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Received: 29 September 2017

| Revised: 13 February 2018


| Accepted: 4 April 2018
DOI: 10.1111/crj.12905

REVIEW ARTICLE

Effects of inspiratory muscle training in COPD patients:


A systematic review and meta-analysis

Marc Beaumont1 | Patrice Forget2 | Francis Couturaud3 | Gregory Reychler4,5,6

1
Pulmonary Rehabilitation Unit, Morlaix
Abstract
Hospital Centre, European University of
Occidental Brittany, Brest, France Objectives: In chronic obstructive pulmonary disease (COPD), quality of life and
2
Department of Anesthesiology and exercise capacity are altered in relationship to dyspnea. Benefits of inspiratory muscle
Perioperative Medicine, Universitair training (IMT) on quality of life, dyspnea, and exercise capacity were demonstrated,
Ziekenhuis Brussel, Brussels, Belgium
but when it is associated to pulmonary rehabilitation (PR), its efficacy on dyspnea is
3
Department of Internal Medicine and not demonstrated. The aim of this systematic review with meta-analysis was to verify
Chest Diseases, EA3878 (G.E.T.B.O.),
the effect of IMT using threshold devices in COPD patients on dyspnea, quality of
CIC INSERM 0502, University Hospital
of Brest, European University of
life, exercise capacity, and inspiratory muscles strength, and the added effect on
Occidental Brittany, Brest, France dyspnea of IMT associated with PR (vs. PR alone).
4
Institut de Recherche Experimentale et Study selection: This systematic review and meta-analysis was conducted on the
Clinique (IREC), P^ole de Pneumologie, databases from PubMed, Science direct, Cochrane library, Web of science, and
ORL & Dermatologie, Universite Pascal. Following key words were used: inspiratory, respiratory, ventilatory, muscle,
Catholique de Louvain, Brussels, Belgium
and training. The searching period extended to December 2017. Two reviewers
5
Service de Pneumologie, Cliniques
independently assessed studies quality.
Universitaires Saint-Luc, Brussels,
Belgium Results: Forty-three studies were included in the systematic review and thirty-seven
6
Cliniques Universitaires Saint-Luc, studies in the meta-analysis. Overall treatment group consisted of six hundred forty
De Medecine Physique Et Readaptation two patients. Dyspnea (Baseline Dyspnea Index) is decreased after IMT. Quality of
Service, Brussels, Belgium life (Saint George’s Respiratory Questionnaire), exercise capacity (6 min walk test)
and Maximal inspiratory pressure were increased after IMT. During PR, no added
Correspondence
effect of IMT on dyspnea was found.
Marc Beaumont, GETBO, EA 3878,
Service de Rehabilitation Respiratoire, Conclusion: IMT using threshold devices improves inspiratory muscle strength,
Centre Hospitalier des Pays de Morlaix, exercise capacity and quality of life, decreases dyspnea. However, there is no added
Kersaint-Gilly, 29600, Morlaix, France. effect of IMT on dyspnea during PR (compared with PR alone).
Email: marc.beaumont7@orange.fr

KEYWORDS
breathing exercises, chronic obstructive, dyspnea, exercise tolerance, physical exercises, pulmonary disease,
quality of life, resistance training

1 | BACKGROUND regarding dyspnea alleviation must be targeted because it is


related to treatment adherence.24
In chronic obstructive pulmonary disease (COPD), quality of Inspiratory muscle training (IMT) has been used for a long
life and exercise capacity are altered1–11 in relationship to time.25 Its benefits were demonstrated on quality of life, dysp-
dyspnea.12–16 Moreover, muscle weakness is frequent and nea, and exercise capacity26–29 and maintaining these benefits
contributes to exercise limitation.17 When it concerns inspira- requires long term treatment.30 IMT is effective alone or asso-
tory muscles, it can increase dyspnea.18–23 As dyspnea is the ciated with pulmonary rehabilitation programs.26–29 However,
main complaint in COPD patients,1 its reduction is one of when IMT is associated to pulmonary rehabilitation, its
the most important aims of the treatment. Clinical efficacy efficacy on dyspnea is not demonstrated.29

2178 | © 2018 John Wiley & Sons Ltd wileyonlinelibrary.com/journal/crj Clin Respir J. 2018;12 2178–2188.
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The previous meta-analysis was written 7 years ago and Sample size and lack of control group were not exclusion
it seems important to update these results with the studies criteria. Title and abstract were reviewed by two investiga-
published more recently because they focused on new topics tors (MB, GR) to identify potential relevant articles.
(dyspnea) and they had a high internal quality and to Disagreements were resolved by consensus or discussion
improve the knowledge of benefits of IMT in COPD with a third investigator.
patients. Indeed, since this time, 11 studies were published
and particularly during the last year.
The aim of this meta-analysis was to verify the effect of 2.4 | Study selection and data collection
IMT using threshold devices in COPD patients on dyspnea, process
quality of life, exercise capacity, and inspiratory muscles Each study was critically and independently appraised by
strength, and the added effect on dyspnea of IMT associated two investigators (MB and GR) for the following compo-
with PR (vs. PR alone). nents: sample size, patient’s characteristics and lung func-
tion, intervention (duration, frequency, intensity, and used
2 | METHOD device), comparison, summary of the results, strength, and
limits of the study. Risk ratio and mean comparison and
This systematic review was registered (PROSPERO registra- adherence/completion level were reported. The GRADE sys-
tion number: CRD42015017638) and is reported according tem was used to assess the quality of a body of evidence for
to the PRISMA guidelines.31 each individual outcome.32 The internal validity of the
randomized (controlled and cross-over) studies and observa-
tional studies was evaluated using the Physiotherapy
2.1 | Data sources and eligibility criteria Evidence Database (PEDro) scale and the Downs and Black
This systematic review was conducted on the databases from tool,33 respectively.
PubMed, Science direct, Cochrane library, Web of science,
and Pascal. Following key words were used: inspiratory,
respiratory, ventilatory, muscle, and training. They were 2.5 | Statistical analysis
applied on following disease conditions: pulmonary disease, The outcomes were isolated from the studies identified
chronic obstructive, chronic obstructive lung disease, chronic as described above. To analyze the mean differences, the
obstructive airway disease, and chronic obstructive pulmo- fixed-effect analysis model for continuous outcomes was
nary disease. The searching period extended from the data- used.
base inception to December 2017. Eligibility criteria were We analyzed the studies according to initial level of
availability of full texts in English or in French. PImax (PImax > or 60 cm H2O), on the basis of the exist-
ing literature and recommendations. Data are presented as
2.2 | Search mean, with their 95% confidence intervals. Heterogeneity
was assessed by the I2 statistics for each comparison. An
The search strategy used was as following: (inspiratory mus- I2 > 40% was considered to reject the homogeneity of the
cle training OR respiratory muscle training OR ventilatory comparison (and to accept heterogeneity hypothesis). In the
muscle training) AND (pulmonary disease OR chronic cases of heterogeneity, a random-effect model was used. For
obstructive OR chronic obstructive lung disease OR chronic all the comparisons, a P value <.05 was considered as statis-
obstructive airway disease OR chronic obstructive pulmo- tically significant.
nary disease). A filter based on the search period (01/01/ All the analyses were done using RevMan 5.3 (the
0001–31/12/2017) was used. Cochrane Collaboration, Oxford, UK).

2.3 | Inclusion criteria


3 | RESULTS
Inclusion criteria were: studies evaluating short and long
term effects of inspiratory muscle training with a threshold Two thousand and fifty-seven articles were identified but
device in stable or experiencing acute exacerbation COPD only 43 studies34–75 (38 RCT, 2 CT, and 3 cohort studies)
patients. Studies had to include one of these outcomes: dysp- were included in the systematic review and 37 out of them in
nea, quality of life, exercise capacity, and maximal inspira- the meta-analysis. Reasons for study exclusion are outlined
tory pressure (PImax). Randomized controlled trials (RCT), in Figure 1.31
non-randomized controlled trials (CT), and cohort studies The characteristics of included studies are described in
were included in this review. Table S1 (see in Supporting Information).
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FIGURE 1 Flow diagram

3.1 | Description of studies was also associated with pulmonary rehabilitation and com-
pared with usual care. In one non-randomized controlled
One thousand forty hundred and twenty-seven patients were
trial, four groups were studied: IMT 1 pulmonary rehabilita-
included in these studies and overall treatment group con-
tion; expiratory muscle training (EMT) 1 pulmonary rehabil-
sisted of six hundred and forty-two patients.
itation; IMT 1 EMT 1 pulmonary rehabilitation; pulmonary
Description of IMT programs is outlined in Table S1 (see
rehabilitation alone (control group).
in Supporting Information). Frequency of IMT was 5 days a
Methodological quality score varied from 3 to 8/10
week for 32 studies and 2 days a week in one study. Dura-
according to PEDro score for the RCT and from 1151 to 1236
tion of the training ranged from 1 week to 1 year and inten-
according to Downs and Black scale33 for the other studies.
sity of IMT varied from 30% to 80% of maximal inspiratory
pressure (PImax).
IMT was used alone in 79% of the studies or associated
3.2 | Outcomes
with general exercise training. When IMT was used alone, it
was compared with sham IMT, general exercise training, The results of effects of IMT according to the different out-
incentive spirometry, education, respiratory muscle stretch comes are mentioned in Table S2 (see in Supporting
gymnastics, expiratory muscle training, and usual care. IMT Information).
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FIGURE 2 Effects of inspiratory muscle training on dyspnea (Borg scale)

3.2.1 | Dyspnea Borg scale and VAS were used to evaluate dyspnea at
the end of the 6MWT, at the end of incremental or constant
Twenty-three studies used dyspnea as outcome. Borg scale load test or during IMT session; the decrease of dyspnea was
or modified Borg Scale, Visual Analogic Scale (VAS), not significant but trends toward a significant decrease
Baseline-Transition Dyspnea Index (BDI-TDI), Multidimen- (Figure 2). Patients without weakness of inspiratory muscles
sional Dyspnea Profile questionnaire (MDP), and item dysp- had a significant decrease of dyspnea.
nea of Chronic Respiratory Questionnaire (CRQ) were used Using BDI-TDI, the decrease of dyspnea was significant
to evaluate dyspnea. (Figure 3). There was no difference according to level of PImax.

FIGURE 3 Effects of inspiratory muscle training on dyspnea (BDI-TDI)


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FIGURE 4 Effects of inspiratory muscle training on quality of life (SGRQ)

Using item dyspnea of CRQ, the decrease of dyspnea the authors founded no difference between groups for
was clinically relevant (more than 0.5 point). improvement in dyspnea and in the last study,36 groups were
In the non-randomized controlled trial,36 dyspnea was not compared.
decreased after the program independently on the group
(control and treatment) and it was systematically clinically
3.2.2 | Quality of life
relevant (more than one point of reduction on the MMRC
scale).76 Nine studies used quality of life as outcome. Saint George’s
IMT and general exercise training reduced dyspnea after Respiratory Questionnaire (5 studies) or CRQ (3 studies) or
4 and 8 weeks, but reduction of dyspnea at the end of the Short Form 236 quality of life questionnaire (SF-36)
6MWT was not significant compared with baseline in IMT (1 study) were used to assess quality of life.
group, whereas it was significant in the general physical The results of the meta-analysis just failed to reach statis-
training group.37 The decrease of dyspnea was clinically sig- tical significant improvement of quality of life using SGRQ
nificant according to the minimal clinical important differ- (Figure 4) or CRQ (Figure 5).
ence (MCID) described by Crisafulli (one point reduction The authors of all studies without one study74 reported
with VAS)76 only for general physical training group.67 relevant improvement (reduction of at least four points in
However, the decrease of dyspnea was almost clinically sig- SGRQ or increase of more than 0.5 per item of CRQ).77
nificant only for the IMT group, at the end of the incremental
exercise test (20.8 point).37
3.2.3 | Exercise capacity
Dyspnea during constant and incremental load tests was
significantly decreased with IMT alone compared with the Thirty-three studies assessed exercise capacity with different
control group reaching the clinical relevance only for the con- tools: 6 min walk test (6MWT) (22 studies), 12MWT (5
stant load test (two points reduction with the modified Borg studies), incremental shuttle walk test (ISWT) (3 studies), or
scale).67 The decrease of dyspnea between the two groups Cardio Pulmonary Exercise Test (CPET) (5 studies).
(CET group vs. CET 1IMT group) was not different.75 IMT improved significantly walked distance during
Dyspnea at the end of 6MWT was decreased in all 6MWT and the improvement was clinically important
studies36,44,61,64,66,72,74 but was clinically relevant in only (143 m) (Figure 6).
two studies.36,61 Using ISWT or 12MWT, IMT improved exercise
Dyspnea during or at the end of IMT session was clini- capacity but the improvement was not significant (ISWT: 1
cally relevant (>2 points on Borg Scale) in all studies.34,40,62 53.96 [232.19, 140.11], P 5 .22); 12MWT: 1114.55
During PR, five authors used dyspnea as out- [289.54, 318.63], P 5 .27).
come.36,44,47,59,74 In all studies, dyspnea was decreased after Using CPET, four studies38,61,69,75 showed improvement
PR program with or without IMT. In four studies,44,47,59,74 and a study a decrease in maximal workload.59
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FIGURE 5 Effects of inspiratory muscle training on quality of life (CRQ)

3.2.4 | Inspiratory muscle strength 4 | DISCUSSION


Only 2 out of 43 studies did not evaluate PImax.46,63
The purpose of this review was to evaluate effects of IMT
PImax increased systematically after IMT training (Table
using threshold device on dyspnea, quality of life, exercise
S2) (see in Supporting Information). The increase of PImax after
capacity, and inspiratory muscle strength in COPD patients.
IMT is significant compared with Control group (Figure 7).

FIGURE 6 Effects of inspiratory muscle training on exercise capacity (6MWD)


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FIGURE 7 Effects of inspiratory muscle training on maximal inspiratory strength (PImax)

We choose to include only studies which use constant This meta-analysis showed that IMT improve dyspnea
load threshold for IMT, as it was recommended.24 compared with control group using BDI-TDI and the
Eight randomized controlled trials and one non random- improvement is clinically relevant. Two previous meta-
ized controlled trial using threshold device for IMT were analysis compared IMT with exercises training but dyspnea
published since the last meta-analysis by Gosselink et al. in was not included as outcome due to the lack of data related
2011 whereas the need for studies was clearly mentioned.29 to this outcome at this time.79,80 Petrovic et al.67 evaluated
Frequency and intensity are variables depending on the effects of IMT on inspiratory capacity (IC) and inspiratory
studies from two times per week to seven times per week fraction (IC/TLC) which are two clinical parameters reflect-
and from 30 to 80% of PImax, respectively. It highlights the ing hyperinflation. They demonstrated that in comparison
lack of clear recommendations on IMT program’s modalities, with usual care, IMT improved more hyperinflation
even if Gloeckl et al. give practical recommendations for the which is an important mechanism explaining dyspnea in
implementation of IMT during pulmonary rehabilitation.78 COPD.14–16,81–84 It provides a novel and interesting hypothe-
The methodological quality of analyzed studies is moder- sis about the mechanisms explaining efficacy of IMT on
ate (for 23 studies) to high (15 randomized controlled trial), dyspnea. However, benefit of IMT on dyspnea seems less
using Pedro scale. High methodological quality trials are important with IMT than with physical training.41,48 The
necessary for improving evidence based on IMT. added benefit of IMT on dyspnea for patients with
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inspiratory muscle weakness (PImax  60 cm H2O) was not muscle weakness) even if heterogeneity of the studies was
verified. Then the initial level of PImax seems to be not a important. However, sensitivity analyses were performed but
good predictor, whereas it is recommended, but the level of did not change significantly the results. Improvement ranged
initial breathlessness should be more appropriated, as it was from 2.5 to 93.7% (median: 25 [18–34.75]). By comparison
already suggested in the previous meta-analysis. with other respiratory disease (as asthma or cystic fibro-
Since 1996, four randomized trials44,47,59,74 and one con- sis),90,91 this improvement in PImax after IMT is similar
trolled trial36 evaluated benefit on dyspnea of adding IMT to whereas in chronic heart failure92 improvement appears more
pulmonary rehabilitation. In all studies, dyspnea was important. To our knowledge, no MCID is determining for
decreased after PR program with or without IMT. In four PImax. It means that the clinical significance of this effect is
studies,44,47,59,74 the authors founded no difference between difficult to interpret. Then to determine a MCID is an impor-
groups for improvement in dyspnea and in the last study,36 tant objective in futures studies. For patients, PImax
groups were not compared. These results show the lack of improvement alone does not seem to be important for them.
added benefit of IMT to PR (vs. PR alone) on subjective So, correlate PImax with clinical outcome could be interest-
parameters such as dyspnea. A study in progress is investi- ing for improving motivation for IMT.
gating the benefit of IMT combination to general exercise
training program.85 According to the ATS/ERS task force,9
further studies are needed to investigate added benefits of 5 | CONCLUSION
IMT on dyspnea, during a pulmonary rehabilitation program.
Since the last meta-analysis,29 only three randomized IMT improves inspiratory muscle strength, quality of life
trial63,71,74 evaluated effects of IMT on quality of life even (SGRQ), and exercise capacity (6MWT), decreases dyspnea
though the quality of life improvement is a major objective (BDI-TDI). There is no added effect of IMT on dyspnea dur-
for patients with chronic disease. Quality of life was signifi- ing PR, compared with PR alone. Level of initial PImax did
cantly and clinically improved with IMT compared with con- not seem to affect results.
trol in two studies.63,71 This clinical benefit is important to However, effects of IMT on dyspnea and quality of life
promote a better observance to the treatment and to maintain have to be more investigated. Moreover, studies are neces-
motivation. Moreover, it was suggested by Gosselink et al. sary to determine the optimal settings for IMT and MCID
using IMT at long term is one of challenges of this treatment related to PImax. Particular attention should be paid to the
to sustain benefits as quality of life.29 association of IMT with pulmonary rehabilitation.
In a study about ground based walking training, Wooton
et al.86 showed clinical benefits with such a training after
eight weeks (six points improvement in SGRQ) compared CO N FLI CT OF I N TER EST S
with usual care. Another study87 reported clinical benefits The authors declare that they have no conflicts of interest
after a 12-weeks whole-body vibration training (>10 points with the contents of this article.
improvement in SGRQ). These results are comparable those
obtained with IMT. AU TH O R CO N TR IB UT IO NS
About exercise capacity, IMT improves walk distance
Literature search, data collection, study design, analysis of
during 6MWT with clinical relevant increase. We did not
data, manuscript preparation, review of manuscript: Marc
found difference according to initial level of PImax.
However, compared with general exercise program, IMT Beaumont
seems not beneficial. It confirms previous systematic Analysis of data, manuscript preparation, review of manu-
reviews.79,80 Although Cooper showed a 23 m improvement script: Patrice Forget
in walked distance during 6MWT after IMT but it is lower Review of manuscript: Francis Couturaud
than the minimal clinical important difference,88,89 contrarily Literature search, data collection, study design, analysis of
to the improvement (32 m) observed in the physical training data, manuscript preparation, review of manuscript:
group. Benzo46 found no improvement in exercise capacity Gregory Reychler
after IMT but it can be nuanced by the short duration of the
program. Beaumont et al.44 and Wang et al.74 found no dif- ET HI CS
ference between groups for exercise capacity. Indeed, dura- No ethical approval is required.
tion of the other programs varied between four and eight
weeks. We can hypothesize that, similarly to pulmonary
rehabilitation,9 longer the program, better the benefit. O RC ID
Our meta-analysis highlighted that PImax improves with Marc Beaumont http://orcid.org/0000-0003-2354-349X
IMT in COPD patients (independently on the inspiratory Gregory Reychler http://orcid.org/0000-0002-7674-1150
2186
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TABLE S1 Characteristics of the included studies
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tions in adults with chronic obstructive pulmonary disease: a
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How to cite this article: Beaumont M, Forget P, Cou-
tory muscle training compared with other rehabilitation interven-
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review update. J Cardiopulm Rehabil Prev. 2008;28(2):128–141. training in COPD patients: A systematic review and
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Inspiratory capacity during exercise: measurement, analysis, and https://doi.org/10.1111/crj.12905
interpretation. Pulm Med. 2013;2013:1.

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