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Effect of Respiratory Muscle Training on Exercise Performance in Healthy Individuals A Systematic Review and Meta-Analysis

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Two distinct types of specific respiratory muscle training (RMT), i.e. respiratory muscle strength (resistive/threshold) and endurance (hyperpnoea) training, have been established to improve the endurance performance of healthy individuals. We performed a systematic review and meta-analysis in order to determine the factors that affect the change in endurance performance after RMT in healthy subjects. A computerized search was performed without language restriction in MEDLINE, EMBASE and CINAHL and references of original studies and reviews were searched for further relevant studies. RMT studies with healthy individuals assessing changes in endurance exercise performance by maximal tests (constant load, time trial, intermittent incremental, conventional [non-intermittent] incremental) were screened and abstracted by two independent investigators. A multiple linear regression model was used to identify effects of subjects' fitness, type of RMT (inspiratory or combined inspiratory/expiratory muscle strength training, respiratory muscle endurance training), type of exercise test, test duration and type of sport (rowing, running, swimming, cycling) on changes in performance after RMT. In addition, a meta-analysis was performed to determine the effect of RMT on endurance performance in those studies providing the necessary data. The multiple linear regression analysis including 46 original studies revealed that less fit subjects benefit more from RMT than highly trained athletes (6.0% per 10 mL · kg⁻¹ · min⁻¹ decrease in maximal oxygen uptake, 95% confidence interval [CI] 1.8, 10.2%; p = 0.005) and that improvements do not differ significantly between inspiratory muscle strength and respiratory muscle endurance training (p = 0.208), while combined inspiratory and expiratory muscle strength training seems to be superior in improving performance, although based on only 6 studies (+12.8% compared with inspiratory muscle strength training, 95% CI 3.6, 22.0%; p = 0.006). Furthermore, constant load tests (+16%, 95% CI 10.2, 22.9%) and intermittent incremental tests (+18.5%, 95% CI 10.8, 26.3%) detect changes in endurance performance better than conventional incremental tests (both p < 0.001) with no difference between time trials and conventional incremental tests (p = 0.286). With increasing test duration, improvements in performance are greater (+0.4% per minute test duration, 95% CI 0.1, 0.6%; p = 0.011) and the type of sport does not influence the magnitude of improvements (all p > 0.05). The meta-analysis, performed on eight controlled trials revealed a significant improvement in performance after RMT, which was detected by constant load tests, time trials and intermittent incremental tests, but not by conventional incremental tests. RMT improves endurance exercise performance in healthy individuals with greater improvements in less fit individuals and in sports of longer durations. The two most common types of RMT (inspiratory muscle strength and respiratory muscle endurance training) do not differ significantly in their effect, while combined inspiratory/expiratory strength training might be superior. Improvements are similar between different types of sports. Changes in performance can be detected by constant load tests, time trials and intermittent incremental tests only. Thus, all types of RMT can be used to improve exercise performance in healthy subjects but care must be taken regarding the test used to investigate the improvements.
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Effect of Respiratory Muscle Training
on Exercise Performance in Healthy
Individuals
A Systematic Review and Meta-Analysis
Sabine K. Illi,
1,2
Ulrike Held,
3
Ire
`
ne Frank
1,2
and Christina M. Spengler
1,2
1 Exercise Physiology, Institute of Human Movement Sciences, ETH Zurich, Zurich, Switzerland
2 Institute of Physiology and Center for Integrative Human Physiology (ZIHP), University of Zurich,
Zurich, Switzerland
3 Horten Center for Patient-Oriented Research and Knowledge Transfer, University of Zurich, Zurich,
Switzerland
Abstract Objectives: Two distinct types of specific respiratory muscle training (RMT),
i.e. respiratory muscle strength (resistive/threshold) and endurance (hyper-
pnoea) training, have been established to improve the endurance performance of
healthy individuals. We performed a systematic review and meta-analysis in
order to determine the factors that affect the change in endurance perfor-
mance after RMT in healthy subjects.
Data sources: A computerized search was performed without language re-
striction in MEDLINE, EMBASE and CINAHL and references of original
studies and reviews were searched for further relevant studies.
Review methods: RMT studies with healthy individuals assessing changes in
endurance exercise performance by maximal tests (constant load, time trial,
intermittent incremental, conventional [non-intermittent] incremental) were
screened and abstracted by two independent investigators. A multiple linear
regression model was used to identify effects of subjects’ fitness, type of RMT
(inspiratory or combined inspiratory/expiratory muscle strength training,
respiratory muscle endurance training), type of exercise test, test duration and
type of sport (rowing, running, swimming, cycling) on changes in perfor-
mance after RMT. In addition, a meta-analysis was performed to determine
the effect of RMT on endurance performance in those studies providing the
necessary data.
Results: The multiple linear regression analysis including 46 original studies
revealed that less fit subjects benefit more from RMT than highly trained
athletes (6.0% per 10 mL
kg
-1
min
-1
decrease in maximal oxygen uptake,
95% confidence interval [CI] 1.8, 10.2%;p= 0.005) and that improvements do
not differ significantly between inspiratory muscle strength and respiratory
SYSTEMATIC REVIEW
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muscle endurance training (p =0.208), while combined inspiratory and expi-
ratory muscle strength training seems to be superior in improving perfor-
mance, although based on only 6 studies (+12.8% compared with inspiratory
muscle strength training, 95% CI 3.6, 22.0%;p= 0.006). Furthermore, con-
stant load tests (+16%,95% CI 10.2, 22.9%) and intermittent incremental tests
(+18.5%,95% CI 10.8, 26.3%) detect changes in endurance performance
better than conventional incremental tests (both p <0.001) with no difference
between time trials and conventional incremental tests (p =0.286). With in-
creasing test duration, improvements in performance are greater (+0.4%
per minute test duration, 95% CI 0.1, 0.6%;p=0.011) and the type of sport
does not influence the magnitude of improvements (all p > 0.05). The meta-
analysis, performed on eight controlled trials revealed a significant im-
provement in performance after RMT, which was detected by constant load
tests, time trials and intermittent incremental tests, but not by conventional
incremental tests.
Conclusion: RMT improves endurance exercise performance in healthy in-
dividuals with greater improvements in less fit individuals and in sports of
longer durations. The two most common types of RMT (inspiratory muscle
strength and respiratory muscle endurance training) do not differ signif-
icantly in their effect, while combined inspiratory/expiratory strength train-
ing might be superior. Improvements are similar between different types of
sports. Changes in performance can be detected by constant load tests, time
trials and intermittent incremental tests only. Thus, all types of RMT can be
used to improve exercise performance in healthy subjects but care must be
taken regarding the test used to investigate the improvements.
1. Introduction
Respiratory muscle fatigue is known to compro-
mise exercise performance in healthy subjects.
[1,2]
Evidence is emerging that fatiguing respiratory
muscles may affect exercise performance via the
so-called metaboreflex,
[3]
i.e. accumulation of
metabolites, such as lactic acid, in the respiratory
muscles activates group III and especially group
IV nerve afferen ts
[4-6]
that then trigger an increase
in sympathetic outflow from the brain causing
vasoconstriction in the (exercising) limbs.
[7-11]
This
consequently increases limb muscle fatigue during
exercise
[12,13]
and results in earlier exercise ter-
mination compared with conditions where res-
piratory muscle fatigue is prevented.
[14,15]
Respiratory muscle training (RM T) has been
shown to reduce the development of respiratory
muscle fatigue,
[16-18]
blood lactate concentration
during exercise
[18-21]
and sympathetic activation.
[12,22]
Therefore, a reduction or delay of the metabore-
flex
[3]
described earlier might be an important
mechanism for improving exercise performance
by RMT. Interestingly, however, of those studies
addressing the effects of specific RMT on exercise
performance in healthy subjects, only about two-
thirds report significant improvements. There-
fore, a detailed analysis of potential factors that
may contribute to the success or failure of RMT
is urgently needed. A brief overview of these
factors is given below.
First, study outcome may be related to study
design, considering that only about half of the
RMT studies included a sham-training group to
account for a possible placebo effect of RMT.
Second, subject selection might influence study
708 Illi et al.
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outcome, since the extent to which respiratory mus-
cles fatigue may differ, for example, with sub-
jects’ fitness level. Indeed, several studies showed
increased respiratory muscle endurance in physi-
cally trained compared with sedentary subjects.
[23-25]
However, when comparing subjects’ physical per-
formance relative to their maximal performance,
trained subjects worked at a higher percentage of
their maximum and performed more respiratory
muscle work,
[26]
which may theoretically neu-
tralize the effect of increased respiratory muscle
endurance on fatigue development. Only two
studies
[27,28]
investigated the difference in devel-
opment of respiratory muscle fatigue depending
on subjects’ fitness. These suggested that res-
piratory muscles indeed fatigue less in endurance
trained subjects compared with sedentary subjects
during exhaustive physical exercise.
[27,28]
This in-
dicates that less fit subjects would generally benefit
more from RMT than highly trained athletes.
Third, it is unclear whether the type of RMT might
influence the degree of improvement in exercise
performance. Currently, two distinct forms of RMT
are used in healthy subjects: respiratory muscle
strength training (RMST; also known as inspi-
ratory muscle [strength] training [IM(S)T], inspi-
ratory [flow] resistive loading [I(F)RL], resistive/
resistance respiratory muscle training [RRMT],
concurrent inspiratory and expiratory muscle
training [CRMT], or expiratory muscle training
[EMT]) and respiratory muscle endurance train-
ing (RMET; also referred to as ventilatory muscle
training [VMT], voluntary isocapnic hyperpnoea
[VIH] or endurance respiratory muscle training
[ERMT]). RMST is performed by breathing against
an external inspiratory and/or expiratory load.
This load consists either of a flow-dependent re-
sistance or of a pressure threshold that needs to
be overcome and sustained to generate flow. RMST
includes high-force, low-velocity contractions and
was shown to specifically increase respiratory
muscle strength, i.e. maximal pressure generation
capacity of the inspiratory and/or expiratory
muscles against a closed airway.
[29]
In contrast,
RMET is performed using normocapnic hyper-
pnoea. This training consists of low-force, high-
velocity contractions of inspiratory and expiratory
muscles, and results in improved respiratory en-
durance.
[29]
Whether strength or endurance train-
ing of the respiratory muscles is more effective in
terms of improving exercise performance, remains
unclear. From a physiological point of view, it
seems that training both inspiratory and expi-
ratory muscles would be most effective, since with
elevated breathing, inspiratory as well as expi-
ratory muscles are increasingly recruited. In fact,
it has been shown by objectively assessing chan-
ges in transdiaphragmatic and abdominal muscle
contractility after exercise that not only inspira-
tory
[30-33]
but also expiratory muscles
[16,34-36]
fa-
tigue during exhaustive high-intensity endurance
exercise. Therefore, a closer look at the effects of
different training regimens is needed. Fourth,
different studies use different types of exercise
testing, e.g. incremental tests (IT), constant load
tests (CLT) or time trials (TT) of different in-
tensities, to assess the effect of RMT on exercise
performance. Whether RMT is more likely to
result in positive effects during some types of per-
formance compared with others remains to be
verified. Considering the degree to which respira-
tory muscles fatigue after these different types of
tests, it could be argued that the effects of RMT
are less likely to be detected in ITs than in the
other types of tests. This assumption is based on
the results of Romer et al.,
[37]
who demonstrated
that the diaphragm of moderately fit subjects did
not fatigue during an incremental cycling test,
despite subjects reaching maximal exercise intensity.
This is surprising, since Johnson et al.
[30]
showed
that higher exercise intensities (oxygen consump-
tion [
.
VO
2
]at>85% maximal
.
VO
2
[
.
VO
2max
]) in-
crease the likelihood for diaphragmatic fatigue to
develop. It seems, therefore, that the duration for
which a given intensity is sustained is as im-
portant as the intensity itself, with respect to both
development of respiratory muscle fatigu e and a
possible benefit from RMT. Finally, the effect of
RMT on performance might differ depending on
the exercise modality used, e.g. rowing, running,
swimming or cycling, since respiratory muscles
are well known to realize more than just respira-
tory tasks, and these tasks differ between exercise
modalities. In rowing, for instance, respiratory
muscles need to combine the motion of the thorax
expanding and contracting with the sometimes
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opposing rowing stroke movement.
[38-40]
In
running, intra-abdominal pressure is increased,
which has been attributed to a protect ing func-
tion of the spine by the abdominal muscles.
[41]
Furthermore, the diaphragm has been shown to
be activated to increase intra-abdominal pressure
during movements of upper limbs, such as when
running.
[42,43]
Thus, when running, respiratory
muscles of the trunk also serve postural tasks.
During swimming and diving, the work of breath-
ing is increased due to the hydrostatic pressure
against which the thorax expands causing an
increase in end-expiratory lung volume, which in
turn leads to suboptimal length for tension de-
velopment of respiratory muscles.
[44]
In addition,
respiratory muscles are involved in propulsion.
Thus, subjects performing exercise modalities that
require additional work from respiratory muscles
might be more susceptible to respiratory muscle
fatigue.
[45]
Consequently, subjects performing these
exercise modalities might benefit the most from
RMT.
The aim of the present work was , therefore, to
assess the importance of the above factors on the
effect of RMT to improve exercise performance.
For this purpose, a systematic review was per-
formed in MEDLINE, EMBASE and CINAHL
(up to October 2011), without language restric-
tion, on all studies including an RMT interven-
tion and assessment of endurance performance as
an outcome variable, independent of the presence
or absence of a sham-training and/or no-training
control group. To specifically analyse the evidence
of a positive effect of RMT on exercise perfor-
mance, a meta-analysis including only controlled
studies was performed.
2. Methods
A systematic review and meta-analysis were
performed on original studies that assessed the
effect of RMT (RMST or RMET) on endurance
performance in healthy humans by use of at
least one of the following exercise tests: a CLT with
fixed exercise intensity and subjects performing to
exhaustion; a TT with either a fixed distance or a
fixed duration and with subjects being required to
row, run, swim, cycle, etc. as fast as possible or
to cover the largest possible distance; an inter-
mittent incremental test (IIT) with a stepwise
increase in exercise intensity including active re-
covery between steps and subjects performing to
exhaustion; or a conventional (non-intermittent)
IT with a stepwise increase in exercise intensity and
subjects performing to exhaustion, a test that is
frequently used to determine
.
VO
2max
and/or the
anaerobic threshold.
2.1 Search
A computerized search without language re-
striction was performed in MEDLINE, EMBASE
and CINAH L (up to 31 Octo ber 2011). The
search strategy included the following keywords:
‘respiratory muscle training’, ‘inspiratory muscle
training’, ‘expiratory muscle training’, ‘inspira-
tory training’, ‘expiratory training’, ‘hyperpnoea
training’, ‘hyperpnea training’, ‘respiratory muscle
endurance training’, ‘threshold training’, resistive
training’, ‘inspiratory loading’, ‘expiratory load-
ing’ and ‘resistive loading’ combined with ‘human’,
‘healthy’ and ‘not patien t’. Only published studies
were included in the analysis.
2.2 Selection
All studies perfor ming RMT in healthy sub-
jects and assessing endurance performance as a
main outcome were selected. RMT had to consist
of either RMST or RMET. One study
[46]
com-
bined RMST and RMET and was excluded due
to the interaction of combined strength and en-
durance training in skeletal muscles yielding dif-
ferent specific adaptations compared with training
in one modality alone.
[47]
Studies performing
unloaded breathing exercises, breathing therapy,
or similar, were not considered. First, all titles of
the primary search were screened for potentially
relevant articles. Of those, abstracts, reviews, short
reports, case reports, editorials and letters were
excluded. Original studies were excluded when
RMT was not performed, endurance performance
was not assessed, physical training was included
as an additional intervention and when exercise
tests were non-exhaustive. References of the in-
cluded studies and of the excluded reviews were
searched for further relevant studies.
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2.3 Quality Assessment
The quality of the selected RMT studies was
assessed using the following criteria.
[48,49]
(i) Ran-
domization: random allocation of the subjects to
intervention and sham-training or no-training
control group. If a trial was called ‘randomized
controlled’ but randomization was not descri bed,
it was considered to be a randomized trial (0 points
if not reported or not randomized, 1 point if re-
ported, 2 points if randomization procedure spe-
cified); (ii) Blinding: observer blinding to group
allocation of the subjects (0 points if not reported,
1 point if the observer was blinded); (iii) Alloca-
tion of concealment: person in charge of subject
recruitment was (at that time) unaware of po-
tential group allocation (0 points if not reported,
1 point if specified); (iv) Dropouts: information
about missing data (0 points if not reported, 1 point
if reported); (v) Intention-to-treat analysis: all
subjects initially considered for the study were
included and data was assessed (0 points if not
performed, 1 point if performed); (vi) Power cal-
culation: statistical power of the study (0 points if
not reported, 1 point if reported). Thus, a max-
imum of 7 points corresponding to 100% could be
reached.
2.4 Data Abstraction
Two investigators (IF, SKI) independently
abstracted the data. Inconsistencies were cross
checked, discussed with the third investigator
(CMS) and resolved by consensus.
2.5 Quantitative Data Synthesis
The main variable of interest was the change in
endurance performance reported or calculated as the
relative difference in test duration or in case of a
TT with fixed duration the relative change in maxi-
mal distance covered. Additional variables of inter-
est were (i) fitness level of the subjects (categorized
as follows: level 1 if
.
VO
2max
<40 mL
kg
-1
min
-1
,
level 2 if
.
VO
2max
4049 mL
kg
-1
min
-1
, level 3 if
.
VO
2max
5059 mL
kg
-1
min
-1
, level 4 if
.
VO
2max
60 mL
kg
-1
min
-1
;if
.
VO
2max
was not pro-
vided,
[50-59]
fitness level was estimated from [a]
endurance performance of subjects and [b] de-
scription of daily activities compared with sub-
jects in the other studies using the same exercise
modality); (ii) respiratory muscles that were trained,
i.e. inspiratory and/or expiratory muscles and type
of training, i.e. RMST or RMET (since specific
expiratory muscle training was investigated in
one single subgroup only,
[60]
it was excluded from
the analysis and three categories were generated
for the remaining types of training: RMST.IN
[inspiratory muscle strength training], RMST.I-
NEX [combined inspiratory and expiratory mus-
cle strength training] and RMET); (iii) type of
test, i.e. CLT, TT, IIT or IT; (iv) test duration
before RMT; and (v) exercise modality, i.e. row-
ing, run ning, swimming (including diving) or cy-
cling. Further potentially relevant variables, such
as training modalities (e.g. number of training
sessions, duration of a single training session,
training intensity, etc.), intensity of the physical
endurance test or subjective ratings of breath-
lessness and respiratory effort, were not included
in the multiple linear regression model in order to
prevent collinearity and/or as a consequence of
missing information in too many of the studies.
Collinearity means that two or more variables are
interchangeable, e.g. test duration and test in-
tensity are interchangeable because test duration
becomes shorter with a higher test intensity.
If both variables were included in the model at
the same time, this would mean a high degree of
multicollinearity and would give invalid estimates
for individual pred ictors.
Generalized estimating equations (GEE; with
exchangeable correlation structure) were fitted
to the dependent variable ‘change in endurance
performance’ in order to account for clustered
data. Independent variables in the multiple linear
regression model were fitness, type of training
(RMST.IN, RMST.INEX and RMET), type of
test (CLT, TT, IIT and IT), test duration and type
of sport (rowing, running, swimming and cy-
cling), including all RMT studies independent
of the presence or absence of a sham-training or
no-training control group. The multiple linear
regression model thus accounts for the influence
of the above confounders on changes in exer-
cise performance after RMT. The analyses were
performed with R 2.13.1 (statistical computing
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software).
[61]
Data from two studies were re-
ported in more than one publication.
[17,62-64]
In
this case, the study that provided more details of
the relevant data
[63,64]
was included in the ana-
lysis. Data from two tests were reported in two
studies.
[65,66]
This data appears only once in the
present analysis.
[66]
In three studies,
[55,67,68]
test
duration at baseline was not indicated nor could
it be calculated by use of the test protocol. There-
fore, these studies were excluded from the re-
gression model.
Furthermore, a meta-analysis was performed
on the main outcome of those studies that included
a sham-training or no-training contro l group, and
that reported the relative change and standard
deviation in exercise performance, such that the
overall difference in exercise performance in-
cluding 95% confidence intervals (CIs) between
RMT and sham/no-training control group could
be calculated. Additionally, subgroup analysis
for the different exercise tests was performed.
Heterogeneity of the studies was assessed by cal-
culating the I
2
-statistics, which are known to be
independent of the number of studies included in
the meta-analysis, and thus preferable compared
with the Cochrane’s chi-squared or Q test.
[69]
A
value of I
2
>50% was considered as evidence for
heterogeneity.
[70]
A random effects model was chosen
for all tests, since substantial heterogeneit y was
expected due to differences between fitness level,
type of RMT, type and duration of test and ex-
ercise modality. As relative improvements in TTs
are generally much smaller compared with those
in CLTs, mean relative differences in exercise
performance were standardized based on their
standard deviations. A potential publication bias
was assessed by use of a funnel plot. These analyses
were performed with Review Manager (RevMan,
Version 5.1, The Nordic Cochrane Centre,
The Cochrane Collaboration, 2011, Copenhagen,
Denmark). In both the multiple linear regression
model and the meta-analysis, a p-value of 0.05
was considered significant.
In those studies that did not report the stan-
dard deviations of relative changes in endurance
performance, the relative differences between the
RMT and sham/no-training control group are
presented without 95% CIs. If this difference was
not given, it was calculated from the difference in
mean absolute values before and after RMT.
3. Results
3.1 Trial Flow and Study Characteristics
7385 citations were identified of which 236
potentially relevant articles remained for further
evaluation (figure 1). Finally, 49 studies were se-
lected.
[16,20,21,38,39,50-60,63-68,71-97]
Of these, 28 (57%)
were randomized controlled trials, 6 (12%)werecon-
trolled trials, and 15 (31%) were non-controlled
trials. Further characteristics of the studies are
given in supplemental table I of the online Sup-
plemental Digital Content (SDC) [http://links.
adisonline.com/SMZ/A9]. Note that three
[55,67,68]
of the 49 studies were excluded from the multiple
regression analysis due to missing test durations.
Of these, the study by Lomax et al.
[55]
was included
in the meta-analysis and the study by Chatham
et al.
[67]
was included in the fourth figure (see section
3.4) only. Methodological quality scored between
14% and 86% (median 29%, i.e. 2 of maximum
7 points; see supplemental table II of the SDC).
Study quality did not correlate with the main out-
come, i.e. with the relative change in performance.
3.2 Study Design: Presence/Absence and
Type of Control Group
Thirteen studies (27%) included a no-training
control group while 21 studies (43%) had a sham-
training group. Seventy-five percent of the non-
controlled studies showed an improvement in
exercise perfor mance after RMT. In studies with
sham-training or no-training control groups, im-
provements for the RMT group were seen in 71%
and 54%, respectively. In those studies that com-
pared improvements of RMT and no-training
control groups, improvements in the RMT group
were significantly greater in 75% of studies with
no-training control and in 69% of studies with
sham-training control.
3.3 Linear Regression Model
Table I dep icts the linear regression model. The
model revealed that (i) less fit subjects benefit more
from RMT than fitter subjects; (ii) effects of RMET
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and RMST.IN are similar, while RMST.INEX
seemstobesuperiortoRMST.INandRMET;
(iii) improvements in performance are greater in
CLTsandIITsthaninITs,withnosignificantdif-
ference between TTs and ITs; (iv) greater improve-
ments are seen with increasing test duration; and (v)
improvements are independent of exercise modality.
3.4 Meta-Analysis
RMT results in a significant increase in exercise
performance (figure 2, standardized mean differ-
ence [SMD] 1.11, 95% CI 0.61, 1.61; p < 0.001),
although with moderate heterogeneity (I
2
= 71%).
Subgroup analysis of different tests revealed sig-
nificant improvements in exercise performance
when assessed by a CLT (SMD 0.66, 95 % CI 0.20,
1.12; p =0.005), a TT (SMD 1.85, 95% CI 0.88,
2.82; p < 0.001) or by an IIT (SMD 2.96, 95% CI
1.12, 4.80; p =0.002), whereas no significant im-
provement in exercise performance was detected
when assessed by an IT (SMD 0.30, 95% CI -0.20,
0.79; p = 0.30). Furthermore, a significant difference
between groups was found (p = 0.003) favouring TT
236 Potentially relevant articles
194 Original studies retrieved for
more detailed evaluation
42 Articles excluded:
abstracts (n = 8), reviews (n = 22), short
reports (n = 1), case reports (n = 1),
editorials (n = 4), letters (n = 6)
138 Studies excluded:
no RMT (n = 84)
no exercise (n = 43)
intervention = RMT + additional
physical training (n = 5)
submaximal exercise test only (n = 6)
46 Studies included in
regression analysis
41 Studies excluded:
non-controlled studies (n = 15)
missing relevant data (n = 26)
3 Studies excluded:
no data for test duration shown
(n = 3)
8 Controlled studies
included in meta-analysis
7 Studies excluded:
no data for change in performance
shown (n = 4)
duplicate publications (n = 2)
intervention = RMST + RMET (n = 1)
56 RMT studies assessing
exercise performance with a
maximal exercise test included
Fig. 1. Flow diagram of the studies excluded from and included in the linear regression model and/or the meta-analysis. RMET =respiratory
muscle endurance training; RMST = respiratory muscle strength training; RMT = respiratory muscle training.
Respiratory Muscle Training in Healthy Individuals 713
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and IIT over CLT and IT (individual p-values not
shown), although with substantial heterogeneity
(I
2
= 78.3%). Subgroup analys is showed evidence
for low heterogeneity in CLT and IT (I
2
= 0% and
18%, respectively) but high heterogeneity in TT
(I
2
= 77%). Heterogeneity for IIT could not be
calculated as only one study was included in the
meta-analysis. Figure 3 shows a funnel plot of those
studies that were included in the meta-analysis.
Figure 4 shows the overall mean difference of
the relative change in exercise performance for all
controlled studies. The overall improvement for
the RMT group over the sham-training or no-
training control group was 11%, while subgroup
differences were 21% for CLT, 2% for TT, 13%
for IIT and 7% for IT (2% without the studies by
Enright et al.
[50,51]
). Thes e results are in agree-
ment with those of the controlled studies included
in the meta-analysis, i.e. RMT effects are seen in
CLTs, IITs and TTs.
4. Discussion
The key finding of this analysis is that RMT
improves performance in healthy subject s, inde-
pendent of the type of RMT and exercise mod-
ality. Less fit individuals seem to benefit more
from RMT than highly trained athletes, and im-
provements are greater with longer exercise du-
rations. Improvements are significant when the
effect of RMT is tested in CLTs, TTs and IITs,
while none are seen in ITs, commonly used to
assess
.
VO
2max
or anaerobic threshold.
4.1 Study Design: Presence/Absence and
Type of Control Group
It could be assumed that study outcome may
be related to study design, since only 43% of RMT
studies included a sham-training group to account
for a possible placebo effect of RMT. However, a
closer look reveals that the presence and type of
control group do not influen ce outcome. When
considering differences betweenRMTandcontrol
groups, 75% of studies including a no-training
control group and 69% of placebo-controlled
studies showed a positive out come for RMT (i.e.
performance improvements for the RMT groups
significantly exceeded those for the control groups),
similar to the 75% positive outcome in studies
without any controls. Thus, the presence or ab-
sence and type of control group did not affect the
outcome regarding performance improvements
for RMT studies in healthy subjects.
Likely reasons for the lack of improvement in
exercise performance after RMT in some studies
include the use of only an IT to evaluate the ef-
fects of RMT on endurance performance,
[73,82,86,94]
low power of the studi es,
[78,89]
lack of recovery
time for respiratory muscles prior to the en-
durance exerci se test,
[38,46,76,78,96,97]
very high-
intensity exercise,
[20,38,58,78,89]
a highly trained
group of subjects
[58,78,96,97]
or an increased res-
piratory drive with concomit antly increased work
of breathing in some subjects after RMET.
[16,96]
4.2 Effect of Subjects’ Fitness on
Improvements in Exercise Performance
The multiple linear regression analysis showed
that less fit subjects benefit more from RMT
than highly trained athletes. This finding is in
accordance with the initial hypothesis suggesting
that untrained subjects might benefit more from
Table I. Multiple linear regression model
Estimate SE 95% CI p-Value
Intercept 17.8 8.8 0.6, 35.1 0.043
Fitness -6.0 2.1 -10.2, -1.8 0.005
RMST.INEX vs RMST.IN
a
12.8 4.7 3.6, 22.0 0.006
RMET vs RMST.IN
a
-4.7 3.7 -12.0, 2.6 0.208
CLT vs IT 16.5 3.2 10.2, 22.8 0.000
TT vs IT -3.7 3.4 -10.4, 3.1 0.286
IIT vs IT 18.5 3.9 10.8, 26.3 0.000
Test duration 0.4 0.1 0.1, 0.6 0.011
Rowing vs cycling 1.9 4.9 -7.7, 11.4 0.701
Running vs cycling -4.6 5.3 -14.9, 5.8 0.390
Swimming vs cycling 5.2 5.5 -5.6, 16.1 0.347
a When RMET was chosen as the reference group, the estimate
for the comparison between RMST.INEX and RMET (17.5,
SE 4.8, 95% CI 8.2, 26.9) was also significant (p = 0.000).
CI =confidence interval; CLT =constant load test; IIT =intermittent
incremental test; IT = conventional (non-intermittent) incremental test;
RMET = respiratory muscle endurance training; RMST.IN = inspiratory
muscle strength training; RMST.INEX = inspiratory and expiratory muscle
strength training; SE = standard error; TT =time trial.
714 Illi et al.
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RMT, since respiratory muscles of less fit subjects
were shown to fatigue more during exhaustive
endurance performance.
[27,28]
However, although
less fit subjects have a higher potential to increase
their physical endurance performance compared
with highly trained athletes,
[98-101]
respiratory
muscle performance seems to improve to a sim-
ilar extent with a ll levels of fitness. Also, when
analysing improvements in maximal inspiratory
mouth pressure (MIP), maximal expiratory mouth
pressure (MEP) or respi ratory muscle endurance
separately for the different types of training, no
effect of fitness could be observed (data not shown).
On the other hand, it might be argued that
greater improvements in performance are asso-
ciated with older age rather than lower fitness,
Study or test
Constant load tests
Subtotal
Time trials
Subtotal
Subtotal
Subtotal
Intermittent incremental test
Incremental tests
Total
McMahon et al.
[87]
1.18 [0.18, 2.17]
1.04 [0.03, 2.10]
0.45 [1.44, 0.55]
3.52 [1.81, 5.24]
3.12 [1.53, 4.70]
2.91 [1.26, 4.56]
2.83 [1.21, 4.45]
1.61 [0.35, 2.87]
2.96 [1.12, 4.80]
0.78 [0.13, 1.70]
0.51 [0.24, 1.27]
0.13 [0.75, 1.01]
0.51 [1.59, 0.57]
–4 –2 0
Favours sham/control
Favours RMT
24
1.20 [0.11, 2.29]
0.91 [0.13, 1.70]
0.25 [0.63, 1.14]
0.19 [0.88, 1.25]
0.66 [0.20, 1.12]
1.85 [0.88, 2.82]
2.96 [1.12, 4.80]
0.30 [0.20, 0.79]
1.11 [0.61, 1.61]
SMD
IV, random, 95% CI
SMD
IV, random, [95% CI]
McMahon et al.
[87]
Stuessi et al.
[64]
Verges et al.
[16]
Verges et al.
[96]
Stuessi et al.
[64]
Verges et al.
[16]
Kilding et al.
[53]
100 m
Romer et al.
[63]
Volianitis et al.
[39]
Lomax et al.
[55]
Verges et al.
[96]
200 m
400 m
20 km
40 km
5000 m
6 min, 4 wk
6 min, 11 wk
Fig. 2. Effect of respiratory muscle training on exercise performance in constant load tests, time trials, intermittent incremental test, and
conventional (non-intermittent) incremental tests. Only those studies providing the necessary information are included in this forest plot.
CI =confidence interval; IV = inverse variance; random = random effects model; RMT =respiratory muscle training; sham/control = sham-
training/no-training control; SMD =standardized mean difference.
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since
.
VO
2max
is known to decrease with age.
[102]
However, separate analyses showed that the re-
lative improvement in exercise performance was
negatively correlated with the level of fitness
(r =-0.440; p < 0.001), while it was not correlated
with age (r =-0.018; p =0.882). Thus, it seems
that the level of fitness is more important than
age in affecting the amount of improvement in
performance after RMT.
4.3 Influence of the Type of RMT on
Improvements in Exercise Performance
The multiple regression analysis revealed that
RMST.IN and RMET did not differ in their ef-
fect on improving exercise performance. This re-
sult seems astonishing, since the degree of fatigue
developing during exhaustive exercise was shown
to be similar in inspiratory and expiratory mus-
cles
[16,30-36]
and both of these muscle groups
[7,10]
were shown to elicit the metaboreflex that is known
to impair exercise performance.
[14]
Thus, one
would assume that training both muscle groups,
as with RMET, would yield a greater effect than
training inspiratory muscles alone, such as during
RMST.IN.
Thus, the question arises: why would increased
inspiratory muscle strength be advantageous for
exercise hyperpnoea? Despite exercise hyperpnoea
being characterized by high flows, it is known
that inspiratory rib-cage muscles produce the pres-
sures needed to expand the rib cage and thereby
let the diaphragm act as the main flow generator.
[103]
Consequently, rib-cage muscles fatigue during
high-flow tasks,
[104]
although to a lesser extent
than with high resistances.
[105]
Thus, it seems
likely that RMST.IN provides a larger training
stimulus to inspiratory muscles than RMET and
that more effectively trained inspiratory muscles,
as with RMST.IN, may be superior in preventing
or delaying the development of inspiratory rib-
cage muscle fatigue, compared with RMET. This
per se would translate into a greater impr ovement
in exercise performance with RMST.IN than
with RMET of inspiratory muscles only. It
has, however, been shown that RMET also trains
expiratory rib-cage and abdominal muscles,
in addition to the inspiratory muscles, which is
substantiated in a smaller degree of expiratory
muscle fatigue during exercise after this type
of training.
[16]
Therefore, an explanation for
the similar improvements in performance with
RMST.IN and RMET might be that, on the one
hand, inspiratory muscles were trained more ef-
fectively with RMST.IN than with RMET, and
on the other hand, the combination of ‘less ef-
fective’ inspiratory muscle train ing with expira-
tory muscle training during RMET results in the
same net effect with respect to improvements in
exercise performance.
The need for train ing the expiratory in addi-
tion to the inspiratory muscles on the one hand
and the potential superiority of respiratory muscle
strength over endurance training to improve
exercise performance, on the other hand, would
also be supported by the model showing that the
combination of both inspiratory as well as ex-
piratory muscle strength training, i.e. RMST.
INEX, improved exercise performance more
than RMST.IN or RMET. It should, however, be
pointed out that so far only three research groups
(six studies) used RMST.INEX and although
0
0.2
0.4
0.6
SE (SMD)
0.8
1.0
4 20
SMD
24
CLT
TT
IIT
IT
Fig. 3. Funnel plot of the studies included in the meta-analysis.
CLT = constant load test; IIT = intermittent incremental test; IT =
conventional (non-intermittent) incremental test; SE = standard error;
SMD =standardized mean difference; TT =time trial.
716 Illi et al.
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Constant load tests
Fairbarn et al.
[78]
Holm et al.
[83]
McMahon et al.
[87]
Morgan et al.
[89]
Stuessi et al.
[64]
Verges et al.
[16]
Verges et al.
[96]
Wylegala et al.
[66]
Bailey et al.
[72]
Gething et al.
[79]
Johnson et al.
[52]
Aznar-Lain et al.
[71]
Downey et al.
[76]
Edwards and Cooke
[77]
Mickleborough et al.
[88]
Wylegala et al.
[66]
Holm et al.
[83]
Leddy et al.
[85]
Romer et al.
[63]
Volianitis et al.
[39]
Kwok and Jones
[84]
Hanel and Secher
[81]
Romer et al.
[20]
Kilding et al.
[53]
Wells et al.
[58]
Lomax et al.
[55]
Nicks et al.
[56]
Tong et al.
[57]
Holm et al.
[83]
Markov et al.
[86]
McMahon et al.
[87]
Stuessi et al.
[64]
Verges et al.
[16]
Verges et al.
[96]
Belman and Gaesser
[73]
Enright and Unnithan
[50]
Enright et al.
[51]
Romer et al.
[63]
Chatham et al.
[67]
Hart et al.
[82]
Romer et al.
[20]
Aznar-Lain et al.
[71]
Sperlich et al.
[94]
RMET
RMST.IN
RMST.INEX
Subtotal
Time trials
RMET
RMST.IN
RMST.INEX
Subtotal
Intermittent incremental tests
Subtotal
Incremental tests
RMET
RMST.IN
Subtotal
Total
Cycle
Cycle
Run
Run
RMST.IN Run
Swim
Swim
Run
Row
Cycle
Cycle
Swim
Run
Cycle
Swim
Surface
Underwater
Maximal
Severe
Ex 1
Ex 2
Ex 3
Surface
Underwater
20 km
Johnson et al.
[52]
40 km
5000 m
6 min, 4 wk
Riganas et al.
[38]
6 min, 11 wk
100 m
200 m
400 m
80% SMIP
0% 20% 40% 60%
60% SMIP
40% SMIP
Cycle
Run
Fig. 4. Mean difference in the effect of respiratory muscle training on exercise performance between intervention and sham-training/
no-training control groups. Dark grey circles: average mean difference of each type of exercise test. Medium grey circles: tests also included in
the forest plot of figure 2. Light grey circles: tests not included in the meta-analysis because data to calculate the confidence interval was not
provided. The size of the circles represents the number of subjects included in the study. RMET = respiratory muscle endurance training;
RMST.IN =inspiratory muscle strength training; RMST.INEX = inspiratory and expiratory muscle strength training; SMIP = sustained maximal
inspiratory pressure (i.e. maximal pressure generation capacity from residual volume to total lung capacity).
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the model accounted for differences in fitness,
type of testing and sports one might need to
consider that subjects in these studies were
slightly less fit than those performing RMST.IN
and RMET, and evidence for physical impr ove-
ments ca me from one single research group (four
studies) testing with CLTs only (known to yield
greater improvements). Final proof of a potential
difference between RMST.INEX versus RMST.IN
and RMET can therefore only be provided when
all three types of training are test ed in the same
study having similar groups of subjects and sim-
ilar performance tests. For example, a direct
comparison of RMST.IN and RMET in one
single study showed that the effects of RMET
were larger than those of RMST.IN, with respect
to the reduction in blood lactate concentration
and perception of respiratory sensations.
[18]
Thus, it
also remains to be tested whether alternating
RMST and RMET yield even great er improve-
ments in performance than one type of RMT
alone.
4.4 Effect of the Type of Exercise Test and
Test Duration on the Improvement in
Exercise Performance
The multiple regression analysis showed that
improvements in exercise performance after RMT
were significantly greater when tested with CLTs
or IITs compared with ITs, with no difference
between TTs and ITs. The meta-analysis of con-
trolled studies revealed no significant effect of
RMT when tested with ITs, while improvements
in CLTs, TTs and in the IIT were all significant.
The fact that RMT does not seem to affect IT
performance is consistent with the notion that the
duration a subject spends exercising above the
threshold of 85 %
.
VO
2max
, the exercise intensity
where respiratory muscles are most likel y to fa-
tigue,
[30]
is too short to elicit respiratory muscle
fatigue.
[37]
This is also supported by the finding
that improvements in performance after RMT
are great er with longer test duration (+0.4% per
minute test duration, table I). Furthermore, of
22 studies assessing
.
VO
2max
before and after
RMT, all but two studies found no change in
.
VO
2max
. Leddy et al.
[85]
observed a signi ficant
increase, while Verges et al.
[96]
observed a signif-
icant decrease in
.
VO
2max
.
Interestingly, half of those tests that reported
exercise intensity (n = 40) were performed below
the threshold of 85%
.
VO
2max
, maximal workload
(W
max
) or maximal velocity (v
max
) the average
of the forty tests being 80%
.
VO
2max
,81% W
max
or
98% v
max
. All but two of the 20 tests that were
performed below 85% showed an improvement in
exercise performance after RMT. In contrast,
only nine of the 20 tests that were performed above
85% showed increased performance. However,
subjects performing above 85%
.
VO
2max
,W
max
or
v
max
were fitter than those performing below this
threshold (fitness level of 3.1 and 2.1, respective-
ly), which could partly explain this finding and
illustrates the importance of using a model that
accounts for confounders. Nevertheless, if res-
piratory muscles do not fatigue below the sug-
gested threshold of 85%
.
VO
2max
, this would mean
that a reduction in respiratory muscle fatigue
could not be the only mechani sm to increase en-
durance performance after RMT.
It is known, for example, that in CLTs, psy-
chological factors such as motivation or boredom
may play an important role in determining the
point of exhaustion.
[106]
Accordingly, after an
extended period of RMT, motivation to withstand
task failure in a CLT might be higher. However,
in studies using CLTs at intensities below the
threshold and including a sham-training group,
improvements in the RMT groups exceeded those
of the sham-training groups
[66,71,79,85,88]
with only
one exception.
[83]
Thus, again, motivation cannot
be the only reason for improvements in CLT
performance after RMT. Another possible ex-
planation for improved endurance performance
after RMT is a reduced perception of respiratory
exertion and/or breathlessness. Of the 15 studies
testing with a CLT below the 85% threshold, only
three specified changes in respiratory sensations,
two
[79,88]
of them reported a significant decrease
while one
[83]
did not.
While the regression model, which accounted
for confounders such as test duration, subjects’
fitness, type of training and type of sports did not
find TTs to be more sensitive than ITs in show-
ing improvements after RMT, the meta-analysis
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showed greater standardized mean differences in
TTs and in the IIT compared with CLTs and ITs
meaning that TTs would detect changes better
than CLTs and ITs. This seems confusing at first;
however, it should be considered that the model is
based on all RMT studies, while the meta-analysis
is based only on those studies that provided the
necessary data. A comparison of average changes
of the studies included in the regression model
and in the meta-analysis shows that the average
change in test duration in studies included in the
regression model was significantly larger (+15%)
than that of the studies included in the meta-
analysis (+5%;p= 0.002). Howeve r, the average
fitness of subjects included in the regression model
tended to be lower (2.6) than fitness of subjects
included in the meta-analysis (3.1; p = 0.065),
which might possibly explain the greater average
improvement in performance of subjects included
in the regression model. Thus, it seems that the
studies included in the meta-analysis despite a
similar number of positive outcomes are not
fully representative of all of the RMT studies in-
cluded in the regres sion model. Also, the studies
by Enright et al.
[50,51]
might contribute to the
discrepancy between model and meta-analysis.
These authors used a protocol resulting in much
shorter test durations (4.44.5 minutes) than the
suggested 812 minutes required for
.
VO
2max
de-
termination.
[107]
Improvements after RMT
[50,51]
were even greater (approximately 25%) than
those reported for physical endurance training
(approximately 10%
[108]
), which raises questions
regarding the validity of this protocol. Without
the two studies by Enright et al.,
[50,51]
the overall
difference between improvements in IT performance
after the RMT and sham/no-training period is
2% equal to that for TTs. Thus, the relatively
small improvements generally seen in TTs, al-
though consistent, might be too small to exceed
the changes found in ITs. However, it must be
noted that these small improvements in TT per-
formance are highly relevant. For example, mean
improvements in the 40 TTs would result in 40 m
or five skiff lengths in a 2 km rowing regatta,
100 m in a 2 km running race, 1.2 m in a 200 m
swimming competition and 1 km in a 30 km cy-
cling race.
The fact that improvements in exercise per-
formance after RMT were significantly greater
(19%) also in IITs compared with ITs, suggests
that amateur and professional athletes perform-
ing intermittent sports, such as football, soccer,
basketball, team handball, etc. might benefit
from RMT similar to subjects performing en-
durance-type sports. This is further supported by
one study that showed a reduction in recovery
duration between sprints, which was in part at-
tributed to a decreased perception of respiratory
effort.
[20]
4.5 Effects of RMT in Different Types of Sports
Although physiological evidence would sug-
gest that RMT might be more effective in sports
where respiratory muscles are subjected to increased
respiratory work
[44]
(swimming) and/or increased
non-respiratory work, i.e. postural
[41-43]
(run-
ning) or moving
[38-40]
(rowing) tasks, the model
did not reveal any significant difference between
improvements in the different types of sports.
Thus, one could assume that respiratory muscles
involved in additional tasks resulting in higher
respiratory muscle work are sufficiently trained,
such that the likelihood to fatigue is similar to
that during, for example, cycling. Supporting this
assumption is the following interesting observa-
tion: for the studies included in the present review
that give respiratory muscle strength data and
include subjects with a fitness level of 3 or 4,
baseline values of MIP and especially MEP ex-
pressed as a percentage of predicted values
[109]
are lowest in cycling and increase with rowing,
running and swimming (data not shown).
4.6 Limitations
Several variables of inter est were not included
in the analysis. For example, duration of the
training period or training intensity might also
influence changes in endurance performance al-
though these variables were quite similar within
RMST and within RMET studies. Therefore, only
the type of training was included in the multiple
linear regression model, while factors describing
training regimens were omitted to prevent colli-
nearity. Furthermore, exercise intensity is believed
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to play a crucial role with respect to the devel-
opment of respiratory muscle fatigue and, there-
fore, with respect to a possible benefit from RMT.
Intensity of the exercise tests was not, however,
included in the model. Since too many studies did
not provide detailed information on exercise in-
tensity (n = 24), the inclusion of this variable
would have led to the exclusion of too many
studies from the regression model. Furthermore,
since only exhaustive tests were included in the
model, test duration and intensity would have led
to collinearity, with the consequence of excluding
one or the other variable from the model. The
same holds true for ratings of perceived breath-
lessness or respiratory effort, which have been
shown to be lower after RMT in some stud-
ies
[16,20,39,53,55,59,60,63,67,72,73,76,79,88,96,110]
but not
in others.
[38,56,58,60,83,97,111]
As only 21 studies
provided this information, the inclusion of these
variables in the linear regression model would
have led to the exclusion of too many studies.
Therefore, the variables ‘intensity’ and ‘respira-
tory sensations’ were omitted, despite their po-
tential to explain possible changes after RMT.
These variables might, however, be included in
the intercept. The significance of the intercept
indicates that additional factors not included in
the model play a role in determining impr ove-
ments in exercise performance.
A further consideration is that the funnel plot
shows a potential publication bias. In general,
without publication bias, studies would be evenly
distributed around the mean, in the form of a
triangle. Studies with small standard errors (often
those with many subjects included) are found at
the top of the triangle close to the mean. Studies
with large standard errors (frequently smaller
studies) are found at the bottom of the triangle,
with some of them having a greater distance to
the mean. In the present meta-analysis, studies at
the bottom left of the triangle are missing. This
could mean that smaller studies with negative out-
come were not published in addition to the pos-
sibility that no such studies were ever conducted.
If those small studies with a negative outcome
were present in the funnel plot, this would mean
that the effect of RMT would be smaller than
shown in the present analysis.
5. Conclusions
This is the first study to systematically assess
the effect of different types of RMT used to im-
prove exercise performance in healthy subjects. It
clearly shows that RMT significantly improves
endurance performance, independent of the type
of RMT or the type of sport. No difference was
found between the effects of the two most com-
monly used respiratory muscle training modalities,
RMST.IN and RMET, while RMST.INEX
seemed to be superior. Less fit individuals benefit
more from RMT than highly trained athletes, and
improvements are greater with longer exercise
durations even at intensities lower than the pos-
tulated threshold for development of respiratory
muscle fatigue (85%
.
VO
2max
). This emphasizes
the importance to report changes in respiratory
sensations after RMT so that this variable can be
included in future regression models as well.
Furthermore, when assessing the effect of RMT,
care must be taken regarding the choice of the test,
since effects are not seen in ITs that are commonly
used to assess
.
VO
2max
or anaerobic threshold.
Also, more well controlled studies are needed to
prove a superiority of RMST.INEX over the
commonly used types of RMT to confirm the
positive results observed in the few studies using
IITs, and to investigate a possible additional
benefit from alternating RMET and RMST.
Acknowledgements
The authors would like to thank Christoph Bra
¨
ndle and
Dr. Alexander Akhmedov for translating the potentially relevant
Japanese and Russian papers, respectively, Dr. Ruth Briggs
for English editing, as well as the Swiss Federal Office of Sport
(grant no. 11-11) and the Swiss National Science Foundation
(grant no. 3200B0-116777) for providing financial support.
The authors have no conflicts of interest to declare that are
directly relevant to the content of this article.
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Correspondence: Prof. Dr. Christina M. Spengler, Exercise
Physiology, Institute of Human Movement Sciences,
University and ETH Zurich, Winterthurerstrasse 190, 8057
Zurich, Switzerland.
E-mail: christina.spengler@hest.ethz.ch
724 Illi et al.
Adis ª 2012 Springer International Publishing AG. All rights reserved. Sports Med 2012; 42 (8)
... Nowadays, endurance athletes worldwide use respiratory muscle training (RMT) to improve exercise performance. The benefits of the RMT are well documented in the literature and this type of training is known to increase performance in endurance exercises such as cycling [1][2][3][4][5], running [4][5][6][7] and rowing [4,8] or acyclic sports [9][10][11]. The underlying mechanisms postulated to explain improved exercise performance after a period of RMT are varied. ...
... Nowadays, endurance athletes worldwide use respiratory muscle training (RMT) to improve exercise performance. The benefits of the RMT are well documented in the literature and this type of training is known to increase performance in endurance exercises such as cycling [1][2][3][4][5], running [4][5][6][7] and rowing [4,8] or acyclic sports [9][10][11]. The underlying mechanisms postulated to explain improved exercise performance after a period of RMT are varied. ...
... Nowadays, endurance athletes worldwide use respiratory muscle training (RMT) to improve exercise performance. The benefits of the RMT are well documented in the literature and this type of training is known to increase performance in endurance exercises such as cycling [1][2][3][4][5], running [4][5][6][7] and rowing [4,8] or acyclic sports [9][10][11]. The underlying mechanisms postulated to explain improved exercise performance after a period of RMT are varied. ...
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Different studies have observed that respiratory muscle training (RMT) improve the endurance and strength of the respiratory muscles, having a positive impact on performance of endurance sports. Nevertheless, it remains to be clarified how to improve the efficiency of such training. The objective of this systematic review was to evaluate the acute physiological responses produced by training the respiratory muscles during exercise with flow resistive devices because such information may support us improve the efficiency of this type of training. A search in the Medline, Science Direct, Web of Science and Scopus databases was conducted, following the PRISMA guidelines. The methodological quality of the articles was assessed using the PEDro scale. Nineteen studies met the inclusion criteria and a total of 212 subjects were included in the studies. The RMT method used in all studies was flow resistive loading, whereas the constant load exercise was the most common type of exercise among the studies. The results obtained seem to indicate that the use of this type of training during exercise reduces the performance, the lactate (La⁻) values and the ventilation, whereas the end – tidal partial pressure of carbon dioxide (PCO2) is increased.
... Further, given that ventilation is higher when walking/running uphill compared to exercise on level ground (Pokan et al. 1995), the ventilatory system might become even more limiting under these conditions. Since RMET has been shown to improve respiratory muscle strength and endurance, exercise performance and ratings of perceived breathlessness and respiratory exertion during exercise (HajGhanbari et al. 2013;Illi et al. 2012), the secondary aim of this study was to evaluate the effects of RMET on uphill exercise performance in healthy active elderly. We hypothesised that RMET would increase endurance performance and decrease the sensation of breathlessness and respiratory exertion during exercise. ...
... Although also IT performance increased in the RMET group, there was no difference when compared to PLA. The finding of an improved CLT performance without changes in IT performance is consistent with previous literature (Illi et al. 2012). The absence of RMET effects on IT performance can likely be explained by the fact that exercise duration above an intensity of 85% VȮ 2max (a threshold for respiratory muscle fatigue development proposed by Johnson et al. 1993) is too short in the IT to elicit significant respiratory muscle fatigue (Illi et al. 2012). ...
... The finding of an improved CLT performance without changes in IT performance is consistent with previous literature (Illi et al. 2012). The absence of RMET effects on IT performance can likely be explained by the fact that exercise duration above an intensity of 85% VȮ 2max (a threshold for respiratory muscle fatigue development proposed by Johnson et al. 1993) is too short in the IT to elicit significant respiratory muscle fatigue (Illi et al. 2012). On the other hand, other respiratory muscle training (RMT) studies fail to show improvements in constant-work exercise tests that exceed placebo and/or learning effects (Sonetti et al. 2001). ...
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Purpose Ageing is associated with increased blood pressure (BP), reduced sleep, decreased pulmonary function and exercise capacity. The main purpose of this study was to test whether respiratory muscle endurance training (RMET) improves these parameters. Methods Twenty-four active normotensive and prehypertensive participants (age: 65.8 years) were randomized and balanced to receive either RMET ( N = 12) or placebo (PLA, N = 12). RMET consisted of 30 min of volitional normocapnic hyperpnea at 60% of maximal voluntary ventilation while PLA consisted of 1 inhalation day ⁻¹ of a lactose powder. Both interventions were performed on 4–5 days week ⁻¹ for 4–5 weeks. Before and after the intervention, resting BP, pulmonary function, time to exhaustion in an incremental respiratory muscle test (incRMET), an incremental treadmill test (IT) and in a constant-load treadmill test (CLT) at 80% of peak oxygen consumption, balance, sleep at home, and body composition were assessed. Data was analyzed with 2 × 2 mixed ANOVAs. Results Compared to PLA, there was no change in resting BP (independent of initial resting BP), pulmonary function, IT performance, sleep, body composition or balance (all p > 0.05). Performance significantly increased in the incRMET (+ 6.3 min) and the CLT (+ 3.2 min), resulting in significant interaction effects ( p < 0.05). Conclusion In the elderly population, RMET might be used to improve respiratory and whole body endurance performance either as an adjunct to physical exercise training or as a replacement thereof for people not being able to intensively exercise even if no change in BP or sleep may be expected.
... In human athletes there is a training-induced adaptation of the respiratory muscles 1,2 with an increase in the inspiratory muscle strength following both non-specific strength training and specific inspiratory muscle training (IMT). [1][2][3] IMT has been used as an ergogenic aid in healthy human subjects, with investigations demonstrating an improvement in athletic performance 4 and a change in a range of physiological parameters 5,6 but most importantly attenuation of inspiratory muscle fatigue. 7 In addition, there is a correlation between diaphragm thickness and inspiratory muscle strength in people, [8][9][10] with an increase in diaphragm thickness and inspiratory muscle strength (measured by maximal inspiratory pressure) following IMT. ...
... The application of IMT is used in human athletes to strengthen the respiratory muscles, delaying the activation of the respiratory muscle metaboreflex, 3 and optimising athletic performance in sports where diaphragm fatigue is performance limitating. 3,4,24 In addition, in human subjects, IMT reduces the perception of respiratory and limb effort. 3,24 The horses' respiratory system is thought to be the limiting factor which determines athletic performance. ...
... Although the results of the linked investigation did not show an increase in the size of the muscles of the upper airway with IMT, previous studies have indicated the potential use of IMT for the management of dynamic upper airway obstruction in both equine and human athletes.22,27 A larger investigation is required to explore any association between IMSi and athletic performance in horses.4 ...
Article
Little is known about the response of the equine respiratory muscles to training. To measure an index of inspiratory muscle strength (IMSi) before and after a period of conventional exercise training (phase 1) and inspiratory muscle training (IMT), comparing high‐load (treatment) and low‐load (control) groups (phase 2). Prospective randomised controlled trial. Phase 1: Twenty National Hunt Thoroughbred racehorses performed an inspiratory muscle strength test (IMST) twice on two occasions; when unfit at timepoint A (July), and when race fit at timepoint B (October). Phase 2: Thirty‐five Thoroughbred racehorses at race fitness were randomly assigned into a high‐load (treatment, n = 20) or low‐load (control, n = 15) IMT group. The high‐load group followed an IMT protocol that gradually increased the inspiratory pressure applied every 4 days. The low‐load group underwent sham IMT with a low training load. The IMT was performed 5 days/week for 10 weeks. The IMST was performed twice on two occasions, timepoint B (October) and timepoint C (January). Conventional exercise training and racing continued during the study period. The peak IMSi values obtained from the different groups at timepoints A, B and C were compared using a Wilcoxon Signed Rank Test. Phase 1: There was a significant increase in IMSi from timepoint A: 22.5 cmH2O (21–25) to timepoint B: 26 cmH2O (24–30) (p = 0.015). Phase 2: From timepoint B to C there was a significant increase in IMSi for the high‐load group 34 cmH2O (28–36) (p = 0.001) but not the low‐load group 26 cmH2O (24–30) (p = 0.929). The peak IMSi at timepoint C was significantly higher for the high‐load than low‐load group (p = 0.019). Single centre study with only National Hunt horses undergoing race‐training included. In horses undergoing race training there is a significant increase in IMSi in response to conventional exercise training and high‐load IMT.
... Respiratory muscles become strong due to regular forceful inspiration and expiration during exercise (Hildebrean et al., 1981). Because the body's oxygen demand increases during sporting activities, the amount of oxygen transported from the respiratory system to the tissues also increases Illi et al., 2012). Endurance and strength exercise intensity is an essential determinant of changes in the fibre types of respiratory muscles (Granata et al., 2018). ...
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The main purpose of this study was to examine the correlation between the aerobic and anaerobic performance of diaphragm thickness in athletes. That study was conducted with 15 team athletes (TA) (age 21.80 ± 2.40 years), 15 individual athletes (IA) (age 18.93 ± 2.31 years) and the control group (CON) 10 people living sedentary lifestyles (age 23.60 ± 2.91 years). In this study, diaphragm muscle thickness (B-mode ultrasonography), respiratory function (spirometry and maximum inspiratory (MIP) and expiratory pressures (MEP), aerobic capacity yo-yo intermittent endurance Test 1 (YYIET-1), and anaerobic power by Monark 834 E were assessed. The diaphragm thickness was determined from the intercostalspace between the 8th and 9th ribs at the expiration time by ultrasound and from the intercostal space between the 10th and 11th ribs at inspiration and then, the thickness of the diaphragm was measured from the diaphragm is seen best. There was a positive correlation between DiTins (r= 0.477) and DiTins-ex (r= 0.473) parameters of TA. In IA, there was a significant correlation between DiTins and DiTins-ex parameters and Peak Power (r= 0.495 and 0.435, respectively) and average power (r= 0.483 and 0.446, respectively). No significant correlation in all parameters of the CON group (p<0.05). As a result, it was determined that athletes with high diaphragm thickness had higher anaerobic performance, and athletes with thinner diaphragm thickness had better VO2Max capacity. The diaphragm thickness of the athletes in individual branches was thicker than the team athletes, and their anaerobic performance was also higher.
... Investigations in human athletes have shown IMT can delay the onset of inspiratory muscle fatigue 9 which can lead to improvements in athletic performance. 10 Recent studies have established the successful application of IMT, performed at rest, in Thoroughbred racehorses, demonstrating an increase in inspiratory muscle strength and change in upper airway muscle function following a period of IMT. [11][12][13] Ultrasonographic measurement is a non-invasive and repeatable method to assess muscle thickness and cross-sectional area, and is performed in human athletes to evaluate the effect of training and to measure the response to rehabilitation. ...
Article
Background: Limited information exists regarding changes in the size of respiratory and locomotor muscles in response to exercise training in the Thoroughbred racehorse. Objectives: To describe and compare the responses of the respiratory and locomotor muscles to conventional exercise training and inspiratory muscle training (IMT). Study design: Prospective randomised controlled trial. Methods: Thoroughbred racehorses, in training for competition in National Hunt races, were recruited from two training establishments. Ultrasonographic images were obtained for selected muscles of the upper airway, diaphragm, accessory respiratory, and locomotor systems and their sizes measured. Examinations were performed at three timepoints; (A) when unfit, (B) following 12 weeks of conventional exercise training, and (C) following 10-12 weeks continued training at race fitness. In addition, horses at yard 1 performed IMT, between timepoint B-C, and were randomly assigned into high-load (treatment) or low-load (control) group. Repeated measures models were constructed to compare the change in muscle measurements over time, and to investigate the effects of yard, previous airway surgery and IMT on the change in ultrasonographic size measurements obtained. Results: Upper airway muscle size increased in response to conventional race training between timepoints A-C, and B-C. Diaphragm size increased in response to conventional exercise training between timepoints A-B. The diaphragm size of horses that undertook high-load IMT was either maintained or increased, whereas diaphragm size decreased in horses that undertook low-load IMT or no IMT between timepoints B-C. A significant interaction between gluteal muscle size and airway surgery status was observed, with greater gluteal muscle thicknesses measured in horses that had not previously undergone airway surgery (left gluteal 3.9%, p <0.001; right 4.5%, p=0.04). Main limitations: Low number of horses underwent IMT. Conclusions: Respiratory and locomotor muscles increase in size in response to conventional exercise training, with a further change in diaphragm size in response to inspiratory muscle training.
... Anatomy, physiological capacities, and the state of the cardiopulmonary system are all important factors for performance. Various exercise modalities/sports may challenge ventilation, and optimal conditions for diaphragmatic and thoracic expansion depend on body posture and breathing frequency (18,19). The larynx plays a role in some exercise modalities, where closure of the glottis facilitates elevation of thoracic and abdominal pressures (20). ...
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Complaints of breathlessness during heavy exercise is common in children and adolescents, and represent expressions of a subjective feeling that may be difficult to verify and to link with specific diagnoses through objective tests. Exercise-induced asthma and exercise-induced laryngeal obstruction are two common medical causes of breathing difficulities in children and adolescents that can be challenging to distinguish between, based only on the complaints presented by patients. However, by applying a systematic clinical approach that includes rational use of tests, both conditions can usually be diagnosed reliably. In this invited mini-review, we suggest an approach we find feasible in our everyday clinical work.
... This observation meets the conclusion of one review [51], in which the results favored earlier transfer to rehabilitation services to improve post-stroke function. As well, another review [52] found that less-fit individuals benefitted more from RMT than highly trained individuals, and their improvements were greater, which also corroborates the results of some studies [19,37] in which patients with acute stroke benefitted more from IMT alone than others. Therefore, people with stroke have good reasons to start RMT implementation as quickly as possible. ...
Article
Background: Previous reviews relating to the effects of respiratory muscle training (RMT) after stroke tend to focus on only one type of training (inspiratory or expiratory muscles) and most based the results on poor-quality studies (PEDro score ≤4). Objectives: With this systematic review and meta-analysis, we aimed to determine the effects of RMT (inspiratory or expiratory muscle training, or mixed) on exercise tolerance, respiratory muscle function and pulmonary function and also the effects depending on the type of training performed at short- and medium-term in post-stroke. Methods: Databases searched were MEDLINE, PEDro, CINAHL, EMBASE and Web of Science up to the end of April 2020. The quality and risk of bias for each included study was examined by the PEDro scale (including only high-quality studies) and Cochrane Risk of Bias tool. Results: Nine studies (463 patients) were included. The meta-analysis showed a significant increase in exercise tolerance [4 studies; n = 111; standardized mean difference [SMD] = 0.65 (95% confidence interval 0.27-1.04)]; inspiratory muscle strength [9 studies; n = 344; SMD = 0.65 (0.17-1.13)]; inspiratory muscle endurance [3 studies; n = 81; SMD = 1.19 (0.71-1.66)]; diaphragm thickness [3 studies; n = 79; SMD = 0.9 (0.43-1.37)]; and peak expiratory flow [3 studies; n = 84; SMD = 0.55 (0.03-1.08)] in the short-term. There were no benefits on expiratory muscle strength and pulmonary function variables (forced expiratory volume in 1 sec) in the short-term. Conclusions: The meta-analysis provided moderate-quality evidence that RMT improves exercise tolerance, diaphragm thickness and pulmonary function (i.e., peak expiratory flow) and low-quality evidence for the effects on inspiratory muscle strength and endurance in stroke survivors in the short-term. None of these effects are retained in the medium-term. Combined inspiratory and expiratory muscle training seems to promote greater respiratory changes than inspiratory muscle training alone.
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Conscious respiratory pattern and rate control is desired by patients with some forms of pulmonary disease that are undergoing respiratory muscle conditioning and rehabilitation, by practitioners of meditation hoping to improve mindfulness and wellbeing, by athletes striving to obtain breathing control in order to increase competitiveness, and by engineers and scientists that wish to use the data from breathing subjects to test hypotheses and develop physiological monitoring systems. Although prerecorded audio sources and computer applications are available that guide breathing exercises, they often suffer from being inflexible and allow only limited customization of the breathing cues. Here we describe a small, lightweight, battery-powered, microprocessor-based respiratory coaching device (RespiCo), which through wireless or wired connections, can be easily customized to precisely guide subjects to breathe at desired respiratory rates using specific breathing patterns through visual, auditory, or haptic cues. Digital signals can also be captured from the device to document the breathing cues provided by the device for research purposes. It is anticipated that this device will have important utility for those who wish to be guided to breathe in a precise manner or in research and development of physiologic monitoring systems.
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The purpose of this study was to assess the influence of the work history of the inspiratory muscles upon the fatigue characteristics of the plantar flexors (PF).We hypothesized that under conditions where the inspiratory muscle metaboreflex has been elicited, PF fatigue would be hastened due to peripheral vasoconstriction. Eight volunteers undertook seven test conditions, two ofwhichfollowed4 week of inspiratorymuscle training(IMT). The inspiratorymetaboreflex was induced by inspiring against a calibrated flowresistor.We measured torque andEMGduring isometric PF exercise at 85% of maximal voluntary contraction (MVC) torque. Supramaximal twitches were superimposed uponMVC efforts at 1 min intervals (MVCTI); twitch interpolation assessed the level of central activation. PF was terminated (Tlim) when MVCTI was<50% of baseline MVC. PF Tlim was significantly shorter than control (9.93±1.95 min) in the presence of a leg cuff inflated to 140 mmHg(4.89±1.78 min; P =0.006), as well aswhen PF was preceded immediately by fatiguing inspiratory muscle work (6.28±2.24 min; P =0.009). Resting the inspiratory muscles for 30 min restored the PF Tlim to control. After 4 weeks, IMT, inspiratory muscle work at the same absolute intensity did not influence PF Tlim, but Tlim was significantly shorter at thesamerelative intensity.Thedata are the first toprovide evidence that the inspiratory muscle metaboreflex accelerates the rate of calf fatigue during PF, and that IMT attenuates this effect.
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Inspiratory muscle training (IMT) has been shown to possibly improve exercise performance, but reports on IMT and running performance are rare. The objective of the present study was to examine the effect of target-flow IMT on running performance in recreational runners. Sixteen healthy recreational runners (five females) were recruited for the present study. They were randomly allocated into either an experimental or control group. Participants in the experimental group underwent a 6-week target-flow IMT programme, while those in the control group underwent a 6-week shoulder circumduction exercise programme. Running performance during a 1,500-m time trial run was assessed before and after the intervention period. After the intervention period, only the experimental group demonstrated an increase in inspiratory muscle strength (by 16.15 ± 7.44 cmH2O; p < 0.05) and reduced completion time in the 1,500-m time trial (by 9.63 ± 5.42 seconds; p < 0.05). Exertion sensation was reduced by 1.63 ± 0.74 points (p < 0.05). No changes were observed in maximal aerobic capacity and pulmonary function in either group after the intervention period. A 6-week target-flow IMT programme enhanced running performance in recreational runners.
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Recently, we have shown that an untrained respiratory system does limit the endurance of submaximal exercise (64% peak oxygen consumption) in normal sedentary subjects. These subjects were able to increase breathing endurance by almost 300% and cycle endurance by 50% after isolated respiratory training. The aim of the present study was to find out if normal, endurance trained subjects would also benefit from respiratory training. Breathing and cycle endurance as well as maximal oxygen consumption ( [(V)\dot]O2 max\dot VO_{2 max} ) and anaerobic threshold were measured in eight subjects. Subsequently, the subjects trained their respiratory muscles for 4 weeks by breathing 85-1601 min–1 for 30 min daily. Otherwise they continued their habitual endurance training. After respiratory training, the performance tests made at the beginning of the study were repeated. Respiratory training increased breathing endurance from 6.1 (SD 1.8) min to about 40 min. Cycle endurance at the anaerobic threshold [77 (SD 6) % [(V)\dot]O2 max\dot VO_{2 max} ] was improved from 22.8 (SD 8.3) min to 31.5 (SD 12.6) min while [(V)\dot]O2 max\dot VO_{2 max} and the anaerobic threshold remained essentially the same. Therefore, the endurance of respiratory muscles can be improved remarkably even in trained subjects. Respiratory muscle fatigue induced hyperventilation which limited cycle performance at the anaerobic threshold. After respiratory training, minute ventilation for a given exercise intensity was reduced and cycle performance at the anaerobic threshold was prolonged. These results would indicate the respiratory system to be an exercise limiting factor in normal, endurance trained subjects.
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Respiratory muscle training (RMT) has been extensively investigated over the past two decades. To date no method of ventilatory muscle training has fixed load throughout range in a manner consistent with the general principles of skeletal muscle training. The purpose of this study was to assess the use of computer-generated fixed-load incremental RMT produced by the performance of repeated sustained sub-maximal inspiratory efforts (80% of maximum, generated from RV to TLC; a full range of contraction/muscle shortening) with progressively reduced recovery times in healthy volunteers.
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The effects of inspiratory muscle (IM) training on maximal 20 m shuttle run performance (Ex) during Yo-Yo intermittent recovery test and on the physiological and perceptual responses to the running test were examined. Thirty men were randomly allocated to 1 of 3 groups. The experimental group underwent a 6 week pressure threshold IM training program by performing 30 inspiratory efforts twice daily, 6 d/week, against a load equivalent to 50% maximal static inspiratory pressure. The placebo group performed the same training procedure but with a minimal inspiratory load. The control group received no training. In post-intervention assessments, IM function was enhanced by >30% in the experimental group. The Ex was improved by 16.3% +/- 3.9%, while the rate of increase in intensity of breathlessness (RPB/4i) was reduced by 11.0% +/- 6.2%. Further, the whole-body metabolic stress reflected by the accumulations of plasma ammonia, uric acid, and blood lactate during the Yo-Yo test at the same absolute intensity was attenuated. For the control and placebo groups, no significant change in these variables was observed. In comparison with previous observations that the reduced RPB/4i resulting from IM warm-up was the major reason for improved Ex, the reduced RPB/4i resulting from the IM training program was lower despite the greater enhancement of IM function, whereas improvement in Ex was similar. Such findings suggest that although both IM training and warm-up improve the tolerance of intense intermittent exercise, the underlying mechanisms may be different.
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Inspiratory muscle training (IMT) has been shown to improve inspiratory muscle function, lung volumes (vital capacity [VC] and total lung capacity [TLC]), work capacity, and power output in people who are healthy; however, no data exist that demonstrate the effect of varying intensities of IMT to produce these outcomes. The purpose of this study was to evaluate the impact of IMT at varying intensities on inspiratory muscle function, VC, TLC, work capacity, and power output in people who are healthy. This was a randomized controlled trial. The study was conducted in a clinical laboratory. Forty people who were healthy (mean age=21.7 years) were randomly assigned to 4 groups of 10 individuals. Three of the groups completed an 8-week program of IMT set at 80%, 60%, and 40% of sustained maximum inspiratory effort. Training was performed 3 days per week, with 24 hours separating training sessions. A control group did not participate in any form of training. Baseline and posttraining measurements of body composition, VC, TLC, inspiratory muscle function (including maximum inspiratory pressure [MIP] and sustained maximum inspiratory pressure [SMIP]), work capacity (minutes of exercise), and power output were obtained. The participants in the 80%, 60%, and 40% training groups demonstrated significant increases in MIP and SMIP, whereas those in the 80% and 60% training groups had increased work capacity and power output. Only the 80% group improved their VC and TLC. The control group demonstrated no change in any outcome measures. This study may have been underpowered to demonstrate improved work capacity and power output in individuals who trained at 40% of sustained maximum inspiratory effort. High-intensity IMT set at 80% of maximal effort resulted in increased MIP and SMIP, lung volumes, work capacity, and power output in individuals who were healthy, whereas IMT at 60% of maximal effort increased work capacity and power output only. Inspiratory muscle training intensities lower than 40% of maximal effort do not translate into quantitative functional outcomes.
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During increased ventilation, inspiratory rib cage muscles have been suggested to take over part of diaphragmatic work after the diaphragm fatigues. We investigated the extent to which this proposed change in muscle recruitment is associated with changes in the relative contribution of chest wall compartments to tidal volume (V(T)). Thirteen healthy subjects performed 1 h of fatiguing normocapnic hyperpnoea. Chest wall volumes were assessed by optoelectronic plethysmography. While breathing frequency increased (43±3 to 56±5 breaths min(-1), p=0.006) and V(T) decreased during normocapnic hyperpnoea (2.6±0.2 to 1.9±0.1l, p<0.001), the relative contribution of chest wall compartments to V(T) remained unchanged (pulmonary rib cage: 48±9 versus 51±14%; abdominal rib cage: 24±4 versus 23±9%; abdomen: 28±8 versus 26±9%; all p>0.05). In conclusion, fatiguing respiratory work is not associated with a change in compartmental contribution to V(T), even in the presence of a change in breathing pattern.