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Open Access Full Text Article Original Research

Respiratory muscle training with normocapnic

hyperpnea improves ventilatory pattern and
thoracoabdominal coordination, and reduces
oxygen desaturation during endurance exercise
testing in COPD patients
This article was published in the following Dove Press journal:
International Journal of COPD
10 September 2015
Number of times this article has been viewed

Eva Bernardi 1 Background: Few data are available about the effects of respiratory muscle training with normo-
Luca Pomidori 1 capnic hyperpnea (NH) in COPD. The aim is to evaluate the effects of 4 weeks of NH (Spirotiger®)
Faisy Bassal 1 on ventilatory pattern, exercise capacity, and quality of life (QoL) in COPD patients.
Marco Contoli 2 Methods: Twenty-six COPD patients (three females), ages 49–82 years, were included in this
Annalisa Cogo 1 study. Spirometry and maximal inspiratory pressure, St George Respiratory Questionnaire,
6-minute walk test, and symptom-limited endurance exercise test (endurance test to the limit of
1
Biomedical Sport Studies Center,
University of Ferrara, Ferrara,
tolerance [tLim]) at 75%–80% of peak work rate up to a Borg Score of 8–9/10 were performed
2
Respiratory Section, Department before and after NH. Patients were equipped with ambulatory inductive plethysmography
of Medical Sciences, University of (LifeShirt®) to evaluate ventilatory pattern and thoracoabdominal coordination (phase angle
Ferrara, Cona (FE), Italy
[PhA]) during tLim. After four supervised sessions, subjects trained at home for 4 weeks –
10 minutes twice a day at 50% of maximal voluntary ventilation. The workload was adjusted
during the training period to maintain a Borg Score of 5–6/10.
Results: Twenty subjects completed the study. After NH, maximal inspiratory pressure
significantly increased (81.5±31.6 vs 91.8±30.6 cmH2O, P,0.01); exercise endurance time
(+150 seconds, P=0.04), 6-minute walk test (+30 meters, P=0.03), and QoL (-8, P,0.01) all
increased. During tLim, the ventilatory pattern changed significantly (lower ventilation, lower
respiratory rate, higher tidal volume); oxygen desaturation, PhA, and dyspnea Borg Score
were lower for the same work intensity (P,0.01, P=0.02, and P,0.01, respectively; one-way
ANOVA). The improvement in tidal volume and oxygen saturation after NH were significantly
related (R2=0.65, P,0.01).
Conclusion: As expected, NH improves inspiratory muscle performance, exercise capacity,
and QoL. New results are significant change in ventilatory pattern, which improves oxygen
saturation, and an improvement in thoracoabdominal coordination (lower PhA). These two facts
could explain the reduced dyspnea during the endurance test. All these results together may
play a role in improving exercise capacity after NH training.
Keywords: COPD, exercise, inspiratory muscle, pulmonary rehabilitation

Introduction
Correspondence: Eva Bernardi
Dyspnea is the primary symptom that limits exercise in many patients with COPD.1,2
Biomedical Sport Studies Center, In COPD, exercise limitation is clearly multifactorial; one of the main contributors1
University of Ferrara, via Gramicia 35,
44100 Ferrara, Italy
is ventilatory limitation due to increased airway resistance and pulmonary hyperin-
Email bernardi.eva@gmail.com flation, both increasing the work of breathing.3–5 In addition, COPD patients exhibit

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http://dx.doi.org/10.2147/COPD.S88609
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abnormal thoracoabdominal motion during exercise and The Ethics Committee of the University of Ferrara
this is another cause of exercise limitation.6–9 In particular, approved the study (protocol number 090591). Informed
Chien et al9 showed that asynchronous thoracoabdominal consent was obtained from each subject.
motion occurred early during exercise in patients with mild
COPD, contributing to a decreased 6-minute walk distance. Study design
Respiratory muscle weakness can also play a role in dyspnea On the first day of the study, patients performed a respiratory
perception and exercise limitation. Indeed, inspiratory muscle function test (forced flow–volume curve) and their inspira-
weakness is observed in COPD patients10,11 and contributes tory muscle strength (maximal inspiratory pressure [MIP])
to dyspnea perception.1,12,13 was measured. After 30 minutes of rest, a 6-minute walk
For this reason, there has been an interest in applying a test (6MWT) was performed.21 The St George Respiratory
specific training to the inspiratory muscles in COPD patients. Questionnaire (SGRQ) for measuring health-related QoL
Different forms of respiratory muscle training (RMT) have was completed.22
been used, and from recent meta-analyses14,15 it is clear that On the second day, an incremental walking test was
RMT increases inspiratory muscle performance and functional performed, followed, after 30 minutes of rest, by an endur-
exercise capacity (ie, 6-minute walk distance, endurance ance test to the limit of tolerance (tLim) (ie, until subjects
exercise capacity, and maximal oxygen consumption14,15), were unable to continue due to symptoms). Daily physical
and decreases dyspnea, but the clinical importance of these activity was monitored using the SenseWear Armband®
improvements remains unclear. Most studies investigated (BodyMedia, Pittsburgh, PA, USA) validated for estimating
the effects of RMT with resistive or threshold loading,14 energy expenditure in COPD patients.23,24
while a few studies evaluated16–18 the effects of RMT with After 4 weeks of respiratory muscle endurance training
normocapnic hyperpnea (NH) even though Koppers et al16 (NH), the subjects repeated all the tests in a standardized
reported that NH could be the most appropriate technique manner and sequence.
for improving respiratory muscle endurance capacity, which The testing and the training procedure are detailed in the
is required during endurance exercises. sections Exercise testing and Respiratory muscle endurance
None of these studies16–18 investigated the effects of NH training.
on thoracoabdominal coordination and oxygen saturation
(SpO2) during exercise in COPD patients, whereas only one Respiratory function
study16 investigated the effects of NH on the ventilatory pat- The forced flow–volume curve was performed (JAEGER®
tern, showing lower minute ventilation and respiratory rate MasterScreen Body; San Diego, CA, USA) to measure forced
and larger tidal volume during exercise. vital capacity and FEV1. In accordance with the guidelines
The aim of this study was to evaluate the effects of of the American Thoracic Society/European Respiratory
4 weeks of NH (using the Spirotiger® device) on thoracoab- Society,25 subjects repeated the maneuver at least three times
dominal coordination, SpO2, ventilatory pattern, exercise and the two largest values of forced vital capacity and FEV1 had
capacity, and quality of life (QoL) in COPD patients. to be within 0.15 L of each other. Reference normal values were
taken from the European Community for Steel and Coal.20
Methods After respiratory function, MIP was measured; starting
Subjects were consecutively recruited from the outpatient from residual volume, the subject was asked to inspire as
clinic of the Department of Respiratory Disease, Ferrara deeply as possible, maintaining the maximal pressure for
University Hospital, Italy. at least 1.5 seconds. The pressure was measured with a
Inclusion criteria were as follows: 1) COPD as defined manometer (CARDINAL Health microRPM®; San Diego,
according to international guidelines;19 2) forced expira- CA, USA). Subjects repeated the maneuver a minimum of
tory volume in 1 second (FEV1) between 30% and 80% five times and reproducibility had to be within 5%–10%
predicted,20 after bronchodilatation; and 3) stable clinical in accordance with the guidelines.26 The highest value was
condition for at least 6 weeks. Exclusion criteria were as considered for comparison before and after training.
follows: 1) cardiac comorbidity (ie, recent myocardial
infarction, myocardial ischemia, and cardiac arrhythmia); 2) Exercise testing
inability to use the device; and 3) inclusion in any pulmonary The 6MWT was performed in a corridor 24 m long. The
rehabilitation program. subjects were instructed to cover as much distance as possible

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Dovepress NH improves ventilatory pattern and oxygen saturation in COPD

in 6 minutes and standardized verbal encouragement was the size of the bag and breathing frequency was changed
given.21 The maximum distance walked was recorded. accordingly to maintain target training ventilation (ie
The maximal incremental exercise test was performed on 50%–60% of maximal voluntary ventilation). The subjects
a treadmill (Runner Galaxy MTC, Cavezzo, Italy). During the trained 20 minutes daily (1 minute of exercise and 1 minute
test, the work rate was increased every 10 meters by 0.2 km/h.27 of rest, ten times, twice a day), 7 days a week, for 5 weeks.
Arterial blood pressure was measured every minute. Heart rate While performing NH, the patients wore a nose clip to ensure
and SpO2 were continuously monitored. At the end of the test, breathing occurred exclusively through the training device.
maximal working capacity (Speedmax) was recorded. During the training period, a diary documented the com-
A constant-load endurance exercise test was performed pliance with home-based training: number, duration of the
on a treadmill at a work rate of 80%–85% of the individual’s sessions, and rating of perceived respiratory exertion (Borg
Speedmax and continued to the tLim.28 Subjects were not Score) were reported.
encouraged during the test. Perception of dyspnea and mus-
cular fatigue were measured using the Borg Scale29 at regular Statistical analysis
intervals. The tLim was terminated when the subjects indi- Data are reported as mean ± standard deviation. The Student’s
cated they were unable to continue due to intolerable dyspnea t-test was used to compare baseline characteristics and train-
and/or muscular fatigue (Borg Score 8–9/10), or were unable ing changes. The one-way ANOVA test with analysis of
to keep up with the speed of the treadmill; the duration of the the covariate was used to evaluate the effects of training on
test was recorded as walking endurance time. ventilation, ventilatory pattern, and PhA; the P-values were
During tLim, patients were equipped with ambulatory adjusted according to the Bonferroni correction. The para-
inductive plethysmography (LifeShirt® System, San Diego, metric Pearson correlation coefficient was used to describe
CA, USA).30 The LifeShirt® features rib cage and abdominal the relationships between variables. Statistical significance
inductance bands embedded within an elasticized vest, con- was accepted at P,0.05. All the analyses were performed
nected to a battery-operated handheld computer. The handheld using GraphPad Prism 40.
computer continuously records data. Before each test, a cali-
bration of the system was performed. After the testing session, Results
the data were downloaded and analyzed with a dedicated Twenty-six patients were included in the study. Baseline
software (Vivologic 3.0, Vivonoetics, San Diego, CA, USA) characteristics of the subjects are shown in Table 1. The mean
for calculating respiratory variables: ventilation, tidal volume, age of the study population was 69±8 years. According to
and respiratory rate. The phase angle (PhA) was obtained as a Armband® data, the physical activity status of the subjects
measure of asynchrony between rib cage and abdominal move- was between low and moderate (Table 1). Medication was
ments (thoracoabdominal asynchrony). A pulse oximeter and an not changed during the study period.
electrocardiograph were integrated into the LifeShirt system.
Table 1 Baseline characteristics (26 subjects)
Respiratory muscle endurance training Variables T0
The training protocol lasted 4 weeks and was performed Age (years) 69±8
by means of Spirotiger® (MVM, Linate, MI, Italy), which Weight (kg) 83.5±13.2
consists of a handheld unit with a pouch and a base station. Body mass index (kg/m2) 29.4±4.8
A two-way piston valve connected to a rebreathing bag FEV1 (L) 1.49±0.47
FEV1 (% pred) 56±16
permits a constant isocapnic end-tidal CO2 fraction31 to be
FVC (L) 2.63±0.84
maintained. FVC (% pred) 75±21
Before starting the protocol, subjects underwent four FEV1/FVC (%) 57±13
supervised training sessions to learn the technique and to MIP (cmH2O) 81.5±31.6
define the target training ventilation. In accordance with MIP (% pred) 81±33
SGRQ (total) 29.6±16.8
previous studies,16–18 the size of the bag was adjusted to
Daily physical activity (METs) 1.4±0.2
50%–60% of the subject’s vital capacity and the breathing
Note: Data are expressed as mean ± SD.
frequency chosen was such that ventilation corresponded to Abbreviations: FEV1, forced expiratory volume in 1 second; FEV1 (% pred), % of
predicted value of forced expiratory volume in 1 second; FVC, forced vital capacity;
50%–60% of maximal voluntary ventilation (calculated as MIP, maximal inspiratory pressure; SGRQ, St George Respiratory Questionnaire;
35 times FEV1). The tidal volume was adjusted by changing T0, baseline; SD, standard deviation; MET, metabolic equivalent of task.

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Bernardi et al Dovepress

Twenty patients completed the study. Six patients did Exercise performance and ventilatory
not complete the study: two because of poor tolerance to the pattern
device, three because of poor compliance, and one because The effects of NH on exercise performance are shown in
of excessive fatigue. Table 2.
Intriguingly, at baseline (T0), a positive correlation is Regarding the 6MWT, the distance covered increased by
found between MIP and FEV1 as a percentage of predicted 30 m (Student’s t-test, P=0.03).
values (Figure 1A) and between MIP and the 6MWT The duration of tLim significantly increased by 2 minutes
(Figure 1B); an inverse correlation is shown between MIP and 30 seconds (Student’s t-test, P=0.04); during the test,
and the total SGRQ score (Figure 1C). average speed was 4.8±0.9 km/h, corresponding to 79% of
Speedmax (6.1±1.2 km/h).
NH training Regarding ventilatory data, a significant increase in
Analysis of the diaries showed that all patients trained tidal volume at rest was shown (T0: 0.29±0.74 mL and
20 minutes daily, every day at a workload corresponding T1: 0.32±0.81 mL; Student’s t-test, P=0.02). During
to 51% of maximal voluntary ventilation with a mean Borg tLim, after the training, significantly lower ventilation and
Score of 6/10. respiratory rate were found (one-way ANOVA, P,0.05;
­Figure 2A–C for ventilation, respiratory rate, and tidal vol-
Inspiratory muscle performance ume, respectively). Furthermore, a lower increase in PhA
Table 2 shows the effects of 4 weeks of home-based NH on was found during exercise (one-way ANOVA, P=0.02;
respiratory function and muscle strength. After training (T1), Figure 3).
MIP significantly increased (+10.3 cmH2O; Student’s t-test, Regarding SpO2, an improvement was found at rest
P=0.0001). A strong correlation was found between the value (Student’s t-test, P=0.02; Table 2). The SpO2 monitoring
at T0 and at T1 (R2=0.90, P,0.00001). The probability plot during tLim showed significantly higher values (one-way
distribution confirms normal distribution of the data. ANOVA, P,0.01; Figure 4).

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Figure 1 Correlation between MIP and FEV1 (A), 6MWT (B), and SGRQ (C) before the training.
Abbreviations: FEV1, forced expiratory volume in 1 second; 6MWT, 6-minute walk test; SGRQ, St George Respiratory Questionnaire; MIP, maximal inspiratory pressure.

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Dovepress NH improves ventilatory pattern and oxygen saturation in COPD

Table 2 Pretraining and posttraining values (20 subjects) Discussion

Variables T0 T1 The aim of this study was to evaluate the effects of 4 weeks
Respiratory function of inspiratory muscle training with NH on ventilatory pat-
FEV1 (L) 1.54±0.44 1.56±0.39 tern, exercise capacity, and QoL in COPD patients. The
FVC (L) 2.57±0.84 2.82±0.77
Respiratory muscle pressure
main results are the changes in ventilatory pattern and the
MIP (cmH2O) 81.5±31.6 91.8±30.6* improved thoracoabdominal coordination during exercise
Exercise performance after training.
6MWT (meters) 423±71 453±73*
Regarding the ventilatory pattern, after training at the
tLim
Time (seconds) 347±235 497±410* same work intensity, we found lower ventilation, a decrease
Heart rate rest (bpm) 80±13 77±14 in respiratory rate, and an increase in tidal volume. The
Heart rate max (bpm) 123±19 123±14 slower and deeper ventilation allows improved alveolar
SpO2 rest (%) 94±2 95±2*
SpO2 min (%)
ventilation, which in turn has an effect on gas exchange. The
90±4 91±2
Dyspnea Borg Score (/10) 8±1 8±1 subjects exhibit improved oxygenation, which is related to
Muscular fatigue Borg Score (/10) 7±1 7±2 the increase in tidal volume. Improved oxygenation is already
SGRQ (total) 29±17 21±12* evident at rest when the ventilatory pattern is characterized
Daily physical activity (METs) 1.5±0.2 1.5±0.2
by a higher tidal volume at the same ventilation. Several
Number of steps 7,210±2,388 7,720±4,199
studies32–34 have already shown that deeper and slower breath-
Notes: Data are expressed as mean ± SD. *Student’s t-test, P,0.05.
Abbreviations: FEV1, forced expiratory volume in 1 second; FVC, forced vital ing (so-called yoga breathing) improves SpO2 in both healthy
capacity; MIP, maximal inspiratory pressure; 6MWT, 6-minute walk test; tLim,
endurance test to the limit of tolerance; SpO2, oxygen saturation; SGRQ, St George
subjects exposed to high altitude32 and subjects suffering from
Respiratory Questionnaire; T0, baseline; T1, after 4 weeks of respiratory muscle chronic diseases such as heart failure33 and COPD.34
training; SD, standard deviation; bpm, beats per minute; MET, metabolic equivalent
of task; min, minimum.
To our knowledge, only Koppers16 has described the ven-
tilatory pattern changes after NH, but only during exercise.
After training, a correlation was found during tLim In his study,16 he also highlights that deeper and slower ven-
between the changes in tidal volume and SpO2 (Figure 5). tilation reduces the work of breathing, delaying respiratory
All these findings were associated with lower dyspnea and muscle fatigue, and dyspnea perception. Moreover, improved
muscular fatigue Borg Score (one-way ANOVA, P,0.01; thoracoabdominal coordination plays a key role in dyspnea
Figure 6A and B, respectively). perception, even though few data are available in literature.

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Figure 2 The ventilation (A), respiratory rate (B), and tidal volume trend (C) during tLim before T0 and after T1 training.
Notes: ANOVA test between T0 and T1. Mean value at rest, at 25%, 50%, 75%, and 100% of the tLim duration at T0. *P0.05 between T0 and T1.
Abbreviations: tLim, endurance test to the limit of tolerance; T0, baseline; T1, after 4 weeks of respiratory muscle training; ANOVA, analysis of variance; min, minute.

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Figure 3 The PhA trend during tLim before and after training. ±     
Notes: ANOVA test between T0 and T1. Mean value at rest, at 25%, 50%, 75%, and ∆6S2 
100% of the tLim duration at T0.
Abbreviations: PhA, phase angle; tLim, endurance test to the limit of tolerance; Figure 5 Correlation between the changes in tidal volume and SpO2, before and
T0, baseline; T1, after 4 weeks of respiratory muscle training. after training, during tLim.
Abbreviations: SpO2, oxygen saturation; tLim, endurance test to the limit of
tolerance.

Indeed, only two studies9,35 have investigated this asynchrony

in COPD subjects. In particular, Chien9 has shown that
increase in respiratory muscle strength, and not just endur-
thoracoabdominal asynchrony reduces exercise capacity
ance, is clinically relevant to COPD patients.38,39 In fact,
in moderate and severe COPD. The mechanism, however,
Terzano et al38 and Tudorache et al39 have demonstrated
remains unclear.36,37 Our results are in line with this result; in
that airway obstruction is closely associated with lower
fact, in our study, patients with moderate and severe COPD
respiratory muscle pressures. In our study, we also found,
show an increased exercise capacity together with better tho-
at baseline, a correlation between MIP and the severity of
racoabdominal coordination. Both the change in ventilatory
bronchial obstruction. Furthermore, Tudorache et al39 found
pattern and the improved thoracoabdominal coordination can
a correlation between MIP and the 6MWT distance, as in
explain the reduction in dyspnea perception.
our study. However, to the best of our knowledge, there is
Besides the innovative results related to ventilation,
no study in literature demonstrating a significant inverse
we also found a significant increase in inspiratory muscle
correlation between MIP and QoL.
strength after NH. This is a quite controversial point. In
Regarding exercise capacity, the positive effects of NH in
fact, it is clear from meta-analyses14,15 that NH increases
COPD16–18 are already known. In this study, we have found a
inspiratory muscle endurance and only one study18 showed
higher duration of the endurance test (+43%) and an increase
that it improved respiratory muscle strength. However, the
in walking distance during the 6MWT (+30 m), which are
the minimal important difference.28,40,41
 Another interesting point is the evidence that the level
of physical activity of the subjects did not change during the

study period. The use of the multi-sensor Armband® allowed

us to verify that the energy expenditure and the number of
6S2 

 daily steps did not change significantly after NH. Therefore,

3
 no significant physical activity changes could have influenced

our results.42
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This study has some limitations. The main limitation is

the absence of a sham group. So far, there is no instrument
5HVW    
available that allows NH without any workload, which should
RIWKHW/LPGXUDWLRQDW7
be the gold standard for control group training. Among all
Figure 4 The SpO2 trend during tLim before and after training. papers discussing NH, only three17,18,43 studied a control
Notes: ANOVA test between T0 and T1. Mean value at rest, at 25%, 50%, 75%, and
100% of the tLim duration at T0. *P0.05 between T0 and T1. group training with an incentive spirometer with minimal
Abbreviations: SpO2, oxygen saturation; tLim, endurance test to the limit of
tolerance; T0, baseline; T1, after 4 weeks of respiratory muscle training; ANOVA,
resistance and a low respiratory rate; however, this device
analysis of variance. does not completely satisfy our purposes.

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Dovepress NH improves ventilatory pattern and oxygen saturation in COPD

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Figure 6 The Borg dyspnea (A) and muscular fatigue (B) trend during tLim before and after training.
Notes: ANOVA test between T0 and T1. Mean value at rest, at 25%, 50%, 75%, and 100% of the tLim duration at T0. *P0.05 between T0 and T1.
Abbreviations: tLim, endurance test to the limit of tolerance; T0, baseline; T1, after 4 weeks of respiratory muscle training; ANOVA, analysis of variance.

Another limitation is the high number of dropouts (23%). References

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