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REVIEW ARTICLE (META-ANALYSIS)
Effects of Respiratory Muscle Training on Respiratory
Function, Respiratory Muscle Strength, and Exercise
Tolerance in Patients Poststroke: A Systematic Review
With Meta-Analysis
Mansueto Gomes-Neto, PT, PhD,
a,b,c
Micheli Bernardone Saquetto, PT, MSc,
a,b
Cassio Magalha˜es Silva, PT, MSc,
a
Vitor Oliveira Carvalho, PT, PhD,
c,d
Nildo Ribeiro, PT, PhD,
a
Cristiano Sena Conceic¸a˜o, PT, PhD
a
From the
a
Department of Physical Therapy, Federal University of Bahia, Salvador, Bahia, Brazil;
b
Postgraduate Program in Medicine and
Health - UFBA, Salvador, Bahia, Brazil;
c
The GREAT Group (Study Group on Physical Activity), Aracaju, Sergipe, Brazil; and
d
Department
of Physical Therapy, Federal University of Sergipe, Aracaju, Sergipe, Brazil.
Abstract
Objective: To examine the effects of respiratory muscle training on respiratory function, respiratory muscle strength, and exercise tolerance in
patients poststroke.
Data Sources: We searched MEDLINE, Cochrane Library, Embase, SciELO, Physiotherapy Evidence Database (PEDro), and CINAHL (from the
earliest date available to November 2015) for trials.
Study Selection: Randomized controlled trials (RCTs) that examined the effects of respiratory muscle training versus nonrespiratory muscle
training in patients poststroke. Two reviewers selected studies independently.
Data Extraction: Extracted data from the published RCTs. Study quality was evaluated using the PEDro Scale. Weighted mean differences
(WMDs), standard mean differences (SMDs), and 95% confidence intervals (CIs) were calculated.
Data Synthesis: Eight studies met the study criteria. Respiratory muscle training improved maximal inspiratory pressure WMDs (7.5; 95% CI,
2.7e12.4), forced vital capacity SMDs (2.0; 95% CI, 0.6e3.4), forced expiratory volume at 1 second SMDs (1.2; 95% CI, 0.6e1.9), and exercise
tolerance SMDs (0.7; 95% CI, 0.2e1.2). No serious adverse events were reported.
Conclusions: Respiratory muscle training should be considered an effective method of improving respiratory function, inspiratory muscle
strength, and exercise tolerance in patients poststroke. Further research is needed to determine optimum dosages and duration of effect.
Archives of Physical Medicine and Rehabilitation 2016;-:-------
ª2016 by the American Congress of Rehabilitation Medicine
Impaired motor function is one of the most frequent and persistent
consequences of stroke.
1
Not only are peripheral muscles involved
in poststroke disability, but respiratory muscle weakness, low
thorax expansion, and postural trunk dysfunction may also play an
important role in exercise capacity and the ability to carry out
activities of daily living.
2-6
Respiratory muscle strength can be reduced in patients post-
stroke,
7,8
which reasonably justifies the use of respiratory muscle
training in this population. However, despite the fact that certain
effects of respiratory muscle training in patients poststroke have
been shown in previous reviews,
9,10
evidence regarding the effi-
cacy of respiratory muscle training is inconclusive and contro-
versial. Xiao et al
9
concluded that there was insufficient evidence
to support inspiratory muscle training after stroke. Pollock et al
10
concluded that respiratory muscle training can improve inspiratory
but not expiratory muscle strength in neurologic conditions, but
that its clinical benefit remains unknown.
Martı
´n-Valero et al
11
recently published a systematic review
with meta-analysis and reported that respiratory muscle training
Disclosures: none.
0003-9993/16/$36 - see front matter ª2016 by the American Congress of Rehabilitation Medicine
http://dx.doi.org/10.1016/j.apmr.2016.04.018
Archives of Physical Medicine and Rehabilitation
journal homepage: www.archives-pmr.org
Archives of Physical Medicine and Rehabilitation 2016;-:-------
can improve strength and endurance of respiratory muscles in
patients poststroke. However, they included in the meta-analysis
studies that were not randomized controlled trials (RCTs) and
studies that did not used respiratory muscle training as an inter-
vention. In addition, the literature search for this meta-analysis
was up to November 2014, and a number of new studies have
been completed and published since.
Since previous reviews were published,
9-11
RCTs have been
completed, but as far as we know, there is no published meta-
analysis on the effects of respiratory muscle training in pa-
tients poststroke. This systematic review and meta-analysis
aimed to analyze the published RCTs that investigated the ef-
fects of respiratory muscle training on respiratory function,
respiratory muscle strength, and exercise tolerance in patients
poststroke.
Methods
This meta-analysis was completed in accordance with Preferred
Reporting Items for Systematic Reviews and Meta-Analyses
guidelines.
12
Eligibility criteria
This systematic review included all RCTs that studied the effects
of respiratory muscle training in patients poststroke. Studies were
considered for inclusion regardless of their publication status,
language, or size. To be eligible, each trial should have random-
ized patients poststroke (independent of time since stroke [ie,
acute, subacute, or chronic stages]) to at least 1 group of respi-
ratory muscle training.
Respiratory muscle strength training was defined as the
application of inspiratory muscle training, expiratory muscle
training, or the combination of inspiratory and expiratory muscle
training. We included all RCTs that studied the effects of respi-
ratory muscle training compared with no respiratory muscle
training or sham respiratory muscle training.
Decisions regarding what health outcomes to include in the
systematic review were made by examining what outcomes
were studied in previously conducted RCTs and systematic
reviews on stroke rehabilitation. These key indicators consisted
of the following: forced vital capacity (FVC) and forced
expiratory volume in 1 second (FEV
1
)asameasureofrespi-
ratory function; maximal inspiratory pressure (MIP) and
maximal expiratory pressure (MEP) as a measure of respiratory
muscle strength; and peak oxygen consumption, exercise time,
or maximum workload during a cardiopulmonary exercise test
or maximal distance in walk tests as a measure of exer-
cise tolerance.
Information sources and search
We searched for references on MEDLINE, Embase, SciELO,
CINAHL, Physiotherapy Evidence Database (PEDro), and the
Cochrane Library up to November 2015 without language re-
strictions. A standard protocol for this search was developed, and
whenever possible, controlled vocabulary (Medical Subject
Heading terms for MEDLINE and Cochrane, and Emtree terms
for Embase) was used. Keywords and their synonyms were used to
sensitize the search.
The optimally sensitive search strategy developed by Higgins
and Green
13
was used to identify RCTs in PubMed/MEDLINE. To
identify RCTs in Embase, a search strategy using similar terms
was adopted, in which there were 4 groups of keywords: study
design, participants, interventions, and outcome measures.
We checked the references of the articles included in this meta-
analysis to identify other potentially eligible studies. For ongoing
studies or when the confirmation of any data or additional infor-
mation was needed, the authors were contacted by e-mail.
Data collection and analysis
The previously described search strategies were used to obtain
titles and abstracts of studies that might be relevant for this review.
Each abstract identified in the research was independently evalu-
ated by 2 authors. If at least 1 of the authors considered 1 refer-
ence eligible, the full text was obtained for complete assessment.
Two reviewers independently evaluated the full-text articles for
eligibility using inclusion and exclusion criteria. In the event of
any disagreement, each of the authors discussed the reasons for
their decisions, and a final decision was made by consensus.
Two authors independently extracted data from the published
reports using standard data extraction forms adapted from the
Cochrane Collaboration
13
model. Aspects of the study population,
types of intervention performed, follow-up and loss to follow-up,
outcome measures, and results were reviewed. Disagreements
were resolved by 1 of the authors. Any further information
required from the original author was requested by e-mail.
Quality of meta-analysis evidence
There are several scales for assessing the quality of RCTs, and the
quality of evidence generated by this meta-analysis was classified
using the PEDro Scale. The PEDro Scale assesses the methodo-
logic quality of a study based on important criteria (eg, concealed
allocation, intention-to-treat analysis, adequacy of follow-up).
These characteristics make the PEDro Scale a useful tool for
assessing the quality of physical therapy and rehabilitation trials.
14
Methodologic quality was independently assessed by 2 re-
searchers. Studies were scored on the PEDro Scale based on a
Delphi list
15
that consisted of 11 items. One item on the PEDro
Scale (eligibility criteria) is related to external validity and is
generally not used to calculate the method score, leaving a score
range of 0 to 10.
16
Data synthesis and analysis
Pooled effect estimates were obtained by comparing the least
squares mean percentage change from baseline to the end of the
study for each group and were expressed as the weighted mean
difference between groups. When the SD of change was
not available, the SD of the baseline measure was used for the
List of abbreviations:
CI confidence interval
FEV
1
forced expiratory volume in 1 second
FVC forced vital capacity
MEP maximal expiratory pressure
MIP maximal inspiratory pressure
PEDro Physiotherapy Evidence Database
RCT randomized controlled trial
2 M. Gomes-Neto et al
www.archives-pmr.org
meta-analysis. Calculations were made using a fixed and random-
effects models, and 1 comparison was made: respiratory muscle
training versus nonrespiratory muscle training group. An avalue
of .05 was considered significant. Statistical heterogeneity of the
treatment effect among studies was assessed using Cochran Q test
and the inconsistency I
2
test, in which values >25% and 50% were
considered indicative of moderate and high heterogeneity,
respectively.
17
All analyses were conducted using Review Man-
ager Version 5.3.
a
Results
Description of selected studies
The initial search led to the identification of 309 abstracts, 19 of
which were considered potentially relevant and were retrieved for
detailed analysis. Seven studies met the eligibility criteria.
Figure 1 shows the Preferred Reporting Items for Systematic
Reviews and Meta-Analyses flow diagram of studies in
this review.
The remaining 7 articles
18-24
were fully analyzed, approved by
both reviewers, and had their data extracted. Each of the articles
was scored using the PEDro Scale methodology by both
reviewers. Studies included in this review had PEDro scores of 4
through 8; the mean methodologic quality of the included studies
was 6.1. The results of the assessment of the PEDro Scale are
presented individually in table 1.
Study characteristics
The number of participants in the included studies ranged from
18
22
to 109.
19
The mean age of the participants ranged from 54 to
65 years. All of the studies included patients of both sexes, but
there was an overall predominance of men. Two studies
19,20
included patients within 2 weeks of stroke onset, whereas
others
18,21-24
included patients with >6 months of stroke. Four
studies
19,20,23,24
evaluated the initial MIP, and 3 studies
19,20,24
evaluated the initial MEP. The average of the initial MIP was
47.4cmH
2
O, and the average of the initial MEP was 61.6cmH
2
O.
Table 2 summarizes the respiratory muscle training characteristics
of the included studies.
The parameters used in the application of respiratory muscle
training were reported in most studies. In all of the studies, 3 to 18
weeks of respiratory muscle training programs were per-
formed.
19,23
Further, sessions were performed 3 to 6 times per
week.
21-24
The intensity of resistance exercise was adjusted by the
MIP assessment.
Fig 1 Search and selection of studies for systematic review according to the Preferred Reporting Items for Systematic Reviews and Meta-
Analyses.
Respiratory muscle training and stroke 3
www.archives-pmr.org
Most respiratory muscle training programs used an inspiratory
threshold loading device,
20,22
but 1 study used a flow-dependent
device,
18
which was adjusted according to the patient’s effort
(not exceeding moderate effort). The loads used in the selected
studies ranged from 30% to 60% of the MIP. In most studies, loads
of 30% to 40% were used initially,
22-24
reaching 60% of the MIP
at the end of the training period. Some authors used 2 to 6 sets
with 10 repetitions. Messaggi-Sartor,
19
Kulnik,
20
and colleagues
Table 1 Study quality on the PEDro Scale
Study
PEDro Scale
Total1*234567891011
Britto et al
23
UUUU UU UU7
Jung et al
22
UU UUU5
Kim et al
18
UU U U UU5
Kim et al
21
UU UU4
Kulnik et al
20
UUUU U UUU7
Messaggi-Sartor et al
20
UUUUU UU UU8
Sutbeyaz et al
24
UUUU UU UU7
Mean 6.1
NOTE. 1, eligibility criteria and source of participants; 2, random allocation; 3, concealed allocation; 4, baseline comparability; 5, blinded participants;
6, blinded therapists; 7, blind assessors; 8, adequate follow-up; 9, intention-to-treat analysis; 10, between-group comparisons; 11, point estimates and
variability.
* Item 1 does not contribute to the total score.
Table 2 Characteristics of the included studies
Study
Patients
(no. analyzed, age, sex)
Outcome Measures
Key Findings
Pulmonary
Function
Respiratory
Muscle
Strength
Exercise
Tolerance
Britto et al
23
NZ21, 54y, 52% men
Stroke >9mo
NA MIP, IME Cycloergometer maximum
workload
MIP and IME improved in
RMT group compared with
non-RMT group (P<.05)
Jung et al
22
NZ18, 54.44y, 61.1%
men
FVC, FEV
1
, PEF,
FEF
NA NA FEV
1
and PEF improved in
RMT group in comparison
with before and after the
intervention (P<.05)
Kim et al
18
NZ37; 59.1y; 45.94%
men
Stroke >9mo
FVC, FEV
1
NA NA FVC and FEV
1
improved in
RMT group compared with
non-RMT group (PZ.05)
Kim et al
21
NZ20; 54y
Stroke >9mo
FVC, VEF1, PEF NA 6MWT FVC, VEF1, PEF, and 6MWT
improved in RMT group
compared with non-RMT
group (P<.05)
Kulnik et al
20
NZ63; 64.4y; 60.33%
men
2wk of stroke onset
NA MIP, MEP NA MIP and MEP not improved
in RMT group compared
with non-RMT group
(P<.01)
Messaggi-Sartor
et al
20
NZ109; 65.5y; 57.8%
men
2wk of stroke onset
NA MIP, MEP NA MIP and MEP improved in
IEMT group compared
with non-IEMT group
(P<.01)
Sutbeyaz et al
24
NZ45, 61.83y, 53.33%
men
Stroke during the
previous 12mo
FVC, FEV
1
, VC,
FEF
25%e75%,
PEF, MVV
MIP, MEP Ergometer test
VO
2
peak
FVC, FEV1, VC, FEF
25%e75%
,
MVV, MIP, and VO
2
peak
improved in RMT group
compared with non-RMT
group (P<.01)
Abbreviations: 6MWT, 6-minute walking test; FEF, forced expiratory flow rate; FEF
25%e75%
, forced expiratory flow rate 25%e75%; IEMT, inspiratory and
expiratory muscle trainer; IME, inspiratory muscular endurance; MEP, muscular expiratory pressure; MIP, muscular inspiratory pressure; MVV, maximum
voluntary ventilation; NA, not assessed; PEF, peak expiratory flow rate; RMT, respiratory muscle training; VC, vital capacity; VEF1, forced expiratory
volume in 1 second; VO
2
peak, peak oxygen uptake.
4 M. Gomes-Neto et al
www.archives-pmr.org
also performed expiratory muscle training. Training loads in the
Messaggi-Sartor study
19
were set to a pressure equivalent to 30%
of the MEP; in the Kulnik study,
20
the load was set at 50% of the
MEP. The duration of the sessions varied from 15 to 30 mi-
nutes.
18,23,24
The characteristics of respiratory muscle training in
included studies are provided in table 3.
Effect of respiratory muscle training on inspiratory
and expiratory muscle strength
Four studies assessed MIP as an outcome.
19,20,23,24
Because of hetero-
geneity between studies, meta-analysis was performed with the
random-effects model. The meta-analyses showed significant
improvement in MIP at 7.55cmH
2
O (95% confidence interval [CI],
2.7e12.4; nZ167) for participants in the respiratory muscle training
group compared with the nonrespiratory muscle training group (fig 2A).
Two studies assessed MEP as an outcome.
19,20
Because of the
absence of heterogeneity between studies, meta-analysis was
performed with the fixed-effects model. The meta-analyses
showed a nonsignificant difference in MEP at 5.49cmH
2
O (95%
CI, e4.48 to 15.6; nZ119) in participants in the respiratory
muscle training group compared with the nonrespiratory muscle
training group (fig 2B).
Effect of respiratory muscle training on pulmonary
function tests
Four studies assessed FEV
1
as an outcome.
18,21,22,24
Because of
the heterogeneity between studies, meta-analysis was performed
with the random-effects model. The meta-analyses showed sig-
nificant improvement in FEV
1
of 1.22mL (95% CI, 0.57e1.88;
nZ93) for participants in the respiratory muscle training group
compared with the nonrespiratory muscle training group (fig 3A).
Four studies assessed FVC as an outcome.
18,21,22,24
Because of
the heterogeneity between studies, meta-analysis was performed
with the random-effects model. The meta-analyses showed sig-
nificant improvement in FVC of 1.99 (95% CI, 0.57e3.42; nZ93)
for participants in the respiratory muscle training group compared
with the nonrespiratory muscle training group (fig 3B).
Effect of respiratory muscle training on exercise
tolerance
Three studies assessed exercise tolerance as an outcome.
21,23,24
Because of the difference between instruments used in the
assessment of exercise tolerance, the cardiopulmonary
exercise test
23,24
and the 6-minute walk test,
21
a meta-analysis was
performed using the standardized mean difference. Because of the
heterogeneity between studies, a meta-analysis was performed with
the random-effects model. The meta-analyses showed significant
improvement in exercise tolerance of .71 (95% CI, 0.21e1.2;
nZ68) for participants in the respiratory muscle training group
compared with the nonrespiratory muscle training group (fig 4).
Discussion
The main results of our systematic review indicate that respiratory
muscle training is effective in increasing MIP, respiratory func-
tion, and exercise tolerance in patients poststroke. These findings
highlight the importance of including respiratory muscle assess-
ment as part of the evaluation and selection of patients who might
benefit from respiratory muscle training.
This systematic review with meta-analysis is important
because it analyzes respiratory muscle training as a potential
coadjuvant modality in the neurologic rehabilitation of patients
poststroke. Functional recovery is a high priority in the health care
system and also to enable independence of patients poststroke.
25
Furthermore, decreased levels of respiratory muscle strength and
exercise tolerance are important because they have been associ-
ated with an increased risk of stroke and mortality.
26,27
Patients poststroke have decreased respiratory muscle strength
and consequent diaphragm and abdominal dysfunction.
10,28
Studies have shown that patients also show decreased respira-
tory function.
28,29
Khedr et al
30
report decreased diaphragmatic
excursion in 41% of patients and reduced FVC and FEV
1
by as
much as 50% of values predicted for unaffected individuals.
Tomczak et al
31
also demonstrated that patients poststroke pre-
sented lower values of FVC, FEV
1
, and tidal volume when
compared with predictive values, which justifies the use of res-
piratory muscle training in patients poststroke. Respiratory muscle
training resulted in an increased FEV
1
and FVC. This improve-
ment can be associated with increased respiratory muscle strength.
Our systematic review showed that respiratory muscle training
is effective in increasing inspiratory muscle strength. In our meta-
analysis, the mean of the MIP in the analyzed studies was
50.6cmH
2
O at baseline, being 70.4cmH
2
O at the end of the
intervention. Specifically, the weighted mean difference in the
MIP was 7.5cmH
2
O, favoring respiratory muscle training, which
represents an improvement of 40%. A minimal clinically
Table 3 Characteristics of the respiratory muscle trainer intervention in the trials included in the review
Study Modality Intensity Time/Repetitions
Frequency
(times per wk) Length (wk) Supervision
Britto et al
23
IMT 30% of MIP 30min 5 8 No
Jung et al
22
IMT 30% of MIP 20min 3 4 Yes
Kim et al
18
IMT NA 15min 5 6 Yes
Kim et al
21
IMT NA 20min 3 4 Yes
Kulnik et al
20
IMT
EMT
50% of MIP
and MEP
5 sets of 10
repetitions
7 4 Yes
Messaggi-Sartor et al
20
IEMT
(IMT plus EMT)
IEMT: 30% of
MIP and MEP plus
10cmH
2
O each week
5 sets of 10
repetitions
5 3 Yes
Sutbeyaz et al
24
IMT 40%e60% of MIP 30min 6 6 Yes
Abbreviations: EMT, expiratory muscle trainer; IEMT, inspiratory and expiratory muscle trainer; IMT, inspiratory muscle trainer; NA, not assessed.
Respiratory muscle training and stroke 5
www.archives-pmr.org
important difference for respiratory muscle strength in patients
poststroke is not available. However, the gains were >30%, which
likely represent clinically meaningful strength gains. The results
of this review are in accordance with the findings of previous
systematic reviews on patients poststroke,
9,11
patients with Par-
kinson disease, and patients with multiple sclerosis.
32
The detected improvement in respiratory muscle strength is
also important because respiratory muscle strength is an important
determinant of exercise tolerance in patients with stroke.
33
Intol-
erance to exercise in patients poststroke may be in part because of
respiratory impairment, resulting from decreased lung volumes
and decreased inspiratory and expiratory strength. Respiratory
muscle training has notably positive effects on pulmonary function
and exercise tolerance, which ultimately can help patients carry
out their activities of daily living more easily.
34
Respiratory muscle training has also been shown to have
positive effects on pulmonary function, inspiratory muscle
strength, exercise tolerance, and activities of daily life in the
context of other chronic diseases.
35,36
The increased exercise tolerance may have been linked to
certain key factors (eg, enhanced aerobic capacity of the inspi-
ratory muscles), enabling greater minute ventilation and reduced
time to fatigue during exercise. In addition, reduced respiratory
muscle strength, elastic recoil of the lungs, and chest wall
compliance can lead to reduced exercise tolerance.
32,37,38
Therefore, the benefit obtained from respiratory muscle
strength and pulmonary function may improve exer-
cise tolerance.
The loads used in the analyzed studies ranged from 30% to
60% of the MIP. Loads <30% of the MIP seem insufficient to
Fig 2 RMT versus non-RMT: inspiratory and expiratory muscle strength. (A) Change in MIP. (B) Change in MEP. Abbreviation: RMT, respiratory
muscle training.
Fig 3 RMT versus non-RMT: FEV
1
and FVC. (A) Change in FEV
1
. (B) Change in FVC. Abbreviation: RMT, respiratory muscle training.
6 M. Gomes-Neto et al
www.archives-pmr.org
achieve improvements in inspiratory muscle strength and exercise
tolerance.
39,40
Higher loads are more commonly associated with
better functional outcomes than lower loads.
41
Another relevant aspect is pretraining respiratory muscle
strength. Four of the included studies
19,20,23,24
reported respiratory
muscle strength at baseline as <70% of the predicted value of the
MIP, or <60cmH
2
O.
42,43
The American Thoracic Society and the
European Respiratory Society show MIP values of considerably
<80cmH
2
O, the threshold for clinically meaningful weakness.
44
In a recent systematic review, Montemezzo et al
38
concluded
that patients with heart failure who had weaker inspiratory mus-
cles at baseline showed greater improvements in maximal and
submaximal exercise capacities after inspiratory muscle strength
training. Patients with greater respiratory muscle weakness
respond better to respiratory muscle training. However, because
this hypothesis was not specifically evaluated in the reviewed
studies, it should be tested in future studies.
An assessment of respiratory muscle strength should be
considered in patients poststroke before commencement of a
rehabilitation program.
45
This will help professionals identify
patients with low respiratory muscle strength, and to propose
respiratory muscle training to enhance functional abilities.
Study limitations
Given the small pool of available studies, some caution is war-
ranted when interpreting our results. A notable limitation of the
included studies is the small sample sizes in the studies. Finally,
the different protocols used to evaluate the patients and to apply
the respiratory muscle training also limited the number of studies
in this meta-analysis. Further investigation is required to explore
how the positive effects of respiratory muscle training can be
sustained over time and to determine optimum dosages, duration,
and outcomes when used in combination with peripheral muscle
training. Clearly, the value of respiratory muscle training in the
survival of patients poststroke deserves special attention in
future studies.
Conclusions
Taking into account the available studies, this systematic review
with meta-analysis showed that respiratory muscle training should
be considered an efficient method of improving MIP, respiratory
function, and exercise tolerance in patients poststroke. More well-
designed RCTs are necessary to determine the most appropriate
methods (device, intensity, frequency, and duration) to optimally
tailor the respiratory training to the particular characteristics of a
patient subgroup or individual patient.
Supplier
a. Review Manager Version 5.3; The Cochrane Collaboration.
Keywords
Exercise; Rehabilitation; Stroke
Corresponding author
Mansueto Gomes-Neto, PT, PhD, Departamento de Fisioterapia,
Curso de Fisioterapia, Universidade Federal da Bahia- UFBA,
Instituto de Cie
ˆncias da Sau
´de, Av. Reitor Miguel Calmon s/n -
Vale do Canela, Salvador CEP 40.110-100, BA, Brazil. E-mail
address: mansueto.neto@ufba.br.
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