Skip to main content
 

Main menu

  • Home
  • Content
    • Current Issue
    • Editor's Commentary
    • Archives
    • Most-Read Papers of 2022
  • Authors
    • Author Guidelines
    • Submit a Manuscript
  • Reviewers
    • Reviewer Information
    • Create Reviewer Account
    • Reviewer Guidelines: Original Research
    • Reviewer Guidelines: Reviews
    • Appreciation of Reviewers
  • CRCE
    • Through the Journal
    • JournalCasts
    • AARC University
    • PowerPoint Template
  • Open Forum
    • 2023 Call for Abstracts
    • 2022 Abstracts
    • Previous Open Forums
  • Podcast
    • English
    • Español
    • Portugûes
    • 国语
  • Videos
    • Video Abstracts
    • Author Interviews
    • Highlighted Articles
    • The Journal

User menu

  • Subscribe
  • My alerts
  • Log in

Search

  • Advanced search
American Association for Respiratory Care
  • Subscribe
  • My alerts
  • Log in
American Association for Respiratory Care

Advanced Search

  • Home
  • Content
    • Current Issue
    • Editor's Commentary
    • Archives
    • Most-Read Papers of 2022
  • Authors
    • Author Guidelines
    • Submit a Manuscript
  • Reviewers
    • Reviewer Information
    • Create Reviewer Account
    • Reviewer Guidelines: Original Research
    • Reviewer Guidelines: Reviews
    • Appreciation of Reviewers
  • CRCE
    • Through the Journal
    • JournalCasts
    • AARC University
    • PowerPoint Template
  • Open Forum
    • 2023 Call for Abstracts
    • 2022 Abstracts
    • Previous Open Forums
  • Podcast
    • English
    • Español
    • Portugûes
    • 国语
  • Videos
    • Video Abstracts
    • Author Interviews
    • Highlighted Articles
    • The Journal
  • Twitter
  • Facebook
  • YouTube
Review ArticleSystematic Review

Inspiratory Muscle Training in COPD

Renata I N Figueiredo, Aline M Azambuja, Felipe V Cureau and Graciele Sbruzzi
Respiratory Care August 2020, 65 (8) 1189-1201; DOI: https://doi.org/10.4187/respcare.07098
Renata I N Figueiredo
Postgraduate Program in Pneumological Sciences, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil.
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Aline M Azambuja
Postgraduate Program in Pneumological Sciences, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil.
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Felipe V Cureau
Postgraduate Program in Endocrinology, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil.
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Graciele Sbruzzi
Postgraduate Program in Pneumological Sciences, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil.
Hospital de Clínicas de Porto Alegre, Porto Alegre, Brazil.
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: [email protected]
  • Article
  • Figures & Data
  • Info & Metrics
  • References
  • PDF
Loading

Abstract

BACKGROUND: The benefits of inspiratory muscle training (IMT) for patients with COPD are documented in the literature, but its isolated effect or association with other interventions, the best training methods, and what type of patient benefits the most are not clear. We sought to assess the effects of IMT on respiratory muscle strength, pulmonary function, dyspnea, functional capacity, and quality of life for subjects with COPD, considering IMT isolated or association with other interventions, presence of inspiratory muscle weakness, training load, and intervention time.

METHODS: We searched the MEDLINE, EMBASE, PEDro, Cochrane CENTRAL, and LILACS databases in June 2018. We also performed a manual search of references in the studies found in the database search and included in this analysis. We included randomized controlled trials that investigated the above-mentioned outcomes and assessed IMT, either isolated or associated with other interventions, in comparison with a control group, placebo, or other interventions, in subjects with COPD. We used the GRADE approach to evaluate the quality of the evidence.

RESULTS: Of 1,230 search results, 48 were included (N = 1,996 subjects). Isolated IMT increased PImax (10.64 cm H2O, 95% CI 7.61–13.66), distance walked in 6-min-walk test (34.28 m; 95% CI 29.43–39.14), and FEV1 (0.08, 95% CI 0.02–0.13). However, there was no improvement in dyspnea and quality of life. The presence of inspiratory muscle weakness did not change the results; higher loads (60–80% of PImax) promoted a greater improvement in these outcomes, and a shorter intervention time (4 weeks) improved PImax, but longer intervention times (6–8 weeks) are required to improve functional capacity. IMT associated with other interventions only showed an increase in PImax (8.44 cm H2O; 95% CI 4.98–11.91), and the presence of inspiratory muscle weakness did not change this result.

CONCLUSIONS: Isolated IMT improved inspiratory muscle strength, functional capacity, and pulmonary function, without changing dyspnea and quality of life. Associated IMT only increased inspiratory muscle strength. These results indicate that isolated IMT can be considered as an adjuvant intervention in patients with COPD.

  • breathing exercises
  • COPD
  • dyspnea
  • physical capacity
  • respiratory muscle training

Introduction

COPD is one of the major causes of chronic morbidity and mortality worldwide.1 Prognosis of patients with COPD is influenced by the severity and recurrence of exacerbation, with yearly mortality rates of 11% for patients who need hospitalization, 5–50% for patients on mechanical ventilation, and rising as high as 37% in case of hospitalization for exacerbation recurrence.2 Strategies are required that aim to reduce the disease progression and thus improve patients’ prognosis as well as reduce costs of health care and the global and socioeconomic burden of the disease.3

Individuals with COPD present with limitations in exercise capacity due to multiple factors, including ventilation, gas exchange, cardiovascular disease,4 and abnormalities in peripheral muscles.5 Inspiratory muscle dysfunction also occurs in these patients and is associated with dyspnea and reduced exercise capacity.6,7 Thus, pulmonary rehabilitation is recommended as an efficient intervention in cardiorespiratory management, generating improvements in exercise performance, with reductions in dyspnea in patients with different degrees of disease severity.8 As a pulmonary rehabilitation strategy, inspiratory muscle training (IMT) optimizes lung capacity and, consequently, improves physical conditioning.9

Gosselink et al10 conducted a systematic review with meta-analysis, including 32 randomized controlled trials (RCTs) on IMT effects in subjects with COPD. The authors made general and subgroup analyses with regard to training modality (strength of resistance and if pulmonary rehabilitation was added) and subject characteristics. The authors concluded that IMT improves inspiratory muscle strength, functional capacity, dyspnea, and quality of life. In subjects with inspiratory muscle weakness, inclusion of IMT in pulmonary rehabilitation programs improved inspiratory muscle strength and tended to improve exercise performance.10

Recently, Beaumont et al11 published a new systematic review on the subject. The authors reviewed 43 studies (37 meta-analyses), including RCTs, nonrandomized controlled trials, and observational studies published until 2017, and they noted the effects of IMT when isolated or associated with pulmonary rehabilitation, considering the presence of respiratory muscle weakness. They observed that IMT improved inspiratory muscle strength, quality of life, exercise capacity, and dyspnea, although there was no additional effect on pulmonary rehabilitation. According to the authors, the presence of respiratory muscle weakness seemed not to affect results, although they suggest further investigations of this intervention regarding dyspnea and quality of life.

Based on the results reported by Gosselink et al10 and Beaumont et al,11 a new systematic review including only RCTs and approaching important clinical issues for this type of training and this type of population is necessary. This systematic review will assess IMT effects on respiratory muscle strength, pulmonary function, dyspnea, functional capacity, and quality of life in patients with COPD, considering 4 factors: (1) IMT isolated or associated to other interventions; (2) the presence of inspiratory muscle weakness; (3) training load; and (4) intervention time.

Methods

This systematic review and meta-analysis followed recommendations proposed by the Cochrane Collaboration12 and the PRISMA Statement.13 The study protocol was registered in PROSPERO (CRD42017080337).

Eligibility Criteria

We included RCTs that assessed the effect of IMT, whether isolated or associated with other interventions, that compared treated subjects with a control group (ie, no intervention), placebo, or other intervention (eg, pulmonary rehabilitation, exercise, breathing exercises, or usual care); subject criteria included a diagnosis of COPD by spirometry, consistent with the GOLD criteria (FEV1/FVC < 70%), during both exacerbation and out-patient clinic care. The following outcomes were considered: respiratory muscle strength, pulmonary function, functional capacity, dyspnea, and quality of life. Studies with incomplete data or lacking data description were excluded.

Search Strategy

We searched the following electronic databases: MEDLINE (accessed via PubMed), EMBASE, Cochrane CENTRAL, PEDro, and LILACS. A manual search was also conducted in references of studies already published on the subject. The research terms used individually or combined include “pulmonary disease, chronic obstructive” (MeSH and entry terms) and “breathing exercises” (MeSH and entry terms) associated with a list of sensitive terms for searches of RCTs as prepared by Robinson and Dickersin.14 There were no restrictions as to year and language. The search occurred in June 2018. The full search strategy used for PubMed can be seen in supplementary materials at http://www.rcjournal.com.

Selection of Studies and Data Extraction

The titles and abstracts of all papers identified with the search strategy were independently assessed by 2 reviewers with a checklist containing inclusion and exclusion criteria. Studies that did not meet the eligibility criteria were excluded, and those that met the criteria or raised questions were selected for assessment of the whole text. The same independent reviewers assessed and selected these articles. Disagreements between reviewers were resolved by consensus. When the studies did not present the data required for meta-analysis, the corresponding author was contacted. In cases when the data were not available, the paper was excluded from the study. Data were extracted through a standardized form containing information on the methodological characteristics of the studies, subjects, interventions, and outcomes. The outcomes extracted were: respiratory muscle strength (ie, maximum inspiratory pressure [PImax] and maximum expiratory pressure), pulmonary function, (FVC, vital capacity, and FEV1), functional capacity (ie, distance walked in the 6-min-walk test [6MWT] and maximum oxygen consumption [Embedded Image ]), dyspnea (Borg scale), and quality of life (St George Respiratory Questionnaire score).

Risk of Bias Assessment

The risk of bias was assessed independently by 2 reviewers using the Cochrane Collaboration tool, considering the following characteristics for all included studies: generation of appropriate sequence, allocation concealment, patient and therapist blinding, description of losses and exclusions, and analysis of intention to treat. Studies without clear descriptions of these items were considered not clear or not informed.

Data Analysis

The meta-analysis was conducted using the random-effects model, and the effect size used was the mean difference, determined by the difference between the means at the baseline moment and at the end of the study for each group. These data were expressed as weighted mean differences among groups and standard deviation of the difference.13 A 95% CI was considered statistically significant. Statistical homogeneity across studies was assessed using the inconsistency test (I2), where values > 25% and > 50% were considered to indicate moderate and high heterogeneity, respectively.15 All analyses were made using Review Manager 5.3 (Cochrane Collaboration) and Stata 14 (StataCorp, College Station, Texas). Heterogeneity across studies was explored with 2 strategies: (1) executing the meta-analysis again, removing 1 paper at a time to check whether any individual study explained heterogeneity; (2) sensitivity analyses to assess sub-groups of studies with higher probability of producing valid intervention estimates, based on relevant prespecified clinical information that influence IMT effects on results (eg, association of interventions with IMT, intervention duration, inspiratory load, and whether the studies included patients with inspiratory muscle weakness, denoted as PImax < 60 cm H2O). In addition, meta-regression analyses were performed for outcome with high number of studies included (ie, PImax and 6MWT) and including main covariates (ie, inspiratory load, intervention duration, and weakness).

Summary of Evidence: GRADE Criteria

The quality of the evidence was assessed using the GRADE approach, as recommended by the Cochrane Handbook for Systematic Reviews of Interventions (Internet tool available at https://gradepro.org).12 For each outcome, the quality of the evidence was based on 5 factors: risk of bias; inconsistency; indirectness; imprecision; and potential for publishing bias. Quality was reduced by one level for each factor not met. The GRADE approach resulted in 4 levels of evidence quality: high, moderate, low, and very low.16

Results

Description of the Studies

The search strategy resulted in 1,230 abstracts, of which 112 were considered potentially relevant and were selected for detailed analysis. A total of 48 studies met the eligibility criteria and were included in the systematic review and in the meta-analysis (N = 1,996 subjects) (Fig. 1); 39 studies (n = 943 subjects) only assessed isolated IMT.17-55 Of these, 25 studies (n = 631 subjects) included subjects with respiratory muscle weakness.17-19,22-28,31-34,37,38,40,41,43,45-49,52 Various loads for IMT were 15% of PImax,42,46,48 30% of PImax,17,28,31,33,38,40,43,51 load progression of 5–35% of PImax,23,24 load progression up to 40–50% of PImax,21,39,53 load progression up to 60% of PImax,18,20,22,24-28,30,34,37,45,47,49,50,52,54-56 70% of PImax,44 and 80% of PImax.36 Belman et al19 and Oh35 used PFLEX equipment, and the load used for IMT was not clear. Leelarungrayub et al32 used Portex equipment, and load/resistance was set by the tube diameter (ie, 6 mm, 4 mm, and 2 mm) (can be seen in supplementary materials at http://www.rcjournal.com).

Fig. 1.
  • Download figure
  • Open in new tab
  • Download powerpoint
Fig. 1.

Flow chart. IMT = inspiratory muscle training.

Nine studies (n = 965 subjects) assessed IMT in association with some other type of intervention.57-65 These other interventions were pulmonary rehabilitation,58,62,64,65 resis-tance/aerobic training with cycle ergometer,59-61,63 or conventional physical therapy.57 In 4 studies (n = 153 subjects), the associated IMT was conducted in subjects with respiratory muscle weakness.57,58,60,63 The loads used for IMT associated with other interventions varied: 30% of PImax,59,63 30–60% of PImax,61,62,64,65 70% of PImax,58,60 and 60–80% of PImax.57 For isolated IMT, most studies used IMT with low or no load, and the control group was IMT placebo. For studies that assessed IMT in association with another intervention, most studies used low-load IMT or pulmonary rehabilitation as control groups (can be seen in supplementary materials at http://www.rcjournal.com).

Risk of Bias

Of the studies included in this systematic review, 15.2% reported allocation concealment, 17.4% reported blinding of therapists, and 30.4% used the principle of intention to treat for statistical analyses, characterizing a high risk of bias for these items. Still, 34.8% used patient blinding, and 39.1% used blinding for outcome appraisers, which carry moderate bias risk. Finally, 80.4% of the included studies described losses in follow-up and exclusions, and 65.2% reported randomization in subject assignment, which carry moderate risk of bias (see the supplementary materials at http://www.rcjournal.com).

Effects of Interventions

Maximum Inspiratory Pressure.

Of the 39 papers included that conducted isolated IMT, 36 studies17-27,29-34,36-41,43-55 assessed PImax (n = 889 subjects). Significant improvement occurred in PImax when IMT was compared to the control groups (10.64 cm H2O, 95% CI 7.61–13.66, I2: 46%) (Fig. 2). Based on the GRADE approach, the quality of evidence for this result was considered low due to methodological limitations, imprecision, and inconsistency of results (Table 1). Considering the 24 studies that only included subjects with inspiratory muscle weakness,17-19,22-27,31-34,37,38,40,41,43,45-49,52 there was significant improvement for this outcome (9.60 cm H2O, 95% CI 5.74–13.46, I2: 40%). In addition, considering studies that included subjects without respira-tory muscle weakness,20,21,29,30,36,39,44,50,51,53-55 significant improvement was also observed for this outcome (13.61 cm H2O, 95% CI 12.45–14.78, I2: 0%). The assessment of studies that used up to 35% of PImax training loads showed improvement in this outcome (8.30 cm H2O, 95% CI 1.38–15.21, I2: 0%); the same behavior was observed for loads between 40% and 50% (11.20 cm H2O, 95% CI 5.86–16.54, I2: 0%), and a slightly superior gain was observed for loads between 60% to 80% of PImax (10.99 cm H2O, 95% CI 6.65–15.33, I2: 68%). Gains observed with shorter intervention times were equivalent to gains obtained with longer interventions: ≤ 4 weeks (11.62 cm H2O, 95% CI 5.32–17.91, I2: 0%); 6–8 weeks (11.69 cm H2O, 95% CI 8.14–15.25, I2: 39%); 16 weeks (15.75 cm H2O, 95% CI 5.03–26.47, I2: 0%); and no difference was observed for 10 weeks and 12 weeks (8.84 cm H2O, 95% CI −0.71 to 18.39, I2: 66%). When included in meta-regression, these covariates were not significantly associated with the heterogeneity observed through the studies (data not shown).

Fig. 2.
  • Download figure
  • Open in new tab
  • Download powerpoint
Fig. 2.

A: PImax for treatment with isolated IMT against control group. PImax = maximum inspiratory pressure; IMT = inspiratory muscle training.

View this table:
  • View inline
  • View popup
  • Download powerpoint
Table 1.

Quality of Evidence

In the analysis of studies that assessed IMT associated with other interventions, we identified 8 papers57-60,62-65 that assessed PImax (n = 985 subjects), and significant improvement was observed in this outcome (8.44 cm H2O, 95% CI 4.98–11.91, I2: 0%) (Fig. 3). The quality of evidence was considered moderate based on methodology limitations, imprecision, and inconsistency of results (Table 1). Considering the 4 studies that only included subjects with inspiratory muscle weakness57,58,60,63 (8.44 cm H2O, 95% CI 0.60–16.28, I2: 0%) and studies including subjects without respiratory muscle weakness (8.46 cm H2O, 95% CI 4.58–12.34, I2: 0%), there was significant improvement in both situations. Studies that used IMT loads between 60% and 80% of PImax obtained significant improvement (10.08 cm H2O, 95% CI 1.05–19.11, I2: 0%). Significant improvement in PImax was also observed in studies with interventions that lasted 3–4 weeks (8.51 cm H2O, 95% CI 4.59–12.42, I2: 0%) and 10–12 weeks (10.97 cm H2O, 95% CI 0.95–20.99, I2: 0%).

Fig. 3.
  • Download figure
  • Open in new tab
  • Download powerpoint
Fig. 3.

PImax for treatment with associated IMT against control group. PImax = maximum inspiratory pressure; IMT = inspiratory muscle training.

FVC.

We identified 10 studies18,19,24,26,32,33,39,52,53,55 that conducted isolated IMT and assessed FVC, and no significant improvement was observed (−0.28, 95% CI −0.62 to 0.07, I2: 85%) (see the supplementary materials at http://www.rcjournal.com). Based on the GRADE approach, the quality of evidence for this result was very low due to methodology limitations and inconsistency of results (Table 1). No change in this result was found for the 6 studies that only included patients with inspiratory muscle weakness18,19,26,32,33,52 (−0.10, 95% CI −0.42 to 0.23, I2: 42%), and the same occurred for subjects without respiratory weakness (−0.62, 95% CI −2.01 to 0.77, I2: 94%). In the analysis of IMT loads up to 35% of PImax (−0.04, 95% CI −0.92 to 0.84, I2: 0%) and intervention durations of 4–5 weeks (−1.22, 95% CI −6.17 to 3.72, I2: 0%) and 6–8 weeks (−0.30, 95% CI −0.68 to 0.07, I2: 90%), no significant difference was observed between IMT and controls.

FEV1.

We identified 10 studies18,19,24,26,29,32,42,52,53,55 that conducted isolated IMT and assessed FEV1 (n = 259 subjects). The comparison between IMT and control groups revealed an improvement in FEV1 (0.08, 95% CI 0.02–0.13, I2: 0%) (Fig. 4). Based on the GRADE approach, the quality of evidence for this result was moderate due to methodology limitations and inconsistency of results (Table 1). For the 6 studies that only included subjects with inspiratory muscle weakness,18,19,24,26,32,52 there was no significant difference (−0.02, 95% CI −0.17 to 0.13, I2: 0%). However, in the analysis of subjects without muscle weakness, there was improvement of this outcome (0.09, 95% CI 0.03–0.16, I2: 0%). No improvement of this outcome was found in the analysis of IMT loads up to 35% of PImax (0.00, 95% CI −0.28 to 0.28, I2: 0%), and improvement occurred according to intervention duration of 6–8 weeks (0.08, 95% CI 0.03–0.14, I2: 0%).

Fig. 4.
  • Download figure
  • Open in new tab
  • Download powerpoint
Fig. 4.

FEV1 for treatment with isolated IMT against control group. IMT = inspiratory muscle training.

Vital Capacity.

Three studies29,33,42 that analyzed isolated IMT and assessed vital capacity (n = 73), and no improvement was observed compared to the control groups (−0.08, 95% CI −0.81 to 0.64, I2: 0%). Based on the GRADE approach, the quality of evidence for this result was low due to methodology limitations and inconsistency of results (Table 1).

Distance Walked in 6MWT.

We identified 22 studies17,18,20,22,23,26,27,29,32-35,37,39-41,46-48,51,53,55 that analyzed isolated IMT and assessed distance walked in 6MWT (n = 605 subjects) with significant improvement (34.28 m, 95% CI 29.43–39.14, I2: 0%) (Fig. 5). Based on the GRADE approach, the quality of evidence for this result was low due to methodology limitations and inconsistency of results (Table 1).

Fig. 5.
  • Download figure
  • Open in new tab
  • Download powerpoint
Fig. 5.

6MWT for treatment with isolated IMT against control group. IMT = inspiratory muscle training; 6MWT = 6-min-walk test.

There was significant improvement for this outcome in the 15 studies that only included subjects with inspiratory muscle weakness17,18,22,23,26,27,32-34,37,40,41,46-48 (28.87 m, 95% CI 8.53–49.22, I2: 0%), and the increase was higher in subjects without respiratory muscle weakness (34.64 m, 95% CI 29.64–39.65 I2: 0%). When IMT loads of 40–50% of PImax were analyzed, there was no significant improvement (21.94 m, 95% CI −10.74 to 54.62, I2: 0%); however, this outcome showed improvement in IMT loads superior to 60–80% (34.72 m, 95% CI 29.72–39.73, I2: 0%). In relation to intervention duration, no improvement was observed for this outcome in studies that carried out the intervention for 4 weeks (20.76 m, 95% CI 12.24 to 53.77, I2: 0%), and the same occurred for interventions that lasted 10–12 weeks (59.05 m, 95% CI 14.88 to 132.97, I2: 0%. The results were different for interventions of 6–8 weeks, which showed significant improvement (34.46 m, 95% CI 29.54–39.38, I2: 0%). In meta-regression analyses, no tested covariates were able to explain the heterogeneity observed (data not shown).

While analyzing studies that performed IMT associated with other interventions, 5 studies57,62-65 assessed 6MWT(n = 869 subjects), and no significant difference was observed for this outcome (8.40 m, 95% CI −22.90 to 39.71, I2: 50%) (Fig. 6). Based on GRADE, quality of evidence for this outcome was considered moderate due to methodology limitations, imprecision and inconsistency of results (Table 1). No improvement was observed for this outcome in studies that carried out the intervention for 3 to 4 weeks (14.10 m [95% CI: −25.16 to 53.35; I2: 62%]). In sensitivity analysis of studies that included subjects without inspiratory muscle weakness,62,64,65 significant improvement was observed in 6MWT in favor of the control group when compared to IMT (−2,34 m [95% CI: −20.47 to 15.80; I2: 0%]).

Fig. 6.
  • Download figure
  • Open in new tab
  • Download powerpoint
Fig. 6.

6MWT for treatment with associated IMT against control group. IMT = inspiratory muscle training; 6MWT = 6-min-walk test.

Maximum Oxygen Consumption.

Three studies36,40,44 that analyzed isolated IMT assessed maximum oxygen consumption (Embedded Image ) (n = 82 subjects), and no difference was observed for this outcome (0.12 mL/kg/min, 95% CI −0.14 to 0.39, I2 0%). Based on the GRADE approach, the quality of evidence for this result was considered very low due to methodology limitations and inconsistency of results (Table 1). In 3 studies58-60 that conducted IMT associated with other intervention and assessed Embedded Image (n = 96 subjects), no difference was observed (−0.02 mL/kg/min, 95% CI −0.22 to 0.19, I2: 0%). All studies included subjects that had respiratory muscle weakness. Based on the GRADE approach, the quality of evidence for this result was considered low due to methodology limitations and inconsistency of results (Table 1).

Dyspnea.

We identified 12 studies29,30,32,33,35,36,40,41,46-48,51 that conducted isolated IMT and assessed dyspnea with the Borg scale (n = 280 subjects), and no significant difference was observed (−0.37, 95% CI −1.21 to 0.47, I2: 58%) (see the supplementary materials at http://www.rcjournal.com). Based on the GRADE approach, the quality of evidence for this result was considered very low due to methodology limitations and inconsistency of results (Table 1). The studies that only assessed subjects with inspiratory muscle weakness32,33,40,46-48 reported significant improvement for this outcome and an absence of heterogeneity (0.59, 95% CI −0.00 to 1.18, I2: 0%). For subjects without respiratory muscle weakness, no improvement was observed for this outcome (−1.27, 95% CI −2.67 to 0.12, I2: 69%)]. The analysis of studies with IMT loads of 40–50% (0.45, 95% CI −0.36 to 1.26, I2: 38%) and 60–80% (0.18, 95% CI −0.93 to 1.29, I2: 0%) showed no significant improvement for this outcome. Studies with intervention durations of 4 weeks (−0.83, 95% CI −1.88 to 0.22, I2: 20%) and 6–8 weeks (−0.26, 95% CI −1.29 to 0.76, I2: 67%) reported no significant improvement.

Quality of Life.

We identified 2 studies17,20 that conducted isolated IMT and assessed quality of life (n = 60 subjects) with loads of 60–80%, and no significant difference was observed for this outcome (18.85, 95% CI −8.00 to 45.70, I2: 0%) (see the supplementary materials at http://www.rcjournal.com). Based on the GRADE approach, the quality of evidence for this result was considered very low due to methodology limitations and inconsistency of results (Table 1).

Discussion

Summary of Evidence

This systematic review and meta-analysis indicates that isolated IMT improves inspiratory muscle strength, functional capacity, and pulmonary function, without difference in dyspnea and quality of life. IMT associated with other interventions, on the other hand, presented increases only in inspiratory muscle strength.

Significant improvement in the distance walked in the 6MWT was observed only for isolated IMT; in subjects without respiratory muscle weakness, the increase was higher. In addition, this improvement can be considered to be a clinically relevant difference for patients with COPD, for whom one of the major limitations is functional capacity.

With regard to Embedded Image , dyspnea, and quality of life, there was no significant difference. Moreover, gains were higher in studies that included subjects with inspiratory muscle weakness, conducted IMT for ≥ 8 weeks, and had control groups that received placebo IMT without load40 or with very low inspiratory load.20,24-27,30,31,35-37,41-43,46-49,60,61 This may be due to the higher level of deficiency in subjects included, longer duration of intervention, and the comparison of an IMT group with a control group that received placebo IMT without inspiratory load. Two studies indicated that dyspnea and distance walked on the 6MWT are inversely proportional, which probably correlates with improvement in exercise capacity.66,67

This meta-analysis observed divergent results for functional capacity. We noted a significant increase in distance walked in the 6MWT (with isolated IMT), which did not occur for maximum Embedded Image . This result may be explained by the fact that maximum and submaximum tests have different physiological determinants and the potential for postintervention improvement.68 Moreover, in the maximum Embedded Image analysis, there was a small number of subjects and, according to the GRADE approach, the quality of evidence for this result was considered very low due to methodology limitations, imprecision, and inconsistency of results.

We also observed that IMT significantly improved PImax compared to control groups. Several studies noted that PImax is reduced in subjects with COPD,10 and that IMT has a beneficial effect on this outcome.17,18,32,57 Improvement in inspiratory muscle function may have reached respiratory discharge with restoration of unbalance between inspiratory muscles capacity to sustain the activity and inspiratory loads. There is evidence that respiratory muscle weakness, observed in subjects with COPD, is improved. Moreover, this variable is directly correlated to Embedded Image , which suggests that respiratory muscle weakness contributes to the deficit in exercise capacity under COPD.69

Another important aspect concerns the loads analyzed in these studies, which ranged from 30% to 60% of PImax. In the study by Basso-Vanelli et al,18 which started IMT with initial load of 10 cm H2O and progressed to 60% of PImax after intervention, there was significant improvement in both groups with regard to respiratory muscle resistance and strength, thoracic-abdominal mobility and distance walked in the 6MWT. There was also reduction of dyspnea at 6MWT peak.

Corroborating the above mentioned results, Beckerman et al20 observed, while using IMT load of 15–60% of PImax, statistically significant increases in inspiratory muscle strength and distance walked in the 6MWT by the end of the third month of training and reduction of dyspnea by the end of 9 months of training in the intervention group, but these increases were not seen in the control group. By the end of one year of training, these changes were maintained.

Strengths and Limitations

This meta-analysis of RCTs was conducted to quantitatively express the results and to assess the quality of evidence for each outcome analyzed. We noted that the RCTs included were methodologically limited because none of them presented in full the items observed in the bias risk assessment. Another limitation is that few studies evaluated IMT for an intervention time > 10 weeks, making it difficult to discuss our results and reinforcing the need for further studies evaluating the effect of IMT in the long term. Nevertheless, there were reasonably large numbers of studies and subjects, which makes our study relevant.

According to the GRADE approach, all results, except for FEV1 outcome (IMT isolated), PImax, and 6MWT (IMT associated), which were considered moderate, presented low or very low quality of evidence. This indicates that any estimate of effect is very uncertain, and it is likely that new research will improve the confidence to estimate the effect.

Comparisons with Other Reviews

Gosselink et al10 performed a systematic review on this subject. However, this work included 32 RCTs that used IMT in subjects with COPD, whereas the present review included 46 papers that used IMT in subjects with COPD. Additionally, Gosselink et al10 limited their search for papers in English, whereas the current review did not have language limitations. Moreover, the meta-analyses analyzed here considered the type of device used, dyspnea outcome with the Borg scale, exercise capacity with the 6MWT, and quality of life with the St George Respiratory Questionnaire for subjects with COPD, which Gosselink et al10 did not do. For these reasons, some studies included in in the meta-analysis by Gosselink et al10 were excluded from our review because they did not meet our eligibility criteria or presented incomplete data, which hampered statistical analyses.

The systematic review carried out by Beaumont et al,11 which verified IMT effects in subjects with COPD regarding dyspnea, quality of life, exercise capacity, and inspiratory muscle strength, included 43 studies, with 37 meta-analyses, but the search was limited to studies in English and French. The number of studies included was similar to that of this review, although Beaumont et al11 included nonrandomized controlled trials and cohort studies in addition to RCTs, which may compromise the quality of the evidence. Our review generates a higher level of evidence against already existing evidence.

We observed that all of above-mentioned reviews assessed PImax and functional capacity with the 6MWT, with positive results for these outcomes, which corroborate our review. Our review assessed outcomes associated to with pulmonary function (ie, FVC, FEV1, maximum Embedded Image , and vital capacity), and the results are inconclusive because we found differences only for FEV1. Quality of life showed positive results as assessed in both previous reviews10,11; this differs from our results, which did not present significant improvement for this outcome. Both previous reviews10,11 assessed dyspnea and found positive results; however, we noted dyspnea improvement only in studies of subjects with inspiratory muscle weakness, showing significant improvement for this outcome and absence of heterogeneity. For most outcomes presented in this review, the evidence level is still low or very low, which indicates the need for more studies on the subject.

Conclusions

Isolated IMT is an effective treatment modality to improve inspiratory muscle strength, functional capacity, and pulmonary function in patients with COPD, without changes in dyspnea and quality of life. The presence of inspiratory muscle weakness did not change the results. Higher loads promoted a greater improvement of these outcomes. Shorter intervention times increased inspiratory muscle strength, but longer intervention times were required to increase functional capacity. Associated IMT only showed increases in inspiratory muscle strength. This analysis indicates that isolated IMT can be considered as an adjuvant intervention in patients with COPD.

Footnotes

  • Correspondence: Graciele Sbruzzi PT ScD, Rua Felizardo, n° 750, Jardim Botânico, Porto Alegre 90690200, Brazil. E-mail: graciele.sbruzzi{at}ufrgs.br
  • Ms Figueiredo presented a version of this paper at the Universidade Federal do Rio Grande do Sul, in November 2018, in Porto Alegre, Brazil.

  • This study was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior. The authors have disclosed no conflicts of interest.

  • Supplementary material related to this paper is available at http://www.rcjournal.com.

  • Copyright © 2020 by Daedalus Enterprises

References

  1. 1.↵
    Global Strategy for the Diagnosis, Management and Prevention of COPD. Global Initiative for Chronic Obstructive Lung Disease (GOLD) 2017. Available at: http://goldcopd.org. Accessed on June 1, 2018.
  2. 2.↵
    1. Halpin DM,
    2. Decramer M,
    3. Celli B,
    4. Kesten S,
    5. Liu D,
    6. Tashkin DP
    . Exacerbation frequency and course of COPD. Int J Chron Obstruct Pulmon Dis 2012(7):653-661.
  3. 3.↵
    1. Mantero M,
    2. Radovanovic D,
    3. Santus P,
    4. Blasi F
    . Management of severe COPD exacerbations: focus on beclomethasone dipropionate/formoterol/glycopyrronium bromide. Int J Chron Obstruct Pulmon Dis 2018;13:2319-2333.
    OpenUrl
  4. 4.↵
    1. Behnia M,
    2. Wheatley C,
    3. Avolio A,
    4. Johnson B
    . Influence of resting lung diffusion on exercise capacity in patients with COPD. BMC Pulm Med 2017;17(1):117.
    OpenUrl
  5. 5.↵
    1. Sanseverino MA,
    2. Pecchiari M,
    3. Bona RL,
    4. Berton DC,
    5. de Queiroz FB,
    6. Gruet M,
    7. et al
    . Limiting factors in walking performance of subjects with COPD. Respir Care 2018;63(3):301-310.
    OpenUrlAbstract/FREE Full Text
  6. 6.↵
    1. Rocha A,
    2. Arbex FF,
    3. Sperandio PA,
    4. Souza A,
    5. Biazzim L,
    6. Mancuso F,
    7. et al
    . Excess ventilation in chronic obstructive pulmonary disease-heart failure overlap. implications for dyspnea and exercise intolerance. Am J Respir Crit Care Med 2017;196(10):1264-1274.
    OpenUrl
  7. 7.↵
    1. Charususin N,
    2. Gosselink R,
    3. Decramer M,
    4. McConnell A,
    5. Saey D,
    6. Maltais F,
    7. et al
    . Inspiratory muscle training protocol for patients with chronic obstructive pulmonary disease (IMTCO study): a multicentre randomised controlled trial. BMJ Open 2013;3(8):e003101.
    OpenUrlAbstract/FREE Full Text
  8. 8.↵
    1. Puhan MA,
    2. Gimeno-Santos E,
    3. Cates CJ,
    4. Troosters T
    . Pulmonary rehabilitation following exacerbations of chronic obstructive pulmonary disease. Cochrane Database Syst Rev 2016;12(12):CD005305.
    OpenUrlCrossRefPubMed
  9. 9.↵
    1. Borge CR,
    2. Hagen KB,
    3. Mengshoel AM,
    4. Omenaas E,
    5. Moum T,
    6. Wahl AK
    . Effects of controlled breathing exercises and respiratory muscle training in people with chronic obstructive pulmonary disease: results from evaluating the quality of evidence in systematic reviews. BMC Pulm Med 2014;14:184.
    OpenUrlCrossRefPubMed
  10. 10.↵
    1. Gosselink R,
    2. De Vos J,
    3. van den Heuvel SP,
    4. Segers J,
    5. Decramer M,
    6. Kwakkel G
    . Impact of inspiratory muscle training in patients with COPD: what is the evidence? Eur Respir J 2011;37(2):416-425.
    OpenUrlAbstract/FREE Full Text
  11. 11.↵
    1. Beaumont M,
    2. Forget P,
    3. Couturaud F,
    4. Reychler G
    . Effects of inspiratory muscle training in COPD patients: a systematic review and meta-analysis. Clin Respir J 2018;12(7):2178-2188.
    OpenUrl
  12. 12.↵
    1. Higgins J,
    2. Green S
    . Cochrane handbook for systematic reviews of interventions, 5th ed. Chichester: John Wiley & Sons; 2011.
  13. 13.↵
    1. Moher D,
    2. Liberati A,
    3. Tetzlaff J,
    4. Altman DG
    , PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 2010;8(5):336-341.
    OpenUrlCrossRefPubMed
  14. 14.↵
    1. Robinson KA,
    2. Dickersin K
    . Development of a highly sensitive search strategy for the retrieval of reports of controlled trials using PubMed. Int J Epidemiol 2002;31(1):150-153.
    OpenUrlCrossRefPubMed
  15. 15.↵
    1. Higgins JP,
    2. Thompson SG,
    3. Deeks JJ,
    4. Altman DG
    . Measuring inconsistency in meta-analyses. BMJ 2003;327(7414):557-560.
    OpenUrlFREE Full Text
  16. 16.↵
    1. Guyatt GH,
    2. Oxman AD,
    3. Vist GE,
    4. Kunz R,
    5. Falck-Ytter Y,
    6. Alonso-Coello P,
    7. et al
    . GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ 2008;336(7650):924-926.
    OpenUrlFREE Full Text
  17. 17.↵
    1. Ahmad H,
    2. Justine M,
    3. Othman Z,
    4. Mohan V,
    5. Mirza FT
    . The outcomes of short term inspiratory muscle training (IMT) combined with chest physiotherapy in hospitalized COPD patients. Bangladesh J Med Sci 2013;12(4):398-404.
    OpenUrl
  18. 18.↵
    1. Basso-Vanelli R,
    2. Lorenzo V,
    3. Labadessa I,
    4. Regueiro E,
    5. Jamami M,
    6. Gomes E,
    7. et al
    . Effects of inspiratory muscle training and calisthenics-and-breathing exercises in COPD with and without respiratory muscle weakness. Respir Care 2016;61(1):50-60.
    OpenUrlAbstract/FREE Full Text
  19. 19.↵
    1. Belman MJ,
    2. Shadmehr R
    . Targeted resistive ventilatory muscle training in chronic obstructive pulmonary disease. J Appl Physiol 1988;65(6):2726-2735.
    OpenUrlPubMed
  20. 20.↵
    1. Beckerman M,
    2. Magadle R,
    3. Weiner M,
    4. Weiner P
    . The effects of 1 year of specific inspiratory muscle training in patients with COPD. Chest 2005;128(5):3177-3182.
    OpenUrlCrossRefPubMed
  21. 21.↵
    1. Bustamante Madariaga V,
    2. Gáldiz Iturri JB,
    3. Gorostiza Manterola A,
    4. Camino Buey J,
    5. Talayero Sebastián N,
    6. Sobradillo Peña V
    . [Comparison of 2 methods for inspiratory muscle training in patients with chronic obstructive pulmonary disease]. Arch Bronconeumol 2007;43(8):431-438.
    OpenUrlPubMed
  22. 22.↵
    1. Chuang HY,
    2. Chang HY,
    3. Fang YY,
    4. Guo SE
    . The effects of threshold inspiratory muscle training in patients with chronic obstructive pulmonary disease: a randomised experimental study. J Clin Nurs 2017;26(23-24):4830-4838.
    OpenUrl
  23. 23.↵
    1. Goldstein R,
    2. De Rosie J,
    3. Long S,
    4. Dolmage T,
    5. Avendano MA
    . Applicability of a threshold loading device for inspiratory muscle testing and training in patients with COPD. Chest 1989;96(3):564-571.
    OpenUrlCrossRefPubMed
  24. 24.↵
    1. Harver A,
    2. Mahler DA,
    3. Daubenspeck JA
    . Targeted inspiratory muscle training improves respiratory muscle function and reduces dyspnea in patients with chronic obstructive pulmonary disease. Ann Intern Med 1989;111(2):117-124.
    OpenUrlCrossRefPubMed
  25. 25.
    1. Heydari A,
    2. Farzad M,
    3. Ahmadi HS
    . Comparing inspiratory resistive muscle training with incentive spirometry on rehabilitation of COPD patients. Rehabil Nurs 2015;40(4):243-248.
    OpenUrl
  26. 26.↵
    1. Hill K,
    2. Jenkins S,
    3. Philippe D,
    4. Cecins N,
    5. Shepherd K,
    6. Green D,
    7. et al
    . High-intensity inspiratory muscle training in COPD. Eur Respir J 2006;27(6):1119-1128.
    OpenUrlAbstract/FREE Full Text
  27. 27.↵
    1. Hsiao S,
    2. Wu Y,
    3. Wu H,
    4. Wang T
    . Comparison of effectiveness of pressure threshold and targeted resistance devices for inspiratory muscle training in patients with chronic obstructive pulmonary disease. J Formos Med Assoc 2003;102(4):240-245.
    OpenUrlPubMed
  28. 28.↵
    1. Kim MJ,
    2. Larson JL,
    3. Covey MK,
    4. Vitalo CA,
    5. Alex CG,
    6. Patel M
    . Inspiratory muscle training in patients with chronic obstructive pulmonary disease. Nurs Res 1993;42(6):356-362.
    OpenUrlPubMed
  29. 29.↵
    1. Koppers R,
    2. Vos P,
    3. Boot C,
    4. Folgering H
    . Exercise performance improves in patients with COPD due to respiratory muscle endurance training. Chest 2006;129(4):886-892.
    OpenUrlCrossRefPubMed
  30. 30.↵
    1. Langer D,
    2. Charususin N,
    3. Jácome C,
    4. Hoffman M,
    5. McConnell A,
    6. Decramer M,
    7. et al
    . Efficacy of a novel method for inspiratory muscle training in people with chronic obstructive pulmonary disease. Phys Ther 2015;95(9):1264-1273.
    OpenUrlAbstract/FREE Full Text
  31. 31.↵
    1. Larson JL,
    2. Kim MJ,
    3. Sharp JT,
    4. Larson DA
    . Inspiratory muscle training with a pressure threshold breathing device in patients with chronic obstructive pulmonary disease. Am Rev Respir Dis 1988;138(3):689-696.
    OpenUrlPubMed
  32. 32.↵
    1. Leelarungrayub J,
    2. Pinkaew D,
    3. Puntumetakul R,
    4. Klaphajone J
    . Effects of a simple prototype respiratory muscle trainer on respiratory muscle strength, quality of life and dyspnea, and oxidative stress in COPD patients: a preliminary study. Int J Chron Obstruct Pulmon Dis 2017;12:1415-1425.
    OpenUrl
  33. 33.↵
    1. Minoguchi H,
    2. Shibuya M,
    3. Miyagawa T,
    4. Kokubu F,
    5. Yamada M,
    6. Tanaka H,
    7. et al
    . Cross-over comparison between respiratory muscle stretch gymnastics and inspiratory muscle training. Intern Med 2002;41(10):805-812.
    OpenUrlPubMed
  34. 34.↵
    1. Nikoletou D,
    2. Man WD,
    3. Mustfa N,
    4. Moore J,
    5. Rafferty G,
    6. Grant RL,
    7. et al
    . Evaluation of the effectiveness of a home-based inspiratory muscle training programme in patients with chronic obstructive pulmonary disease using multiple inspiratory muscle tests. Disabil Rehabil 2016;38(3):250-259.
    OpenUrl
  35. 35.↵
    1. Oh E
    . The effects of home-based pulmonary rehabilitation in patients with chronic lung disease. Int J Nurs Stud 2003;40(8):873-879.
    OpenUrlPubMed
  36. 36.↵
    1. Petrovic M,
    2. Reiter M,
    3. Zipko H,
    4. Pohl W,
    5. Wanke T
    . Effects of inspiratory muscle training on dynamic hyperinflation in patients with COPD. Int J Chron Obstruct Pulmon Dis 2012;7:797-805.
    OpenUrlPubMed
  37. 37.↵
    1. Preusser BA,
    2. Winningham ML,
    3. Clanton TL
    . High- vs low-intensity inspiratory muscle interval training in patients with COPD. Chest 1994;106(1):110-117.
    OpenUrlCrossRefPubMed
  38. 38.↵
    1. Quintero JI,
    2. Borzone G,
    3. Leiva A,
    4. Villafranca C,
    5. Lisboa C
    . Effects of inspiratory muscle training on the oxygen cost of breathing in patients with chronic obstructive pulmonary disease. Rev Med Chil 1999;127(4):421-428.
    OpenUrlPubMed
  39. 39.↵
    1. Ramirez-Sarmiento A,
    2. Orozco-Levi M,
    3. Guell R,
    4. Barreiro E,
    5. Hernandez N,
    6. Mota S,
    7. et al
    . Inspiratory muscle training in patients with chronic obstructive pulmonary disease: structural adaptation and physiologic outcomes. Am J Respir Crit Care Med 2002;166(11):1491-1497.
    OpenUrlCrossRefPubMed
  40. 40.↵
    1. Sánchez Riera H,
    2. Montemayor Rubio T,
    3. Ortega Ruiz F,
    4. Cejudo Ramos P,
    5. Del Castillo Otero D,
    6. Elias Hernandez T,
    7. et al.
    Inspiratory muscle training in patients with COPD: effect on dyspnea, exercise performance, and quality of life. Chest 2001;120(3):748-756.
    OpenUrlCrossRefPubMed
  41. 41.↵
    1. Séron P,
    2. Riedemann P,
    3. Muñoz S,
    4. Doussoulin A,
    5. Villarroel P,
    6. Cea X
    . Effect of inspiratory muscle training on muscle strength and quality of life in patients with chronic airflow limitation: a randomized controlled trial. Arch Bronconeumol 2005;41(11):601-606.
    OpenUrlPubMed
  42. 42.↵
    1. Sudo E,
    2. Ohga E,
    3. Matsuse T,
    4. Teramoto S,
    5. Nagase T,
    6. Katayama H,
    7. et al
    . The effects of pulmonary rehabilitation combined with inspiratory muscle training on pulmonary function and inspiratory muscle strength in elderly patients with chronic obstructive pulmonary disease. Nihon Ronen Igakkai Zasshi 1997;34(11):929-934.
    OpenUrl
  43. 43.↵
    1. Villafranca C,
    2. Borzone G,
    3. Leiva A,
    4. Lisboa C
    . Effect of inspiratory muscle training with an intermediate load on inspiratory power output in COPD. Eur Respir J 1998;11(1):28-33.
    OpenUrlAbstract/FREE Full Text
  44. 44.↵
    1. Wanke T,
    2. Formanek D,
    3. Lahrmann H,
    4. Brath H,
    5. Wild M,
    6. Wagner C,
    7. et al
    . Effects of combined inspiratory muscle and cycle ergometer training on exercise performance in patients with COPD. Eur Respir J 1994;7(12):2205-2211.
    OpenUrlAbstract/FREE Full Text
  45. 45.↵
    1. Weiner P,
    2. Azgad Y,
    3. Ganam R
    . Inspiratory muscle training combined with general exercise reconditioning in patients with COPD. Chest 1992;102(5):1351-1356.
    OpenUrlCrossRefPubMed
  46. 46.↵
    1. Weiner P,
    2. Magadle R,
    3. Beckerman M,
    4. Weiner M,
    5. Berar-Yanay N
    . Comparison of specific expiratory, inspiratory, and combined muscle training programs in COPD. Chest 2003;124(4):1357-1364.
    OpenUrlCrossRefPubMed
  47. 47.↵
    1. Weiner P,
    2. Magadle R,
    3. Beckerman M,
    4. Weiner M,
    5. Berar-Yanay N
    . Maintenance of inspiratory muscle training in COPD patients: one year follow-up. Eur Respir J 2004;23(1):61-65.
    OpenUrlAbstract/FREE Full Text
  48. 48.↵
    1. Weiner P,
    2. Magadle R,
    3. Berar-Yanay N,
    4. Davidovich A,
    5. Weiner M
    . The cumulative effect of long-acting bronchodilators, exercise, and inspiratory muscle training on the perception of dyspnea in patients with advanced COPD. Chest 2000;118(3):672-678.
    OpenUrlCrossRefPubMed
  49. 49.↵
    1. Weiner P,
    2. Weiner M
    . Inspiratory muscle training may increase peak inspiratory flow in chronic obstructive pulmonary disease. Respiration 2006;73(2):151-156.
    OpenUrlPubMed
  50. 50.↵
    1. Heijdra YF,
    2. Dekhuijzen PNR,
    3. Herwaarden C. V,
    4. Folgering HT
    . Nocturnal saturation improves by target-flow inspiratory muscle training in patients with COPD. Am J Respir Crit Care Med 1996;153(1):260-265.
    OpenUrlPubMed
  51. 51.↵
    1. Lisboa C,
    2. Villafranca C,
    3. Leiva A,
    4. Cruz E,
    5. Pertuze J,
    6. Borzone G
    . Inspiratory muscle training in chronic airflow limitation: effect on exercise performance. Eur Respir J 1997;10(3):537-542.
    OpenUrlAbstract
  52. 52.↵
    1. Wu W,
    2. Guan L,
    3. Zhang X,
    4. Li X,
    5. Yang Y,
    6. Guo B,
    7. et al
    . Effects of two types of equal-intensity inspiratory muscle training in stable patients with chronic obstructive pulmonary disease: a randomised controlled trial. Respir Med 2017;132:84-91.
    OpenUrl
  53. 53.↵
    1. Cooper CB
    . Desensitization to dyspnea in COPD with specificity for exercise training mode. Int J Chron Obstruct Pulmon Dis 2009;4(1):33-43.
    OpenUrlPubMed
  54. 54.↵
    1. Covey MK,
    2. Larson JL,
    3. Wirtz SE,
    4. Berry JK,
    5. Pogue NJ,
    6. Alex CG,
    7. et al
    . High-intensity inspiratory muscle training in patients with chronic obstructive pulmonary disease and severely reduced function. J Cardiopulm Rehabil 2001;21(4):231-240.
    OpenUrlCrossRefPubMed
  55. 55.↵
    1. Mehani SHM
    . Comparative study of two different respiratory training protocols in elderly patients with chronic obstructive pulmonary disease. Clin Interv Aging 2017;12:1705-1715.
    OpenUrl
  56. 56.↵
    1. Agusti A,
    2. Calverley PM,
    3. Celli B,
    4. Coxson HO,
    5. Edwards LD,
    6. Lomas DA,
    7. et al
    . Characterisation of COPD heterogeneity in the ECLIPSE cohort. Respir Res 2010;11:122.
    OpenUrlCrossRefPubMed
  57. 57.↵
    1. Dellweg D,
    2. Reissig K,
    3. Hoehn E,
    4. Siemon K,
    5. Haidl P
    . Inspiratory muscle training during rehabilitation in successfully weaned hypercapnic patients with COPD. Respir Med 2017;123:116-123.
    OpenUrl
  58. 58.↵
    1. Dekhuijzen PN,
    2. Beek MM,
    3. Folgering HT,
    4. Van Herwaarden CL
    . Psychological changes during pulmonary rehabilitation and target-flow inspiratory muscle training in COPD patients with a ventilatory limitation during exercise. Int J Rehabil Res 1990;13(2):109-117.
    OpenUrlPubMed
  59. 59.↵
    1. Larson JL,
    2. Covey MK,
    3. Wirtz SE,
    4. Berry JK,
    5. Alex CG,
    6. Langbein WE,
    7. et al
    . Cycle ergometer and inspiratory muscle training in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1999;160(2):500-507.
    OpenUrlCrossRefPubMed
  60. 60.↵
    1. Mador MJ,
    2. Deniz O,
    3. Deniz O,
    4. Aggarwal A,
    5. Shaffer M,
    6. Kufel TJ,
    7. Spengler CM
    . Effect of respiratory muscle endurance training in patients with COPD undergoing pulmonary rehabilitation. Chest 2005;128(3):1216-1224.
    OpenUrlCrossRefPubMed
  61. 61.↵
    1. Majewska-Pulsakowska M,
    2. Wytrychowski K,
    3. Rożek-Piechura K
    . The role of inspiratory muscle training in the process of rehabilitation of patients with chronic obstructive pulmonary disease. Adv Exp Med Biol 2016;885:47-51.
    OpenUrl
  62. 62.↵
    1. Beaumont M,
    2. Mialon P,
    3. Le Ber-Moy C,
    4. Lochon C,
    5. Péran L,
    6. Pichon R,
    7. et al
    . Inspiratory muscle training during pulmonary rehabilitation in chronic obstructive pulmonary disease: a randomized trial. Chron Respir Dis 2015;12(4):305-312.
    OpenUrlCrossRefPubMed
  63. 63.↵
    1. Wang K,
    2. Zeng G-Q,
    3. Li R,
    4. Luo Y-W,
    5. Wang M,
    6. Hu Y-H,
    7. et al
    . Cycle ergometer and inspiratory muscle training offer modest benefit compared with cycle ergometer alone: a comprehensive assessment in stable COPD patients. Int J Chron Obstruct Pulmon Dis 2017;12:2655-2668.
    OpenUrl
  64. 64.↵
    1. Schultz K,
    2. Jelusic D,
    3. Wittmann M,
    4. Krämer B,
    5. Huber V,
    6. Fuchs S,
    7. et al
    . Inspiratory muscle training does not improve clinical outcomes in 3-week COPD rehabilitation: results from a randomised controlled trial. Eur Respir J 2018;51(1):1702000.
    OpenUrlAbstract/FREE Full Text
  65. 65.↵
    1. Beaumont M,
    2. Mialon P,
    3. Le Ber C,
    4. Le Mevel P,
    5. Péran L,
    6. Meurisse O,
    7. et al
    . Effects of inspiratory muscle training on dyspnoea in severe COPD patients during pulmonary rehabilitation: controlled randomised trial. Eur Respir J 2018;51(1):1701107.
    OpenUrlAbstract/FREE Full Text
  66. 66.↵
    1. Laohachai K,
    2. Winlaw D,
    3. Selvadurai H,
    4. Gnanappa GK,
    5. d’Udekem Y,
    6. Celermajer D,
    7. Ayer J
    . Inspiratory muscle training is associated with improved inspiratory muscle strength, resting cardiac output, and the ventilatory efficiency of exercise in patients with a Fontan circulation. J Am Heart Assoc 2017;6(8):e005750.
    OpenUrlAbstract/FREE Full Text
  67. 67.↵
    1. Laoutaris ID,
    2. Dritsas A,
    3. Brown MD,
    4. Manginas A,
    5. Kallistratos MS,
    6. Degiannis D,
    7. et al
    . Immune response to inspiratory muscle training in patients with chronic heart failure. Eur J Cardiovasc Prev Rehabil 2007;14(5):679-685.
    OpenUrlCrossRefPubMed
  68. 68.↵
    1. Plentz RD,
    2. Sbruzzi G,
    3. Ribeiro RA,
    4. Ferreira JB,
    5. Dal Lago P
    . Inspiratory muscle training in patients with heart failure: meta-analysis of randomized trials. Arq Bras Cardiol 2012;99(2):762-771.
    OpenUrlCrossRefPubMed
  69. 69.↵
    1. Albuquerque AL,
    2. Quaranta M,
    3. Chakrabarti B,
    4. Aliverti A,
    5. Calverley PM
    . Exercise performance and differences in physiological response to pulmonary rehabilitation in severe chronic obstructive pulmonary disease with hyperinflation. J Bras Pneumol 2016;42(2):121-129.
    OpenUrl
PreviousNext
Back to top

In this issue

Respiratory Care: 65 (8)
Respiratory Care
Vol. 65, Issue 8
1 Aug 2020
  • Table of Contents
  • Table of Contents (PDF)
  • Cover (PDF)
  • Index by author

 

Print
Download PDF
Article Alerts
Sign In to Email Alerts with your Email Address
Email Article

Thank you for your interest in spreading the word on American Association for Respiratory Care.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Inspiratory Muscle Training in COPD
(Your Name) has sent you a message from American Association for Respiratory Care
(Your Name) thought you would like to see the American Association for Respiratory Care web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Citation Tools
Inspiratory Muscle Training in COPD
Renata I N Figueiredo, Aline M Azambuja, Felipe V Cureau, Graciele Sbruzzi
Respiratory Care Aug 2020, 65 (8) 1189-1201; DOI: 10.4187/respcare.07098

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero

Share
Inspiratory Muscle Training in COPD
Renata I N Figueiredo, Aline M Azambuja, Felipe V Cureau, Graciele Sbruzzi
Respiratory Care Aug 2020, 65 (8) 1189-1201; DOI: 10.4187/respcare.07098
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Tweet Widget
  • Facebook Like
  • Google Plus One

Jump to section

  • Article
    • Abstract
    • Introduction
    • Methods
    • Results
    • Discussion
    • Conclusions
    • Footnotes
    • References
  • Figures & Data
  • Info & Metrics
  • References
  • PDF

Related Articles

Cited By...

Keywords

  • breathing exercises
  • COPD
  • dyspnea
  • physical capacity
  • respiratory muscle training

Info For

  • Subscribers
  • Institutions
  • Advertisers

About Us

  • About the Journal
  • Editorial Board

AARC

  • Membership
  • Meetings
  • Clinical Practice Guidelines

More

  • Contact Us
  • RSS
American Association for Respiratory Care

Print ISSN: 0020-1324        Online ISSN: 1943-3654

© Daedalus Enterprises, Inc.

Powered by HighWire