ORIGINAL ARTICLE
Effect of inspiratory muscle training on exercise
performance and quality of life in patients with
chronic obstructive pulmonary disease
Ahmed Saad Elmorsi
a, Mohamad Elsayed Eldesoky
a,
Mona Ahmad Abdelwahab Mohsen
b, Nesrien Mohammad Shalaby
a,
Dina Abouelkheir Abdalla
a,*a
Chest Medicine Department, Faculty of Medicine, Mansoura University, Mansoura 35516, Egypt
b
Rheumatology and Rehabilitation Department, Faculty of Medicine, Mansoura University, Mansoura 35516, Egypt Received 6 July 2015; accepted 18 October 2015
Available online 23 November 2015
KEYWORDS COPD;
Exercise capacity;
Inspiratory muscle training; Peripheral muscle exercise training;
Quality of life
Abstract Background: Chronic obstructive pulmonary disease (COPD) is associated with skeletal muscle dysfunction. This study aimed to evaluate effectiveness of inspiratory muscle training (IMT) as a part of exercise training in COPD patients.
Methods: Sixty male patients were assigned to 3 groups; twenty in each group. In addition to medical treatment given for all patients; patients in group A received peripheral muscles exercise training plus IMT at an intensity that increased from 30% to 60% of their maximal inspiratory pressure (PImax). Patients in group B received peripheral muscle exercise training alone, and in
group C; they received no training. All patients underwent clinical evaluation, chest X-ray, electro-cardiogram, body mass index, and spirometry. Outcome measures in the form of respiratory muscle strength [PImax, maximal expiratory pressure (PEmax)], dyspnea, exercise performance (six minutes
walk test) and quality of life [BODE index and St. George’s Respiratory questionnaire for COPD patients (SGRQ-C)] were carried out at study entry, after 4 and 8 weeks.
Results: IMT plus peripheral muscle exercise training led to a significant improvement in PImax,
PEmax,and 6-min walking distance (6MWD) compared to peripheral muscle exercise training alone.
Both IMT plus peripheral muscle exercise training and peripheral muscle exercise training alone improved dyspnea, BODE index and SGRQ-C without significant differences between 2 groups.
Abbreviations:6MWD, 6-min walk distance; 6MWT, 6-min walk test; BMI, body mass index; COPD, chronic obstructive pulmonary disease; FEV1, forced expiratory volume in the first second; FVC, Forced vital capacity; GER, general exercise reconditioning; GOLD, Global Initiative for Chronic Obstructive Lung Disease; IMT, Inspiratory muscle training; LABD, long acting bronchodilators; MCID, minimal clinical important difference; mMRC, modified Medical Research Council; PEmax, maximal expiratory pressure; PImax, maximal inspiratory pressure; SGRQ-C, St
George’s Respiratory Questionnaire for COPD patients * Corresponding author. Tel.: +20 01009976012.
E-mail addresses: [email protected] (A.S. Elmorsi), [email protected] (M.E. Eldesoky), [email protected] (M.A.A. Mohsen),[email protected](N.M. Shalaby),[email protected],[email protected](D.A. Abdalla).
Peer review under responsibility of The Egyptian Society of Chest Diseases and Tuberculosis. H O S T E D BY
The Egyptian Society of Chest Diseases and Tuberculosis
Egyptian Journal of Chest Diseases and Tuberculosis
www.elsevier.com/locate/ejcdt www.sciencedirect.com
http://dx.doi.org/10.1016/j.ejcdt.2015.10.006
0422-7638Ó 2015 The Authors. Production and hosting by Elsevier B.V. on behalf of The Egyptian Society of Chest Diseases and Tuberculosis. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Conclusion: For PImax, PEmax,and 6MWD; IMT provides additional benefits to peripheral
mus-cle exercise training in COPD patients. However, this did not translate into additional improvement in dyspnea and quality of life compared with what is achieved by peripheral muscle exercise alone.
Ó 2015 The Authors. Production and hosting by Elsevier B.V. on behalf of The Egyptian Society of Chest Diseases and Tuberculosis. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction
Chronic obstructive pulmonary disease (COPD) is a multisys-tem disease affecting the skeletal muscle both peripheral and respiratory [1,2]. Weakness of respiratory muscle in COPD patients leads to hypercapnia, dyspnea, and decreased exercise capacity[3]. In COPD; inspiratory muscle training (IMT) as a monotherapy improves inspiratory muscle strength, exercise capacity, and decreases dyspnea[3,4]. However, the value of addition of IMT to a general exercise training program is still questionable[5,6]. The aim of this work was to evaluate the effectiveness of IMT as a part of exercise training program in patients with COPD.
Methods
This prospective comparative interventional study was carried out at Chest Medicine and Rheumatology and Rehabilitation Department; Mansoura University Hospital; Egypt. All sub-jects enrolled from October, 2011 to April, 2014. Ethics approval has been obtained from Medical Research Ethics Committee in July, 19th, 2011; Mansoura University. The pro-tocol for this work was published on ClinicalTrials.gov (iden-tifier: NCT02257463).
Ninety-four male patients between 45 and 65 years old with moderate to very severe COPD were recruited in this study. The severity was classified according to Global Initiative for Chronic Obstructive Lung Disease (GOLD) into stage II, III, and IV based on post bronchodilator forced expiratory volume in one second (FEV1) values in patients with FEV1/
forced vital capacity (FVC) < 0.70 [7]. In addition to theo-phylline, patients also received medications in the form of either inhaled long acting bronchodilators (LABD) or com-bined LABD and inhaled steroids according to GOLD recom-mendations [7]. All patients were exsmokers, had a stable clinical condition at the time of study and with low maximal inspiratory pressure (PImax) [<60 cm H2O][8]. Patients with
significant reversibility following bronchodilation defined as an increase in FEV1of more than 12% and 200 ml from the
pre-bronchodilator value[9], those with unstable cardiac dis-eases, uncontrolled hypertension, recent pneumothorax, recent abdominal or thoracic surgery, known progressive neuromus-cular disorders, advanced liver diseases, or renal impairment, known connective tissue diseases, or significant endocrinal abnormalities were excluded from the study.
While 34 patients dropped out from the study, 60 patients completed the study and were classified into 3 groups. Group A (study group) included 20 patients treated with pharmaco-logical therapy, peripheral muscle exercise training, and IMT. Group B (control positive group) included 20 patients treated with pharmacological therapy, peripheral muscle exercise training without IMT; and 20 patients were enrolled
into group C (control negative group). They were treated only with pharmacological therapy without any kind of pulmonary rehabilitation.
Patients in group A and group B were chosen randomly. Those with odd numbers were classified to be in group A while those with even numbers were classified to be in group B. For group C and to decrease the drop out ratio, patients from dis-tant localities who found difficulty in adherence with the study protocol from the start because of the economic state and transportation issues were classified in this group to ensure only one monthly visit. We also chose male patients as the dis-ease is not common in females in our locality, and to avoid gender-associated differences in the response to pulmonary rehabilitation.
All patients underwent baseline assessment including thor-ough history taking, clinical examination, plain chest X-ray, electrocardiogram, and body mass index (BMI). Patients were then evaluated before the study, after 4 and 8 weeks (except for reversibility after bronchodilators) using spirometry, respira-tory muscle strength device, six minute walk test (6MWT), dyspnea grading, BODE index, and St. George’s Respiratory questionnaire for COPD patients (SGRQ-C). Spirometry was performed to measure FEV1, FVC, FEV1/FVC ratio, and
reversibility after bronchodilators using smart pft lab, Medical Equipment Europe GmbH, Germany according to the stan-dardized protocol[10]. Respiratory muscle strength was evalu-ated using a handheld mouth pressure meter (Micro MPM; Micro Medical, UK) with measuring PImaxand maximal
expi-ratory pressure (PEmax) as previously described[11]. Six minute
walk test (6MWT) was conducted according to the procedures recommended by the American Thoracic Society[12]. Grading of dyspnea was performed using the modified Medical Research Council (mMRC) [13]. With recording BMI, the FEV1, mMRC dyspnea scale, and the six minutes walk
dis-tance (6MWD); BODE index was calculated [14]. Finally, assessment of quality of life using St. George’s Respiratory questionnaire for COPD patients (SGRQ-C) was done.[15]. Training protocol
1. Peripheral exercise trainingWe followed The Pulmonary Rehabilitation Toolkit on behalf of The Australian Lung Foundation[16]. The program was conducted following a schedule of 24 visits in the 8 week period. Patients in group A and group B were subjected to a combination of lower limb endurance training using treadmill walking, upper limb endurance training with a combination of arm raise and arms together, upper limb strength training using hand weights for biceps and triceps, and lower limb strength training using straight leg raise.
2. Inspiratory muscle training (IMT)All subjects in group A only were trained daily, six times a week; each session con-sisted of 30 min, for 2 months using a threshold inspiratory
muscle trainer (ThresholdÒ Inspiratory Muscle Trainer, Healthscan, New Jersey, NJ, USA). Patients started breath-ing at a resistance that required the generation of 30% of their PImaxfor one week. The load was then increased
incre-mentally, 5–10%, to reach a generation of 60% of their PImaxat the end of the first month. Specific IMT was then
continued at 60% of their PImaxadjusted weekly to the new
PImaxachieved.
Statistical analyses
The statistical analysis of data was done using SPSS program version 16.0. For mMRC dyspnea scale; data were expressed as median (minimum–maximum); non-parametric two-related-samples test (Wilcoxon type) was used to compare the results in the same group. Kruskal–Wallis H test was used to compare the results between the three groups; and
two-independent-samples tests (Mann–Whitney U type) were used to compare the results between the two groups. For data with normal distribution; descriptive statistics were used to cal-culate mean ± standard deviation (SD); paired sample t-test was used to compare the results in the same group. A one way ANOVA test was used to compare the results between the three groups; and post hoc Bonferroni test was used to compare the results between the two groups. Statistical signif-icance was defined as p value less than 0.05.
Results
Thirty-four patients dropped out of the study for the following reasons: acute exacerbation of COPD with hospitalization (n = 2), facial burn (n = 1), inability to perform training (n = 1), late diagnosis of knee osteoarthritis (n = 1), diabetic retinopathy (n = 1), economic and social problems (n = 6), or withdrawal from the study without known reasons
Table 1 Patients’ characteristics, and baseline spirometry.
Group A (n = 20) Group B (n = 20) Group C (n = 20) pvalue
Age (Years) (mean ± SD) 57.20 ± 5.08 55.70 ± 6.12 56.80 ± 4.95 0.664
Smoking index (P-Y) (mean ± SD) 55.60 ± 19.63 58.30 ± 28.79 44.95 ± 15.38 0.137
BMI (kg/m2) (mean ± SD) 24.98 ± 5.16 25.47 ± 4.90 27.61 ± 4.69 0.207 COPD group [N (%)] GOLD II 7 (35%) 5 (25%) 5 (25%) 0.773 GOLD III 7 (35%) 10 (50%) 11 (55%) GOLD IV 6 (30%) 5 (25%) 4 (20%) MVV (% predicted) (mean ± SD) 40.17 ± 10.96 39.42 ± 10.43 38.16 ± 8.86 0.817
Base line spirometry (mean ± SD)
FEV1(% predicted) 41.77 ± 17.76 38.04 ± 14.05 41.01 ± 12.17 0.704
FVC (% predicted) 65.22 ± 22.16 63.65 ± 17.98 60.51 ± 13.78 0.711
FEV1/FVC (%) 50.40 ± 9.85 48.35 ± 9.68 53.25 ± 8.60 0.262
P-Y: pack-year index; BMI: body mass index; COPD: chronic obstructive pulmonary disease; GOLD: Global Initiative for Chronic Obstructive Lung Disease; FEV1: forced expiratory volume in one second; FVC: forced vital capacity; MVV: maximal voluntary ventilation.
Table 2 Baseline values and changes in PImax, PEmaxand 6MWD at 4 and 8 weeks.
Baseline Week 4 Week 8 p*value p#value
PImax(cm H2O) Group A 51.05 ± 3.22 58.80 ± 3.89 70.75 ± 3.34,e 0.000 0.000 Group B 52.95 ± 4.73 59.00 ± 5.21 65.60 ± 5.09 0.000 0.000 Group C 51.50 ± 4.76 52.40 ± 4.76 53.20 ± 4.95 0.001 0.000 pvalue 0.351 0.000 0.000 PEmax(cm H2O) Group A 84.20 ± 7.67 94.30 ± 8.15 107.70 ± 10.28 0.000 0.000 Group B 87.50 ± 7.12 95.25 ± 8.15 105.60 ± 9.18 0.000 0.000 Group C 86.55 ± 8.42 87.60 ± 8.53 88.95 ± 8.66 0.000 0.000 pvalue 0.389 0.009 0.000 6MWD (m) Group A 296.65 ± 28.12 335.95 ± 29.24 387.20 ± 32.87 0.000 0.000 Group B 311.60 ± 46.18 337.20 ± 45.81 372.45 ± 45.37 0.000 0.000 Group C 289.25 ± 39.54 292.60 ± 44.07 300.70 ± 42.47 0.295 0.000 pvalue 0.186 0.001 0.000
PImax: maximal inspiratory pressure; PEmax:maximal expiratory pressure; 6MWD: 6-min walking distance; p value: p value between the groups;
p*value: p value within the group at 4 weeks in comparison to 0 week; p#
value: p value within the group at 8 weeks in comparison to 0 week; values are expressed as mean ± SD; number of patients in each group = 20.
Significant from group C. eSignificant from group B.
(n = 22). Sixty patients completed the study; twenty in each group. The general characteristics of patients are described in Table 1. The three groups were well-matched as regard age, smoking index, BMI, GOLD staging, and spirometric measures with no significant difference for any variable between groups.
There were no significant differences among the three groups at baseline for any of the outcomes (Tables 2, 4 and 5). PImax, PEmaxand 6MWD increased significantly in all groups
with significant differences between group A and group B compared to group C (Table 2). Also, there were significant differences between group A and group B in these 3 outcomes (Table 3).
The mMRC dyspnea scale (Table 4), BODE index and SGRQ-C total score (Table 5) improved significantly in group A and group B but not in group C, with no significant differ-ences between group A and group B in mMRC dyspnea scale (Table 4), BODE index and SGRQ-C total score (Tables 5). Discussion
In this study; PImaxshowed a statistically significant
improve-ment in all groups. However; there was a statistically signifi-cant improvement in group A in comparison to group B and group C. These findings were in agreement with previously published studies on patients with COPD who received com-bined IMT plus general exercise reconditioning (GER) versus patients who received GER alone [17,18]. In other studies; however; PImax improved only in patients that received
addi-tional IMT beside GER [19–22]. On the other hand; various studies on general exercise training alone in patients with COPD found improvement in PImaxafter training[23,24].
Addition of IMT to GER results in significant improve-ments in inspiratory muscle strength than GER alone. IMT is known to improve pulmonary oxygen uptake kinetics [5] Furthermore, Ramirez-Sarmiento et al. [25]found structural adaptations in external intercostal muscles following IMT in patients with COPD. Therefore; IMT seems to have specific physiological effects on respiratory muscles. General exercise training alone can also improve PImaxas during the course of
training; if the respiratory muscles become sufficiently over-loaded, substantial structural and functional adaptation will
Table 3 Median differences for PImax, PEmaxand 6MWD at 4 and 8 weeks.
Group A Group B Group C pvalue
PImaxmedian difference at 4 weeks 8 (5–11)e, 6 (4–8) 1 ( 1–3) 0.000
PImaxmedian difference at 8 weeks 20 (15–23)e, 13 (9–15) 1.5 (1–3) 0.000
PEmaxmedian difference at 4 weeks 10 (7–17)e
, 7.5 (4–13) 1 ( 1–3) 0.000
PEmaxmedian difference at 8 weeks 23 (16–38)e
, 19 (7–24) 2 (1–4) 0.000
6MWD median difference at 4 weeks 37 (28–66)e, 25 (13–38) 11 ( 24–18) 0.000
6MWD median difference at 8 weeks 89.5 (66–121)e, 61 (45–84) 10 ( 7–36) 0.000
Values are expressed as median (mim-max); number of patients in each group = 20.
Significant from group C. e Significant from group B.
Table 4 Baseline and changes in mMRC dyspnea scale at 4 and 8 weeks.
Baseline Week 4 Week 8 p*value p#value
Group A 3 (2–3) 2 (2–3) 1.5 (1–2) 0.001 0.000 Group B 3 (2–3) 2 (2–3) 2 (1–2) 0.002 0.000 Group C 3 (2–3) 3 (2–3) 3 (2–3) 0.317 0.317 pvalue 0.151 0.024 0.000
mMRC: modified Medical Research Council; p value: p value between the groups; p*value: p value within the group at 4 weeks in
comparison to 0 week; p#value: p value within the group at 8 weeks in comparison to 0 week; number of patients in each group = 20.
Significant from group C.
Table 5 Baseline and. changes in BODE index and SGRQ-C total score at 4 and 8 weeks.
Baseline Week 4 Week 8 p*value p#value
BODE index Group A 5.15 ± 1.57 4.30 ± 1.87 3.05 ± 1.61 0.000 0.000 Group B 5.20 ± 1.24 4.60 ± 1.31 3.50 ± 1.36 0.000 0.000 Group C 4.95 ± 1.28 5.05 ± 1.23 4.90 ± 1.25 0.330 0.577 pvalue 0.830 0.289 0.000 SGRQ-C total score GroupA 81.86 ± 10.05 65.22 ± 10.90 49.19 ± 10.72 0.000 0.000 Group B 80.69 ± 12.08 64.36 ± 11.62 52.99 ± 11.11 0.000 0.000 Group C 76.63 ± 10.08 78.11 ± 10.17 81.12 ± 8.49 0.174 0.000 pvalue 0.281 0.000 0.000
SGRQ-C: St. George’s Respiratory questionnaire for COPD patients; p value: p value between the groups; p*value: p value within the group at
4 weeks in comparison to 0 week; p#value: p value within the group at 8 weeks in comparison to 0 week; values are expressed as mean ± SD;
number of patients in each group = 20.
occur[26]. The difference in the effect of GER on PImaxamong
the studies may be explained by the difference in patients’ characteristics, number of patients involved in the studies, dif-ferent training protocol, or difdif-ferent training intensities.
We also noticed that the mean PImaxin group C increased
significantly (p < 0.001). This increase, however; did not translate into clinical improvement as regards dyspnea, 6MWD and quality of life. This could be attributed to the learning effect, theophylline, bronchodilator therapy or improved patients’ effort with repetition of the test.
PEmaxalso showed a statistically significant improvement in
group A and group B in comparison to group C with a signifi-cant difference in improvement between group A compared to group B. Most of the previous studies did not evaluate the effect of training on PEmax. O’Donnell et al.[23]showed a significant
increase in PEmaxin response to exercise despite they did not
use IMT in their protocol. On the other side, Larson et al.[21] did not demonstrate a change in PEmaxin their study in any of
the four studied groups (IMT alone, GER alone, combined IMT and GER, and health education). However; in that study; PImaxdid not also improve in the group that received general
exercise training only. These differences may be attributed to different populations studied, different protocols or intensities. In this study; 6MWD showed a statistically significant improvement in group A and group B compared to group C. Also; the improvement in 6MWD in group A was statistically significant from group B. These results were in agreement with many authors who found a significant increase in the group that received additional IMT beside GER [17–19]. On the other hand, our results were in disagreement with other authors who found a significant improvement in walking dis-tance in the group that received combined IMT and GER and in the group received GER alone with no statistically sig-nificant difference between the groups[27–29]. The difference in the results may be attributed to difference in training dura-tion, intensity, protocols among the studies, or patients’ char-acteristics. For example; Dekhuijzen and colleagues[17]beside using higher intensity for IMT (70% of patients’ PImax) and
longer duration (10 weeks); they also selected patients with ventilatory limitation that was defined by the authors as a nor-mal resting arterial partial pressure of carbon dioxide that rose during progressive exercise. This may indicate an insufficiency of the respiratory muscles to maintain adequate ventilation during the higher metabolic rate of exercise.
In group C, although the mean 6MWD increased signifi-cantly, it was not translated into clinical improvement in dys-pnea or quality of life as Holland et al. defined minimal clinical importance difference (MCID) of 25 m[30]. The improvement in this group may be due to optimization of pharmacotherapy during the study, or because patients acquired more confidence in performing the test.
In this study; mMRC dyspnea scale showed a statistically sig-nificant improvement in group A and group B but not in group C, with no statistically significant difference between group A and group B. While our results were in agreement with studies conducted by Larson et al.[21], Berry et al.[28], and Mador et al.[29]; however; Sykes and Hang[18], Magadle et al.[22], and Weiner et al.[31]found a significant decrease in the percep-tion of dyspnea in the combined IMT and GER group but not in the group that received GER alone. Again, this difference may be attributed to difference in training duration, intensity, proto-cols among the studies, or patients’ characteristics.
After training; oxidative capacity and skeletal muscle effi-ciency improve. This can lead to a reduction in ventilatory requirement for a given submaximal work rate; which by its turn may reduce dynamic hyperinflation, thereby adding to the reduction in exertional dyspnea[32,33]. Exercise programs can also result in desensitization to dyspnea through the antidepressant effect of exercise, social interaction, and dis-traction from dyspneic sensations that occur during exercise with a group of patients who have the same condition[34,35]. In this work, there was a statistically significant change in the BODE index at 4 and 8 weeks in group A and group B but not in the group C with no significant difference between group A and group B in the BODE index after 8 weeks. To our knowledge, studies that compared combined IMT and GER versus GER alone did not evaluate the changes in BODE index. However, some studies on pulmonary rehabilitation demonstrated the effect of rehabilitation on the BODE index. Cote and Celli[14]found an improvement in the BODE index of 19% in the group that received pulmonary rehabilitation. Many other studies found significant reductions in BODE index after training[36–39].
Cote and Celli[14]had defined a one unit change in the BODE index as clinically significant as a change in any of its components is important to influence clinical outcomes. They also found that the change in the BODE index after pulmonary rehabilitation provides valuable prognostic information. Bis-cione et al.[36]and Kosmas et al. [38]found that the BODE index could be a useful indicator of the quality of life.
In our study; SGRQ-C total score showed a statistically sig-nificant improvement in group A and group B but not in the group C with no statistically significant difference between group A and group B. This was in agreement with studies con-ducted by Dekhuijzen et al.[17]and Mador et al.[29]. How-ever, our results were in disagreement with Sykes and Hang [18]and Magadle et al.[22]who found a greater decrease in patients that received combined IMT and GER. This differ-ence may be explained by the differdiffer-ence in patient characteris-tics, number of patients involved in the study, different training protocol, or different training intensities.
In conclusion; IMT provides additional benefits to COPD patients undergoing peripheral muscle exercise training as regards respiratory muscle strength and exercise capacity. However, this improvement did not translate into additional improvement in dyspnea and quality of life compared with what is achieved by peripheral muscle exercise training alone. Further studies with different IMT intensities and longer dura-tion are recommended.
Conflict of interest
There is no conflict of interest to declare. References
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