repeated-measures analysis of variance.


   Results
TOP
 Abstract
 Introduction
 Patients and Methods
 Results
Discussion
 References
 
There were no differences among the four groups in age, height, and weight at the beginning of the study.

Spirometry
The mean baseline values of FEV1 and FVC were similar in all four groups (Table 1) . Following the training period, there was no significant change in FEV1 or FVC in either the training groups or in the control group. Although some of the patients may have had somewhat low FVC values, there was no evidence of additional restrictive lung disease.

Respiratory Muscle Strength and Respiratory Muscle Endurance
Before the training period, there were no differences in PImax, PEmax, PImpeak, or PEmpeak between the study groups and the control group. Following the training period, there was a statistically significant increase in mean PEmax in the SEMT group (83 ± 4.7 to 100 ± 4.9 cm H2O) and the SEMT + SIMT group (79 ± 4.4 to 105 ± 4.9 cm H2O; p < 0.005), but not between the groups. There was no change in PEmax in the SIMT and control groups (Fig 1 ). There was a statistically significant increase in PImax in the SIMT group (48 ± 2.7 to 60 ± 3.3 cm H2O) and the SEMT + SIMT group (42 ± 2.6 to 56 ± 2.9 cm H2O; p < 0.005), but not between the groups. There was no change in PImax in the SEMT and control groups (Fig 1) .



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  		Figure 1.. Respiratory muscle strength, as assessed by the PEmax and the PImax, before and following the training period.

 
Expiratory muscle endurance, as assessed by the PEmpeak, also increased significantly in the SEMT group (55 ± 2.9% to 72 ± 3.2%) and the SEMT + SIMT group (55 ± 2.9% to 69 ± 3.1%; p < 0.001), but not in the SIMT and control groups, and not between the groups. Inspiratory muscle endurance, as assessed by the PImpeak, increased significantly in the SIMT group (48 ± 2.7% to 60 ± 3.1) and SEMT + SIMT group (42 ± 2.6% to 56 ± 3.0%; p < 0.001), but not in the SEMT and the control groups, and not between the groups (Fig 2 ).



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  		Figure 2.. Respiratory muscle endurance, as assessed by the PEmpeak and the PImpeak, before and following the training period.

 
6-Min Walk Test
There were no statistically significant differences among the four groups in the results of the 6-min walk test before the study (Table 1) . Following the training period, there was a small but significant increase in the mean distance walked in 6 min in the SEMT group (27 ± 41 to 304 ± 47 m; p < 0.05), the SIMT group (276 ± 44 to 347 ± 47 m, p < 0.05), and the SEMT + SIMT group (297 ± 47 to 345 ± 47 m; p < 0.05), but not in the control group (Fig 3 ). As shown in Figure 3 , there were no statistically significant differences between the SEMT + SIMT group and the SIMT group.



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  		Figure 3.. The distance walked in 6 min before and following the training period. 6MW = 6-min walk.

 
Dyspnea-Mahler BDI
There were no statistically significant differences among the four groups in the different components of the BDI (Table 3 ). Following the training period, there were statistically significant mean increases in the BDI in the SIMT group (5.2 ± 0.8 to 7.3 ± 1.0; p < 0.01) and in the SEMT + SIMT group (4.8 ± 0.8 to 7.3 ± 0.9; p < 0.01), with no change in the SEMT and control groups.


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  		Table 3.. Values at Baseline and Following Training for Dyspnea in the Training Groups and in the Control Group*

 
POD
There were no differences in the POD among the four groups before training. A statistically significant decrease in the mean Borg score during breathing against resistance was associated with an increase in inspiratory muscle strength in the SIMT group (p < 0.05) and in the SEMT + SIMT group (p < 0.05). However, no change in the POD was associated with an improvement in expiratory muscle performance (ie, in the SEMT group) [Fig 4 ].



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  		Figure 4.. Baseline mean ± SEM POD (Borg score) during breathing against load in all COPD patients and following training in the four groups.

 

   Discussion
TOP
 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
References
 
This study shows that respiratory muscle strength and endurance are impaired in patients with significant COPD. In addition, it shows that the inspiratory and expiratory muscles can be specifically trained, with improvement of both muscle strength and endurance. The improvement in the inspiratory muscle performance is associated with an increase in exercise performance and sensation of dyspnea in daily activities. There is no additional benefit on exercise performance and in the sensation of dyspnea in daily activities in the SEMT group in addition to the SIMT group.

The evidence that the respiratory muscle weakness may contribute to dyspnea and exercise limitation in patients with significant COPD2 3 has led many investigators to train the inspiratory muscles in COPD patients in an attempt to reduce the severity of breathlessness and to improve exercise tolerance. The scientific evidence about inspiratory muscle training at the present time is somewhat controversial. However, in a meta-analysis of 17 articles on SIMT,24 it has been shown that when the training stimulus was adequate to induce significant improvement in respiratory muscle performance there was a significant reduction in the severity of dyspnea and improved functional exercise capacity.

There is much less data related to the expiratory muscles (ie, abdominal muscles and the internal intercostal muscles) in COPD patients. There are several reports2 11 25 showing that expiratory muscle strength is impaired in most patients with significant COPD. While inspiratory muscle weakness is usually considered to be caused by hyperinflation, placing the inspiratory muscles at a mechanical disadvantage, the expiratory muscles partake in the generalized muscle weakness that is observed in patients with COPD.26 The decreased expiratory muscle strength was associated with reduced exercise tolerance and reduced quality of life. In addition to the expiratory muscle weakness, it recently has been shown11 that the endurance of the expiratory muscles is decreased in COPD patients. This decrease was related to the severity of air-flow obstruction and to the decrease in the strength of different muscle groups.

Expiratory muscle recruitment has been observed, under different circumstances, in patients with COPD.27 28 29 The mechanism and the results by which air-flow limitation is followed by expiratory muscle recruitment have not been completely clarified. Younes30 has pointed out that expiratory muscle contraction during expiration may be a nonspecific natural component of the response of the respiratory system to the increased respiratory stimulus. More recent data27 suggest that abdominal muscle recruitment during expiration allows the preservation of diaphragm muscle fiber length and the force-generating ability of the diaphragm at the onset of inspiratory muscle contraction, despite lung hyperinflation. It has been shown15 that training both the inspiratory and expiratory muscles by normocapnic hyperpnea results in improved exercise performance, health-related quality of life, and dyspnea in daily activities.

In the present study, it has been shown that the inspiratory and expiratory muscles can be specifically trained, with improvement of both muscle strength and endurance. The improvement in inspiratory muscle performance was associated with an increase in the 6-min walk test distance and in the sensation of dyspnea in daily activities. When the expiratory muscles were specifically trained, a significant increase in exercise performance also was shown. However, when SIMT and SEMT were combined, there was no additional benefit in the 6-min walk test distance and in the sensation of dyspnea, compared to SIMT alone. Therefore, SIMT seems to be the only ventilatory muscle training that is necessary to improve dyspnea and exercise performance in symptomatic COPD patients.


   Footnotes
 
Abbreviations: BDI = baseline dyspnea index; PEmax = maximal expiratory pressure; PEmpeak = peak expiratory pressure; PImax = maximal inspiratory pressure; PImpeak = peak inspiratory pressure; POD = perception of dyspnea; SEMT = specific expiratory muscle training; SIMT = specific inspiratory muscle training

Received for publication September 23, 2002. Accepted for publication May 19, 2003.


   References
TOP
 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
 References
 

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