Respiratory Muscle Endurance Training in Chronic
Obstructive Pulmonary Disease
Impact on Exercise Capacity, Dyspnea, and Quality of Life

Department of Internal Medicine, Triemli Hospital, Zurich, and Department of Exercise Physiology, Federal Institute of Technologyand University of Zurich, Switzerland Inspiratory muscle training may have beneficial effects in certain
which imitates most closely the load on the respiratory mus- patients with chronic obstructive pulmonary disease (COPD). Be-
cles during exercise, was considered difficult to apply on a cause of the lack of a home training device, normocapnic hyper-
large scale (14). In only one study was home-based training pnea has rarely been used as a training mode for patients with
applied in conjunction with a comprehensive rehabilitation COPD, and is generally considered unsuitable to large-scale appli-
cation. To study the effects of hyperpnea training, we randomized
As compared with resistive breathing through a fixed ori- 30 patients with COPD and ventilatory limitation to respiratory
fice (0.5 cm) at a breathing rate of 15 breaths/min, or TL with muscle training (RMT; n ϭ 15) with a new portable device or to
a threshold pressure of 30% of maximum inspiratory pressure breathing exercises with an incentive spirometer (controls; n ϭ
) at a breathing rate of 15 breaths/min, normocapnic hy- 15). Both groups trained twice daily for 15 min for 5 d per week for
perpnea at a target minute ventilation ( E 8 wk. Training-induced changes were significantly greater in the
mal voluntary ventilation (MVV) generates the greatest work RMT than in the control group for the following variables: respira-
of breathing (16). Prior work in subjects with COPD showed tory muscle endurance measured through sustained ventilation
ϩ825 Ϯ 170 s [mean Ϯ SEM] versus Ϫ27 Ϯ 61 s, p Ͻ 0.001), in-
that training with normocapnic hyperpnea improves respira- spiratory muscle endurance measured through incremental in-
tory muscle endurance and exercise performance (5, 15). The spiratory threshold loading (ϩ58 Ϯ 10 g versus ϩ21.7 Ϯ 9.5 g, p ϭ
effects of such training on dyspnea and quality of life, impor- 0.016), maximal expiratory pressure (ϩ20 Ϯ 7 cm H
tant outcome variables for patient compliance and well-being, 2O versus
0.009), 6-min walking distance ( 58 11 m versus
11 Ϯ 11 m, p ϭ 0.002), O
A recently developed training device allows respiratory 2.5 0.6 ml/kg/min versus
Ϫ0.3 Ϯ 0.9 ml/kg/min, p ϭ 0.015), and the SF-12 physical compo-
muscle training (RMT) with normocapnic hyperpnea at home.
nent score (ϩ9.9 Ϯ 2.7 versus ϩ1.8 Ϯ 2.4, p ϭ 0.03). Changes in
Studies with healthy subjects using this device resulted in in- dyspnea, maximal inspiratory pressure, treadmill endurance, and
creased cycling endurance (17) and decreased perceived respi- the SF-12 mental component score did not differ significantly be-
ratory exertion during exercise (18). On the basis of these re- tween the RMT and control groups. In conclusion, home-based
sults, we wanted to test the feasibility and effectiveness of respiratory muscle endurance training with the new device used in
home training with this device in a randomized, controlled this study is feasible and has beneficial effects in subjects with
study of subjects with COPD. The aim was not only to assess COPD and ventilatory limitation.
the effects on respiratory muscle and exercise performance,but also to include the important variables of dyspnea and Many patients with chronic obstructive pulmonary disease (COPD) are limited in their physical activity by dyspnea. Lunghyperinflation, increased deadspace ventilation, and increased energy consumption during hyperpnea lead to decreased ven-tilatory reserve and dyspnea on exertion (1, 2). Some subjects The study protocol was approved by the ethics committee of the Tri- with COPD show decreased maximal respiratory pressures (3, 4), which are indicative of respiratory muscle weakness and Subjects
which may contribute to the perception of dyspnea.
Some studies have shown that the respiratory muscles can Subjects were recruited from the outpatient clinic of the Pulmonary be trained if an adequate training stimulus is applied, and that Division of the Triemli Hospital. Consecutive patients were screenedby reviewing their charts and by interview. Those who met the inclu- exercise performance (5, 6) and dyspnea (6, 7) may improve as sion criteria, agreed to participate, and had signed the informed con- a result of such training. In most studies inspiratory muscle sent form were randomly assigned to an RMT group or a control training has been done with resistive breathing or threshold group, according to a computer-generated randomization table. Inclu- loading (TL) (6–11). Few patients have been trained with nor- sion criteria were chronic airflow obstruction (FEV Ͻ mocapnic hyperpnea (5, 12, 13) because the complicated equipment needed to prevent hypocapnia has usually required after bronchodilatation with 200 ␮g of albuterol inhaled from a pres- a hospital facility or research laboratory, and has not been surized metered-dose inhaler with a spacer), an age of 20 to 80 yr, and available for home training. Therefore, this training mode, a stable clinical condition for at least 1 mo. The patients’ physical ac-tivity had to be limited by pulmonary dyspnea only. In case of anypossibility that cardiac disease limited physical performance, patients (Received in original form on December 7, 1999 and in revised form on May 4, 2000) underwent cardiopulmonary exercise testing and echocardiography Correspondence and requests for reprints should be addressed to Thomas A.
before inclusion in the study. Patients with dyspnea at rest, cardiac Scherer, M.D., LungenZentrum Hirslanden, Witellikerstrasse 36, 8008 Zurich, disease, poor compliance, drug or alcohol abuse, pregnancy or lacta- Switzerland E-mail: thsche@swissonline.ch tion, a requirement for supplemental oxygen, CO2 retention, or use of Supported by grants from Astra Pharmaceutica, Dietikon, and Merck Sharpe and any mechanical ventilatory support were excluded.
Dohme-Chibret, and Rhône-Poulenc Rorer.
Forty-nine patients were initially screened for the study. Ten pa- Am J Respir Crit Care Med
Vol 162. pp 1709–1714, 2000
tients refused to participate and five met one or more exclusion crite- Internet address: www.atsjournals.org
ria. Thirty-four subjects were initially included. One patient assigned AMERICAN JOURNAL OF RESPIRATORY AND CRITICAL CARE MEDICINE to RMT withdrew during the initial testing and one control subject ratory pressures (PImax and PEmax) measured at the mouth, and were withdrew during Week 2 of the study. One patient in the RMT and given a dyspnea questionnaire (baseline or transition dyspnea index), one in the control group had to be excluded after traumatic hip and 6-min walking test, 20-min rest period, respiratory muscle endurance rib fractures. Thirty subjects completed the study.
test (sustained ventilation), and health questionnaire, and underwent Baseline characteristics of the study population are outlined in Ta- measurement of peak oxygen consumption ( O ble 1. The age range of the study population was 46 to 80 yr. No signif- rest period, testing of inspiratory muscle endurance (TL), a third 20- icant differences existed between the two study groups. During the min rest period, and an endurance test on a treadmill.
study, subjects in the RMT group experienced 1.1 Ϯ 0.2 (mean Ϯ Day 2. On Day 2 of the study the subjects had a 6-min walking test, SEM) intercurrent illnesses, had 1.1 Ϯ 0.2 medication changes, and 20-min rest period, inspiratory muscle endurance test (TL), 20-min had 1.3 Ϯ 0.5 missed training days per patient, versus 1.0 Ϯ 0.2 inter- rest period, 6-min walking test, 20-min rest period, and second in- current illnesses, 1.1 Ϯ 0.2 medication changes, and 0.7 Ϯ 0.3 missed spiratory muscle endurance test (TL).
training days per patient, respectively, in the control group (no signif-icant differences existed between the RMT and control groups in Pulmonary function tests were done according to American Tho- racic Society criteria (19, 20), with measurement of slow VC, tidal vol-ume (VT), FVC, FEV1, peak expiratory flow (PEF), and 12-s MVV, Study Protocol
with the Medical Graphics CPX/D System (Medical Graphics Corpo-ration, St. Paul, MN). Reference normal values were taken from the All tests were performed in a standardized manner and sequence be- European Community for Steel and Coal (21).
fore starting the training and 1 wk after its completion. Care was given were measured from RV and TLC, respectively, with that subjects were familiarized with the different tests and devices used.
a handheld device (Micro M.P.M.; Micro Medical Ltd., Rochester, UK) Throughout the study period, subjects documented their training, their that has a built-in small air leak to prevent pressure generation by glottis pulmonary and other physical symptoms, physical activity, and any closure. The highest pressure from among 10 measurements was re- medication change in a diary, which, in addition to interviews of the corded. Reference normal values were taken from Black and Hyatt (22).
subjects and evaluation of their training progress, served as a control Endurance of the respiratory muscles was measured in two ways, for compliance with the training program. The study was conducted in a single-blind manner (i.e., subjects of both groups were told that theywere undergoing respiratory muscle training, and that two different de- 1. With the respiratory muscle endurance test to assess performance of vices for this were being compared). The subjects in one group were the inspiratory and expiratory muscles. This test was based on the not informed about the device or training of the other group.
12-s MVV, which was performed three times. The highest MVV was recorded. Respiratory muscle endurance was measured as sustainedventilation at 66% of each subject’s highest MVV. The time during which subjects were able to sustain this target ventilation was re- Day 1. On Day 1 of the study, subjects were given pulmonary func- corded. If a subject surpassed 15 min of breathing at this level, the tion tests (PFTs), had their 12-s MVV, maximal inspiratory and expi- test was repeated on the following day at 75% of MVV. Subjectswere not coached and breathing was not paced. To assure nor-mocapnia, the training device (described subsequently), connectedto the metabolic cart (CPX/D system; Medical Graphics), was used.
ide pressure (PETCO ), and Sa (Minolta Pulsox 5; Minolta Switzer- RESPIRATORY MUSCLE TRAINING AND CONTROL GROUPS
land, Dietikon, Switzerland) were measured continuously.
2. With the inspiratory muscle endurance test to assess performance of the inspiratory muscles. This test was done with an inspiratory TL device built according to the specifications of Nickerson and Keens (23). The inspiratory threshold pressure was varied with weights that were attached to a plunger, which closed the inspira- tory valve. The initial threshold pressure was set to about 20% of PImax. The weight was increased every 2 min by 50% of the initial weight until the subject was unable to continue breathing. The greatest weight the subject was able to sustain for at least 1 min was taken as the measure for inspiratory muscle endurance. The test was performed three times, and the greatest weight the subject en- dured was recorded. Results were compared with normal reference values established by Johnson and coworkers (24).
Exercise performance was tested with a 6-min walking test and a treadmill endurance test. The 6-min walking test was performed in a corridor of 90 m length. The subjects were instructed to cover as much distance as possible during 6 min. They were not verbally coached, but a person was walking about 1 m behind them. The test was re- peated three times, and the longest distance walked was recorded.
Results were compared with normal reference values established by Troosters and coworkers in healthy elderly subjects (25).
The endurance test on the treadmill was performed at a submaxi- mal workload (see the subsequent discussion), and subjects were not encouraged during this test. To determine the level of the submaximal workload used in the test, peak power output and O Definition of abbreviations: BDI ϭ Baseline Dyspnea Index; BMI ϭ body mass index; MVV ϭ 12-s maximal voluntary ventilation; PE sured with an incremental treadmill test by first gradually adjusting maximal inspiratory pressure; PEF ϭ peak expiratory flow; RET ϭ respiratory muscle en- the treadmill speed until the subject walked comfortably. The inclina- durance measured as sustained ventilation; RMT ϭ respiratory muscle training; SF-12 P ϭ tion of the treadmill was then increased by 2.5% in 2-min intervals un- score on physical component of the SF-12 health questionnaire; SF-12 M ϭ score on til the subject was exhausted. Normal reference values for O mental component of the SF-12 questionnaire; TL ϭ inspiratory muscle endurance were taken from Hansen and coworkers (26). To determine treadmill measuring with threshold loading device; TM ϭ endurance on treadmill; E endurance, the treadmill was set to 80% of the inclination and to Scherer, Spengler, Owassapian, et al.: Respiratory Muscle Training V 2peak speed was reduced by 20%. The test cises. This was done by connecting the training device to the meta- was terminated when subjects indicated that they were exhausted and bolic cart and attaching a pulse oximeter to the subject’s finger. Dur- unable to keep up with the speed of the treadmill. The time during ing these weekly control sessions, breathing frequency was increased which a subject was able to walk at the preset load was recorded as reach a maximal training stimulus. Three subjects complained of dys- Before training, dyspnea in daily activities was assessed with pnea or dizziness during training. They were immediately called to the Mahler’s Baseline Dyspnea Index, and the change after training was laboratory to monitor training instrument settings, SaO , and PET assessed with Mahler’s Transition Dyspnea Index (TDI) (27, 28).
In the cases of two patients, settings had to be adjusted to correct for Health-related quality of life was tested with the SF-12 health ques- tionnaire (acute form), issued by the Medical Outcomes Trust (Bos- The mean respiratory rate (RR) increased by 29% during the ton, MA), which consists of a physical (SF-12 P) and a mental compo- training period (p Ͻ 0.001; Week 1: 26.3 Ϯ 1.0 breaths/min; Week 2: nent (SF-12 M) score. Because both questionnaires were originally 28.6 Ϯ 1.5 breaths/min; Week 3: 29.1 Ϯ 1.2 breaths/min; Week 4: 30.9 Ϯ written in English, three persons fluent in English translated the ques- 1.5 breaths/min; Week 6: 32.6 Ϯ 1.8 breaths/min; Week 7: 33.5 Ϯ 2.1 tionnaires independently into German, and one bilingual person breaths/min; and Week 8: 33.9 Ϯ 2.0 breaths/min). T translated the German versions back into English. All translations significantly during training (1.07 Ϯ 0.06 L at start of the training ver- were compared, discussed, and adjusted to the most correct version.
sus 1.12 Ϯ 0.05 L at the end; p ϭ 0.50).
Breathing Exercises in the Control Group
Respiratory muscle endurance training was done with a device that Subjects in the control group were told that they were engaging in res- we developed, consisting of tubing (I.D. ϭ 19 mm) that connects a re- piratory muscle training with an incentive spirometer (COACH 2 breathing bag with a mouthpiece in a 90-degree angle. A sideport (of Volumetric Incentive Spirometer; DHD Healthcare, Canastota, NY).
the same diameter as the tube) is inserted in the middle of this con- This device was chosen for the sham training to give the subjects the necting piece. This sideport contains a 6-mm hole that allows inspira- impression that they were undergoing training. Because airflow resis- tion from and expiration to fresh air, and also contains a valve. Sub- tance through this device is minimal, and the RR during breathing ex- jects fill and empty the rebreathing bag completely during inspiration ercises was kept at about 6 to 8 breaths/min, we assumed that no train- and expiration, while also inhaling additional fresh air through the ing effect would result. The target inspiratory VT was set to 70% of sideport during inspiration and breathing partly out through the side- each subject’s VC. Subjects were instructed to breathe in slowly after port during expiration. To assure a constant VT, the valve inserted in a deep exhalation at a rate of 6 to 8 breaths/min, but their breathing the sideport closes when subjects have emptied the bag during inspi- was not paced. The exercises were performed twice daily for 15 min ration. In our study the size of the bag was adjusted to 50 to 60% of on 5 d per week for 8 wk. Splitting the exercises into 5-min sessions the subject’s VC, and the breathing frequency chosen was such that was allowed if the subject was unable to train for 15 min without inter- V corresponded to 60% of MVV (monitored while the training de- ruption. The subjects also had weekly control sessions of their breath- vice was connected to the metabolic cart). Correct performance was ing exercises without a change in VT or breathing rate.
checked by analyzing PETCO with the metabolic cart and Sa with the Subjects in both the RMT and control groups who experienced pulse oximeter. If PETCO deviated from normal baseline values during acute breathing problems (e.g., due to an exacerbation of their the 10- to 15-min trial run, VT was adjusted by changing the size of the COPD) were allowed to stop training for a maximum of 14 d. These rebreathing bag and breathing frequency was changed accordingly subjects resumed their training from the same point at which they had V at 60% of MVV. Values of training PETCO ranged from stopped, in order to complete 40 training days.
33.1 Ϯ 1.1 mm Hg to 38.5 Ϯ 1.3 mm Hg. Hypocapnia during trainingwas corrected by increasing the size of the rebreathing bag, and hy- Statistics
percapnia was corrected by decreasing the size of the bag. Hypoxemia The results of the study are presented as mean Ϯ SEM. Because the values were not normally distributed (normality of distribution was While performing the breathing exercises, subjects wore a nose tested with the Shapiro–Wille’s test), the nonparametric Mann–Whit- clip to ensure breathing exclusively through the training device. The ney U test was used to compare baseline characteristics and training- exercises were performed twice daily for 15 min on 5 d per week for related changes in the RMT and control groups, Wilcoxon’s matched 8 wk. Splitting the exercise into 5-min sessions was allowed if the sub- pairs test was used to assess training-induced changes within a partic- ject was unable to train for 15 min without interruption. Inspiration ular group, and Friedman’s analysis of variance with Kendall’s con- and expiration were paced by an electronic metronome (Seiko Digital cordance was used to assess weekly changes over the course of the Metronome; Seiko Corp., Tokyo, Japan).
training. A value of p Ͻ 0.05 was considered significant. The Statistica Before the 8-wk training period and once every week during the for Windows software program (Statsoft Inc., Tulsa, OK) was used for , breathing rate, and VT were monitored in the all calculations. To achieve a difference in change in respiratory mus- pulmonary laboratory while subjects performed the breathing exer- cle endurance of 20% with an SD of 50 s and a statistical power of80%, it was calculated that 12 to 15 patients had to be included in eachstudy group. The primary endpoint of the study was respiratory mus- cle endurance; secondary endpoints were respiratory muscle strength,exercise performance, dyspnea, and health-related quality of life.
Training-related changes in the RMT as compared with the control group are shown in Table 2 and Figures 1 through 6.
Figure 1. Change in respiratory
muscle endurance (RET), mea-sured as time of sustained ventila- Definition of abbreviations: ⌬FEV1 ϭ change in forced expiratory volume in 1 s; ⌬FVC ϭ change in FVC; ⌬PEmax ϭ change in maximal expiratory pressure; ⌬PImax ϭ change in maximal inspiratory pressure; ⌬PEF ϭ change in peak expiratory flow; RMT ϭ respira- tory muscle training; ⌬SF-12 M ϭ change in score on mental component of the SF-12 V 2peak ϭ change in maximal oxygen consumption.
muscle endurance, measured with
Figure 4. Change in score of the
Improvement in respiratory muscle endurance measured as Keens and coworkers (12) found an increase from 74 to 109 L/ sustained ventilation (RMT group at 69 Ϯ 7% of MVV; con- min (ϩ47%), and Levine and coworkers (13) found an in- trol group at 70 Ϯ 5% of MVV) (Figure 1), and assessed with crease from 56 to 79 L/min (ϩ41%) in MSVC. We are aware incremental TL (Figure 2), was significantly greater in the of only one study that evaluated home-based training (15).
RMT group. Likewise, change in PEmax (but not in PImax), in- The investigators in this study achieved an increase from 34 to crease in 6-min walking distance (Figure 3), O physical (Figure 4) (but not the mental) component of the SF-12 Subjects in the present study also increased their exercise health survey were significantly greater in the RMT than in performance as a result of RMT. Their 6-min walking dis- the control group. Both groups showed a decrease in dyspnea in daily activities, but the difference was not significant (Fig- changes were significantly larger in the RMT than in the con- ure 5). Likewise, the change in treadmill endurance did not trol group. The 58-m increase in 6-min walking distance in the differ significantly between the two groups (Figure 6).
RMT group was large enough to be considered clinically rele-vant (29). Belman and Mittman (5) reported comparable re- DISCUSSION
sults. A 6-wk period of training increased the 12-min walking Our results in subjects with COPD and ventilatory limitation distance from 1,058 m to 1,188 m (ϩ12%). Ries and Moser show that home-based RMT with normocapnic hyperpnea im- (15), who applied home-based respiratory muscle endurance proved respiratory muscle endurance, exercise performance, training in conjunction with pulmonary rehabilitation, ob- health-related quality of life, and dyspnea in daily activities, whereas pulmonary function did not change significantly.
min to 16.4 ml/kg/min (ϩ9%), and in 12-min walking distance, Baseline characteristics, incidences of intercurrent illnesses, from 943 m to 1,020 m (ϩ8%), which are also in the range of and medication changes were comparable in the RMT and our training-induced changes. Although the training-related increase in treadmill endurance was considerably greater in The inclusion criteria for the study were directed to chronic the RMT group in our study, the changes did not differ signifi- airflow limitation and limitation in physical activity by pulmo- cantly between the two study groups. One reason for this in- nary dyspnea. Respiratory muscle weakness and/or ventila- significant difference may be that the individual improve- tory limitation of physical activity were not prerequisites to ments varied widely. The sample size was too small to reliably study inclusion. Analysis of our data show, however, that ven- exclude a difference in treadmill endurance, and a type II er- tilatory limitation, reflected by high ventilation at MVV of 85%), was clearly present. As compared with a The increased exercise performance with RMT is impor- healthy control population, our study subjects also had some tant for patients with COPD, since it may help in their daily weakness of their respiratory muscles, as expressed by their activities. It is unclear, however, how this translates into an improvement in dyspnea and quality of life, which are impor- Imax, MVV, and TL. These findings probably had an ef- fect on our results, and support the view that subjects with tant parameters (30, 31). Without subjective benefits, patients COPD, respiratory muscle weakness, and ventilatory limita- will hardly be willing to engage in daily training of their respi- ratory muscles. We therefore included the SF-12 Health Sur- The hyperpnea training in our study was usually well toler- vey and Mahler’s dyspnea indices in our study. The SF-12 ated. Only three patients called because they experienced ad- Health Survey is a 12-item questionnaire that closely mirrors verse effects, and their problems were readily solved.
the scores of the SF-36 short-form Health Survey (32), and In RMT, the increase in respiratory muscle endurance, which had proved to reflect health status in patients with measured as sustained ventilation, was large (258%). Previous chronic lung disease (33). The significant impact of RMT on studies, using normocapnic hyperpnea as a training mode in the physical component of the SF-12 health questionnaire is subjects with COPD, had already demonstrated the beneficial an important finding, because the effect of hyperpnea training effects of this training mode on respiratory muscle endurance.
on quality of life has not yet been tested. It is already known Using maximal sustained ventilatory capacity (MSVC) as a that pulmonary rehabilitation with and without additional in- measure of respiratory muscle endurance, Belman and Mitt- spiratory muscle training can improve quality of life in pa- man (5) reported an increase from 32 to 42 L/min (ϩ31%), tients with COPD (34–36); however, the effect of RMT with-out additional intervention is unknown.
Figure 3. Change in 6-min walking
Figure 5. Change in Transition
durance training group; C ϭcontrol group.
Scherer, Spengler, Owassapian, et al.: Respiratory Muscle Training (38–40). Currently, it is recommended that ventilatory muscletraining be considered within a pulmonary rehabilitation pro- Figure 6. Change in treadmill
gram only for selected patients with decreased ventilatory In summary, the results of the present study show that res- piratory muscle endurance training with normocapnic hyper-pnea improves respiratory muscle and exercise performance,health-related quality of life, and dyspnea. The new portabletraining device used in the study makes home-based endur-ance training with normocapnic hyperpnea feasible, and al- The TDI of 4.7 in our RMT group represents a distinct im- provement in dyspnea. Lisboa and coworkers (6) reportedcomparable results after TL training at 30% of PImax. Their References
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Zagazig University Faculty of Science Department of Geology AN INTEGRATED STUDY OF POTENTIAL AND SEISMIC METHODS ON SOUTH SITRA AREA, WESTERN DESERT, EGYPT. To the Department of Geology, Faculty of Science, Supervisors Late Prof. Dr. M. A. Shabaan Prof. Dr. Ali Ali El-Khadragy Prof. Dr. Salah Shebl Saleh Dr. Mohamed Housein Saad Zagazig University Facu


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