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Inspiratory muscle training lowers the oxygen cost of voluntary hyperpnea
Louise A. Turner,
1,2
Sandra L. Tecklenburg-Lund,
1,3
Robert F. Chapman,
1
Joel M. Stager,
1
Daniel P. Wilhite,
1
and Timothy D. Mickleborough
1
1
Human Performance Laboratory, Department of Kinesiology, Indiana University, Bloomington, Indiana;
2
Department of
Sport and Exercise Science, Northumbria University, Newcastle upon Tyne, United Kingdom; and
3
Health and Human
Performance, Nebraska Wesleyan University, Lincoln, Nebraska
Submitted 28 July 2011; accepted in final form 3 October 2011
Turner LA, Tecklenburg-Lund SL, Chapman RF, Stager JM, Wil-
hite DP, Mickleborough TD. Inspiratory muscle training lowers the oxygen
cost of voluntary hyperpnea. J Appl Physiol 112: 127–134, 2012. First
published October 6, 2011; doi:10.1152/japplphysiol.00954.2011.—The
purpose of this study was to determine if inspiratory muscle training
(IMT) alters the oxygen cost of breathing (V
˙
O
2RM
) during voluntary
hyperpnea. Sixteen male cyclists completed 6 wk of IMT using an
inspiratory load of 50% (IMT) or 15% placebo (CON) of maximal
inspiratory pressure (P
I
max
). Prior to training, a maximal incremental
cycle ergometer test was performed to determine V
˙
O
2
and ventilation
(V
˙
E
) at multiple workloads. Pre- and post-training, subjects performed
three separate 4-min bouts of voluntary eucapnic hyperpnea (mimic),
matching V
˙
E
that occurred at 50, 75, and 100% of V
˙
O
2 max
.PI
max
was
significantly increased (P ⬍ 0.05) by 22.5 ⫾ 8.7% from pre- to
post-IMT and remained unchanged in the CON group. The V
˙
O
2RM
required during the mimic trial corresponded to 5.1 ⫾ 2.5, 5.7 ⫾ 1.4,
and 11.7% ⫾ 2.5% of the total V
˙
O
2
(V
˙
O
2T
) at ventilatory workloads
equivalent to 50, 75, and 100% of V
˙
O
2 max
, respectively. Following
IMT, the V
˙
O
2RM
requirement significantly decreased (P ⬍ 0.05) by
1.5% (4.2 ⫾ 1.4% of V
˙
O
2T
) at 75% V
˙
O
2 max
and 3.4% (8.1 ⫾ 3.5% of
V
˙
O
2T
) at 100% V
˙
O
2 max
. No significant changes were shown in the
CON group. IMT significantly reduced the O
2
cost of voluntary
hyperpnea, which suggests that a reduction in the O
2
requirement of
the respiratory muscles following a period of IMT may facilitate
increased O
2
availability to the active muscles during exercise. These
data suggest that IMT may reduce the O
2
cost of ventilation during
exercise, providing an insight into mechanism(s) underpinning the
reported improvements in whole body endurance performance; how-
ever, this awaits further investigation.
respiratory muscles; exercise; hyperventilation; respiratory muscle
training
THE OXYGEN COST of breathing or energy requirement of the
respiratory muscles are shown to increase relative to the level
of ventilation (V
˙
E
) and the work of breathing (W
b
) (1, 8).
During moderate-intensity exercise the respiratory musculature
requires ⬃3– 6% of total oxygen consumption (V
˙
O
2T
), increas-
ing to ⬃10 –15% at maximal exercise (1, 3). The W
b
is derived
from a combination of elastic work, the work done to over-
come the elastic recoil of the lung (during inspiration) and
chest wall (during expiration), and resistive work that is re-
quired to overcome airway resistance (4, 15). Reducing the W
b
by ⬃50% via a proportional assist-ventilator during whole
body exercise has been shown to result in an ⬃7% decrease in
pulmonary oxygen consumption (17) and a significant im-
provement in exercise tolerance (⬃90% V
˙
O
2 max
) (18).
Inspiratory muscle training (IMT) is an intervention that has
been associated with improvements in whole body exercise
performance (24, 31, 34), enhanced pulmonary oxygen uptake
kinetics (5), reduced blood lactate concentrations (6, 24),
diaphragmatic fatigue, and cardiovascular responsiveness (37).
In addition, recent evidence suggests that improved exercise
performance following a period of IMT is associated with
reduced W
b
(28). Based on the relationship between W
b
and
V
˙
O
2
(1, 3, 16), it is plausible to suggest that if IMT does act to
decrease respiratory muscle work during exercise, then the
energy requirement for exercise hyperpnea would presumably
decrease, potentially leading to an increase in O
2
availability to
the limb locomotor muscles during exercise and the favorable
changes previously described. However, this postulate remains
to be elucidated. Eucapnic voluntary hyperpnea (EVH) is a
measurement technique previously used to determine the O
2
cost of breathing, thereby assessing the energy requirements of
the respiratory musculature for any given ventilation (1, 3).
Accordingly, by determining the O
2
cost of breathing using
EVH at rest, rather than whole body V
˙
O
2
during exercise, it is
possible to assess changes in the metabolic demand of the
respiratory muscles following IMT. Therefore, the purpose of
this study was to evaluate the influence of IMT on the O
2
cost
of breathing during EVH, mimicking the ventilator volumes
and rates obtained during moderate-to-maximal exercise inten-
sities. We hypothesized that following a period of IMT, the O
2
cost of breathing for a given ventilatory workload during
voluntary hyperpnea would be reduced.
METHODS
Subjects. Sixteen healthy, highly trained male cyclists [mean ⫾
SD; age 24 ⫾ 5 yr, height 1.80 ⫾ 0.05 m, body mass 77 ⫾ 8 kg,
maximal oxygen consumption (V
˙
O
2 max
) 61.8 ml·kg
⫺1
·min
⫺1
] who
competed regularly in local cycle races were recruited for participa-
tion in the study. All subjects were free from cardiovascular and
pulmonary disease as determined from a self-reporting medical ques-
tionnaire. All subjects had normal pulmonary function (Table 1).
Subjects were instructed to adhere to their normal diet and training
regimen throughout the duration of the study and to abstain from
participating in any strenuous exercise 24 hr prior to any tests. All
tests and procedures were approved by the Indiana University Insti-
tutional Review Board for Human Subjects, and all subjects provided
written informed consent to participate in the study.
Study design. Prior to commencing the study, subjects were famil-
iarized with all test procedures, including all respiratory muscle and
pulmonary function tests. Upon entering the study, subjects were
required to visit the laboratory on three separate occasions. During
session 1, subjects completed a medical and physical activity ques-
tionnaire, baseline pulmonary function tests (PFTs), and an incremen-
tal cycle ergometer test to the limit of exercise tolerance to determine
V
˙
O
2 max
and peak power output (W
max
). Sessions 2 and 3 each
consisted of a voluntary hyperpnea test and were completed pre- and
Address for reprint requests and other correspondence: T. D. Micklebor-
ough, Human Performance Laboratory, Dept. of Kinesiology, Indiana Univ.,
1025 E. 7th St., HPER 112, Bloomington, IN 47401 (e-mail: tmickleb
@indiana.edu).
J Appl Physiol 112: 127–134, 2012.
First published October 6, 2011; doi:10.1152/japplphysiol.00954.2011.
8750-7587/12 Copyright
©
2012 the American Physiological Societyhttp://www.jap.org 127
post-training intervention. Following the completion of the pretraining
voluntary hyperpnea test, subjects were randomly assigned in a
double-blind manner to either an inspiratory muscle training group
(IMT) or a placebo-controlled sham-training group (CON). Both
groups completed the prescribed daily training (IMT or CON) for
6 wk.
Pulmonary function and maximal inspiratory pressure measurements.
Pulmonary function tests were performed on all subjects in triplicate
according to the American Thoracic Society recommendations, which
requires the subject to perform at least three acceptable spirograms,
where two of the largest forced vital capacity (FVC), forced expira-
tory volume in1sFEV
1
, and forced expiratory flow at 25–75% of
vital capacity (FEF
25–75%
) values may not differ by more than 10%
(4a). The highest recorded value was reported. Maximal inspiratory
pressure (P
I
max
) was measured as an index of inspiratory muscle
strength using a portable hand-held mouth pressure meter (Micro
Medical, Kent, UK). All maneuvers were conducted in an upright-
seated position, and were initiated from residual lung volume (RV).
Measurements of P
I
max
were conducted at 30-s intervals, where the
variability of the best values was 5% or within 5 cmH
2
O (36); the
largest value was reported.
Maximal incremental exercise testing. A maximal incremental
cycling ergometer test was performed using a Monark cycle ergom-
eter (model 828E, Varberg, Sweden) to determine V
˙
O
2 max
and W
max
.
The test was initiated at a workload of 150 W and increased by 50 W
every 3 min until volitional exhaustion, or was terminated when the
subject’s cadence dropped by more than 10 rpm below their self-
selected pedal rate. Verification that V
˙
O
2 max
was achieved was
determined by a plateau (⬍150 ml) or a decrease in V
˙
O
2
during the
final 2 min of the incremental exercise test, respiratory exchange ratio
of greater than 1.1, or maximal heart rate exceeding 85% of predicted
(220 ⫺ age). At least two of these criteria were required for a valid
V
˙
O
2 max
test. The V
˙
O
2 max
reported was the highest 60-s average value
attained prior to volitional exhaustion.
Ventilatory and metabolic data were continuously monitored using
open-circuit, indirect calorimetry. Subjects breathed through a low-
resistance two-way non-breathing valve (Hans Rudolph 2700, Kansas
City, MO) that was connected on the expired side to a 5-liter mixing
chamber. Dried expired gases were continuously sampled at a rate of
300 ml/min for fractional concentrations of O
2
and CO
2
using an
Applied Electrochemistry S-3A oxygen analyzer and a CD-3A carbon
dioxide analyzer (Ametek, Thermox Instruments, Pittsburgh, PA).
Inspired and expired ventilation were measured using a pneumota-
chometer on both the inspired and expired side (Hans Rudolph 3813).
The pneumotachometer on the expired side was heated to 37°C (Hans
Rudolph pneumotachometer heater control). V
˙
E
was calculated from
the inspired ventilation.
Flow volume loops were collected during the final 30 s of each
minute during the V
˙
O
2 max
test and during the final 30 s of each minute
throughout each voluntary hyperpnea stage. Tidal volume loops were
computer averaged for ⬃12–15 breaths. The average tidal volume
loop was placed within a maximum flow volume loop, obtained at rest
(pre-exercise), based on a measurement of end-expiratory lung vol-
ume (EELV). EELV was determined by subtracting an inspiration to
maximal lung capacity (IC maneuver) from forced vital capacity
(FVC). Subjects performed an IC maneuver at 30 s and 50 s of each
minute during the exercise test.
Voluntary hyperpnea. The voluntary hyperpnea protocol required
subjects at rest (seated on the cycle ergometer) to mimic the exercise V
˙
E
from three workloads, each corresponding to 50, 75, and 100% of
V
˙
O
2 max
. Each target V
˙
E
was maintained for 4 min. To mimic the
mechanical parameters of exercise hyperpnea, the target V
˙
E
was achieved
by matching the exercise tidal volume (V
T
) and breathing frequency (f
b
),
which were held constant for both pre- and post-training (IMT and CON).
Subjects were paced for f
b
using an audio metronome, and real-time
visual feedback was provided for V
T
. Eucapnia was maintained through
inspiration of a premixed gas (5% CO
2
, 21% O
2
, balance N
2
) from a
Douglas bag that was connected to a two-way breathing valve via tubing
containing a humidifier. The O
2
cost of hyperpnea (V
˙
O
2RM
) was calcu
-
lated by subtracting the V
˙
O
2
measured during passive rest from the values
obtained during the mimic trial.
Training intervention. Following baseline testing, subjects were
assigned to either the IMT or CON group. The IMT group completed
30 dynamic inspiratory maneuvers twice daily (AM and PM session)
at a pressure-threshold load of 50% of PI
max
for 6 wk; this protocol
has previously been shown to elicit improvements in inspiratory
muscle function (7, 29, 30, 32). Subjects in the CON group completed
a sham training intervention, which consisted of 60 breaths, once daily
(AM or PM session) for 6 wk at ⬃15% of PI
max
; this protocol has
been shown to exhibit no changes in inspiratory muscle function (7,
30). Subjects were instructed to initiate each breath from residual lung
volume and to continue until total lung capacity. Breathing frequency
during the inspiratory efforts was reduced to prevent hyperventilation-
induced hypocapnea. All inspiratory training was performed using a
pressure-threshold training device (POWERbreathe, HaB Interna-
tional, Southam, UK).
Compliance to training was assessed by monitoring the cumulative
number of breaths completed during the intervention using a pressure
sensor suspended within the main body of the inspiratory muscle trainer
(30). An inspiratory effort was registered and counted when the negative
pressure generated during inspiration exceeded the set point on the
pressure switch. The cumulative number of pressure threshold
changes were recorded and computed into total number of breaths.
Daily physical activity and IMT training logs were kept by all subjects
Table 1. Pulmonary and respiratory muscle function
IMT (n ⫽ 8) Control
Pre Post Pre Post
Pulmonary Function
FVC, liters 5.78 ⫾ 0.67 5.79 ⫾ 0.78 5.97 ⫾ 0.62 6.00 ⫾ 0.52
%Predicted 100.7 ⫾ 11.9 100.8 ⫾ 14.1 110.0 ⫾ 9.8 110.8 ⫾ 10.1
FEV
1
, liters
4.88 ⫾ 0.78 4.89 ⫾ 0.77 4.83 ⫾ 0.61 4.84 ⫾ 0.54
%Predicted 105.0 ⫾ 16.5 105.0 ⫾ 16.7 111.7 ⫾ 11.9 112.0 ⫾ 10.4
FEV
1
/FVC, %
84.2 ⫾ 7.7 84.5 ⫾ 7.2 80.9 ⫾ 5.0 80.60 ⫾ 5.7
%Predicted 106.6 ⫾ 9.8 106.9 ⫾ 9.2 102.4 ⫾ 6.9 102.0 ⫾ 6.8
PEFR, liters 10.82 ⫾ 1.78 10.82 ⫾ 2.40 9.39 ⫾ 2.26 9.35 ⫾ 2.09
%Predicted 108.8 ⫾ 16.7 108.0 ⫾ 24.3 99.1 ⫾ 21.8 98.1 ⫾ 20.3
Respiratory Muscle Function
PI
max
(cmH
2
0)
116 ⫾ 15 142 ⫾ 19* 127 ⫾ 16 129 ⫾ 20
Values are reported as means ⫾ SD (n ⫽ 8). FVC, forced vital capacity; FEV
1
, forced expiratory volume in 1 s; PEFR, peak expiratory flow rate; PI
max
,
maximal inspiratory pressure. Predicted values from Morris (26). *Significant difference (P ⬍ 0.05) from pre-inspiratory muscle training (IMT).
128 INSPIRATORY MUSCLE TRAINING AND VOLUNTARY HYPERPNEA
J Appl Physiol • doi:10.1152/japplphysiol.00954.2011 • www.jap.org
throughout the duration of the study to monitor training volume/
intensity and adherence to training, respectively.
Data analysis. Data were analyzed using SPSS version 17.0 sta-
tistical software. The data were assessed for normality using the
Kolmogorov-Smirnov test, and Levene’s test was used to test for
homogeneity of variance between tests. Within and between group
interactions were analyzed using a split-plot 2 ⫻ 2 [time (pre vs. post)
by group (IMT vs. CON)] ANOVA. A priori simple main effects were
computed to determine time and group differences. Pearson product
moment correlation coefficients were used to assess the relationship
between the ventilatory parameters (V
˙
E
,f
b
,V
T
, and EELV) attained
during the maximal exercise test and voluntary hyperpnea. The
relationship between V
˙
O
2RM
and V
˙
E
during voluntary hyperpnea was
determined from regression analysis. Statistical significance was set at
P ⬍ 0.05. Values are reported as means ⫾ SD.
RESULTS
There was no significant difference in age, height, or weight
between the CON and IMT groups. Furthermore, pretraining
measures of V
˙
O
2 max
and power output (W
˙
max
) were not signifi
-
cantly different between the IMT and CON groups (64.3 ⫾ 9.1 vs.
59.1 ⫾ 4.2 ml·kg
⫺1
·min
⫺1
and 369 ⫾ 46 vs. 331 ⫾ 26 W,
respectively). Physical activity levels were not significantly dif-
ferent between (IMT and CON) or within (pre to post) groups.
Adherence to training was also high in both groups as demon-
strated by a compliance rate of 90% for both the IMT and CON
groups.
Pulmonary and respiratory muscle function. All pulmonary
function measures were within normal predictive values (26;
Table 1). There was no significant difference in pulmonary
function between CON and IMT and pre- or post-training in
either group. Baseline values for respiratory muscle strength
(P
I
max
) were not significantly different between the IMT and
CON groups. Following 6 wk of training, the IMT group
demonstrated a significant increase (P ⬍ 0.05) in P
I
max
of 22 ⫾
13.2%. There was no significant change in P
I
max
values from
pre- to post-training in the CON group.
Comparison of ventilatory parameters during exercise and
voluntary hyperpnea. The ventilator parameters attained during
maximal exercise and voluntary hyperpnea are presented in
Table 2. V
˙
E
was significantly increased (P ⬍ 0.05) across all
exercise intensities through a significant increase (P ⬍ 0.05) in
both f
b
and V
T
. There was no significant difference in EELV at
any exercise intensity. The time spent on inspiration expressed
as a percentage of total time of one breathing cycle or duty
cycle (Ti/TT) was not significantly different between 50 and
75% V
˙
O
2 max
, but was significantly increased (P ⬍ 0.05) at
100% V
˙
O
2 max
.V
˙
E
and breathing patterns (f
b
,V
T
, EELV) were
closely matched between the maximal incremental exercise test
and mimic trial (prior to training) for both the IMT and CON
groups as shown by significant correlations in V
˙
E
(IMT r ⫽
0.98, P ⬍ 0.05; CON r ⫽ 0.99, P ⬍ 0.05), f
b
(IMT r ⫽ 0.99,
P ⬍ 0.05; CON r ⫽ 0.99, P ⬍ 0.05), V
T
(IMT r ⫽ 0.95, P ⬍
0.05; CON r ⫽ 0.90, P ⬍ 0.05), and EELV (IMT r ⫽ 0.63,
P ⬍ 0.05; CON r ⫽ 0.80, P ⬍ 0.05).
Oxygen cost of voluntary hyperpnea. The curvilinear rela-
tionship between oxygen uptake (V
˙
O
2RM
) and V
˙
E
for all sub
-
jects (IMT and CON) at all levels of voluntary hyperpnea (r ⫽
0.88) is shown in Fig. 1. At higher levels of V
˙
E,
it is evident
Table 2. Ventilatory responses for exercise and voluntary hypernea (mimic)
50% V
˙
E
max
75% V
˙
E
max
100% V
˙
E
max
Exercise Mimic Exercise Mimic Exercise Mimic
IMT (n ⫽ 8)
V
˙
E
, l/min-BTPS
52.47 ⫾ 7.21 54.96 ⫾ 4.70 89.95 ⫾ 14.93 85.58 ⫾ 14.97 164.64 ⫾ 24.87 157.04 ⫾ 20.80
f
b
, breath/min
25 ⫾ 825⫾ 834⫾ 833⫾ 755⫾ 11 54 ⫾ 10
V
T
, l-BTPS
2.37 ⫾ 0.82 2.42 ⫾ 0.68 2.73 ⫾ 0.54 2.68 ⫾ 0.59 3.11 ⫾ 0.46 2.87 ⫾ 0.49
Ti/TT, % 45.1 ⫾ 2.0 44.3 ⫾ 5.1 46.2 ⫾ 2.2 43.7 ⫾ 5.0 47.7 ⫾ 1.5 48.5 ⫾ 3.5
EELV, %FVC 37.6 ⫾ 4.6 38.4 ⫾ 8.4 40.6 ⫾ 5.8 40.0 ⫾ 8.1 38.6 ⫾ 2.1 39.1 ⫾ 3.9
CON (n ⫽ 8)
V
˙
E
, l/min-BTPS
51.97 ⫾ 6.67 50.29 ⫾ 7.51 85.17 ⫾ 9.46 81.36 ⫾ 9.46 148.70 ⫾ 23.17 134.69 ⫾ 20.42
f
b
, breath/min
23 ⫾ 522⫾ 529⫾ 629⫾ 749⫾ 949⫾ 10
V
T
, l-BTPS
2.36 ⫾ 0.42 2.42 ⫾ 0.50 2.99 ⫾ 0.33 2.85 ⫾ 0.38 3.11 ⫾ 0.44 2.86 ⫾ 0.47
Ti/TT, % 46.3 ⫾ 3.4 45.9 ⫾ 2.1 48.9 ⫾ 2.5 45.2 ⫾ 2.6 49.8 ⫾ 2.2 48.2 ⫾ 4.1
EELV, %FVC 38.2 ⫾ 14.6 38.9 ⫾ 11.2 36.2 ⫾ 12.9 37.1 ⫾ 11.7 38.2 ⫾ 11.4 37.2 ⫾ 13.1
Values are reported as means ⫾ SD for the pretraining maximal incremental exercise test (exercise) and voluntary hyperpnea trial (mimic). V
˙
E
, minute
ventilation; BTPS, volume corrected to body temperature, ambient pressure saturated with water vapour; f
b
, breathing frequency; V
T
, tidal volume; Ti/TT, ratio
of inspiratory time to total time of a breath; EELV, end-expiratory lung volume; FVC, forced vital capacity. No significant difference (P ⬎ 0.05) was detected
between the exercise and mimic trials at any exercise intensity.
Fig. 1. Individual subject values for the oxygen cost of voluntary hyperpnea
(V
˙
O
2RM
) at low (50% V
˙
O
2max
), moderate (75% V
˙
O
2 max
), and high (100%
V
˙
O
2max
) levels of V
˙
E
for all subjects pretraining. ●, Preinspiratory muscle
training (IMT);
‘
, precontrol (CON). The equation for the line: V
˙
O
2RM
(ml·kg
⫺1
·min
⫺1
) ⫽ 0.0003·V
E
(l/min)
2
⫺ 0.0045·V
E
(l/min) ⫹ 0.9787 (r ⫽
0.88, P ⬍ 0.05). Dashed lines represent 95% confidence intervals.
129INSPIRATORY MUSCLE TRAINING AND VOLUNTARY HYPERPNEA
J Appl Physiol • doi:10.1152/japplphysiol.00954.2011 • www.jap.org
that an increase in V
˙
E
was disproportionate to the increase in
V
˙
O
2RM
. There was no significant difference in pre- and post-
training V
˙
E
between the IMT and CON groups at 50 or 75%
V
˙
O
2 max
, but was significantly higher (P ⬍ 0.05) in the IMT
group at 100% V
˙
O
2 max
both pre- and post-training. Pre- and
post-training measures of V
˙
E
during the mimic trials were not
significantly different within groups (IMT or CON) at 50, 75,
or 100% V
˙
O
2 max
. The O
2
cost of voluntary hyperpnea data for
the IMT and CON groups, pre- and post-training are shown in
Table 3. At ventilatory workloads equivalent to 50% V
˙
O
2 max
(V
˙
E
⬃50 –55 l), the O
2
cost of ventilation per liter of V
˙
E
(V
˙
O
2RM
/V
˙
E
) averaged ⬃2.0 ml O
2
·l
⫺1
·min
⫺1
in both the IMT
and CON groups. When V
˙
E
increased to ⬃150 l/min at 100%
V
˙
O
2 max
in the IMT group, V
˙
O
2RM
/V
˙
E
increased to 3.7 and to
2.6 ml O
2
·l
⫺1
·min
⫺1
in the CON group (V
˙
E
⬃135 l/min).
Assuming that the O
2
cost of ventilation does not differ be
-
tween voluntary hyperpnea and exercise, it is possible to deter-
mine the percentage of the total V
˙
O
2
(V
˙
O
2T
) that is used to achieve
a given V
˙
E
during exercise. During exercise at 50% V
˙
O
2 max
pre-IMT, the ventilatory load required 5.1 ⫾ 2.5% of V
˙
O
2T
and
increased to 5.7 ⫾ 1.4% of V
˙
O
2T
at 75% V
˙
O
2 max
and 11.7% ⫾
2.5% of V
˙
O
2T
at 100% V
˙
O
2 max
(Fig. 2A).
Post-IMT, the ventila-
tory requirement for the same absolute V
˙
E
significantly decreased
(P ⬍ 0.05) to 4.2 ⫾ 1.4 and 8.1 ⫾ 3.5% of V
˙
O
2T
at 75% and
100% V
˙
O
2 max
, respectively. There was no significant change in
V
˙
O
2T
at 50% V
˙
O
2 max
from pre- to post-IMT or at any level of V
˙
E
from pre- to post-CON (Fig. 2B). Individual changes in V
˙
O
2RM
at
100% V
˙
O
2 max
in response to training are shown in Fig. 3, A and
B. Six subjects in the IMT group demonstrated decreased V
˙
O
2RM
following training. No significant change was observed in V
˙
O
2RM
from pre- to post-training in the CON group.
Ventilatory parameters during voluntary hyperpnea pre-
and post-intervention. The ventilatory parameters attained dur-
ing voluntary hyperpnea for both the IMT and CON groups are
Table 3. Oxygen cost of voluntary hyperpnea
IMT (n ⫽ 8) CON (n ⫽ 8)
Pre Post Pre Post
50% V
˙
O
2max
V
˙
O
2RM
/V
˙
E
,mlO
2
/l
2.08 ⫾ 0.95 1.99 ⫾ 1.03 2.07 ⫾ 0.49 1.91 ⫾ 0.60
V
˙
E
, l/min-BTPS
54.96 ⫾ 4.70 59.43 ⫾ 9.13 50.29 ⫾ 7.51 54.49 ⫾ 9.80
V
˙
O
2RM,
ml·kg
⫺1
·min
⫺1
1.56 ⫾ 0.77 1.60 ⫾ 1.12 1.36 ⫾ 0.38 1.44 ⫾ 0.52
V
˙
O
2T
, ml·kg
⫺1
·min
⫺1
31.01 ⫾ 5.72 – 34.17 ⫾ 4.62 –
75% V
˙
O
2max
V
˙
O
2RM
/V
˙
E
,mlO
2
/l
2.31 ⫾ 0.53 1.70 ⫾ 0.77 1.92 ⫾ 0.65 1.75 ⫾ 0.99
V
˙
E
, l/min-BTPS
85.58 ⫾ 14.97 87.87 ⫾ 13.86 81.36 ⫾ 9.46 81.46 ⫾ 11.16
V
˙
O
2RM,
ml·kg
⫺1
·min
⫺1
2.83 ⫾ 0.98 2.06 ⫾ 1.28* 2.38 ⫾ 1.22 2.03 ⫾ 1.20
V
˙
O
2T
, ml·kg
⫺1
·min
⫺1
48.68 ⫾ 6.01 – 45.21 ⫾ 4.61 –
100% V
˙
O
2max
V
˙
O
2RM
/V
˙
E
,mlO
2
/l
3.68 ⫾ 0.75† 2.59 ⫾ 0.88* 2.59 ⫾ 0.81 2.56 ⫾ 1.00
V
˙
E
, l/min-BTPS
157.04 ⫾ 20.08† 152.99 ⫾ 18.94‡ 134.69 ⫾ 20.42 139.91 ⫾ 21.58
V
˙
O
2RM,
ml·kg
⫺1
·min
⫺1
7.61 ⫾ 2.17† 5.33 ⫾ 2.81* 4.36 ⫾ 1.69 4.87 ⫾ 1.75
V
˙
O
2T
, ml·kg
⫺1
·min
⫺1
64.28 ⫾ 9.08 – 59.10 ⫾ 4.23 –
Values are reported as means ⫾ SD. V
˙
O
2RM
/V
˙
E
, oxygen cost of ventilation, per liter of V
˙
E
;V
˙
O
2RM
, respiratory muscle oxygen consumption; V
˙
O
2T
, oxygen
consumption achieved at the corresponding workload during the maximal incremental exercise test. *, †, ‡ Significant difference (P ⬍ 0.05) from pre-IMT,
pre-CON, and post-CON, respectively.
Fig. 2. The oxygen cost of voluntary hyperpnea (V
˙
O
2RM
) and V
˙
O
2RM
expressed as a percentage of total oxygen consumption (V
˙
O
2T
) graphed against V
˙
E
at low
(50% V
˙
O
2 max
), moderate (75% V
˙
O
2 max
), and high (100% V
˙
O
2 max
) exercise intensities for both IMT (A) and CON (B) groups, pre- and post-training (means ⫾
SE). ●, Pre-IMT; Œ, post-IMT;
‘
, pre-CON; ⌬, post-CON. *Significant difference (P ⬍ 0.05) from pre-IMT.
130 INSPIRATORY MUSCLE TRAINING AND VOLUNTARY HYPERPNEA
J Appl Physiol • doi:10.1152/japplphysiol.00954.2011 • www.jap.org
shown in Table 4. There was no significant difference in V
˙
E
,
V
T
, f
b
, Ti/TT, EELV, end-inspiratory lung volume (EILV) at
any level of voluntary hyperpnea from pre- to post-training in
either the IMT or CON group. Peak inspiratory (PF
I
) and
expiratory flow (PF
E
) rates significantly increased (P ⬍ 0.05)
during all mimic trials as V
˙
E
increased. Following training,
there was a significant decrease (P ⬍ 0.05) in PF
I
or PF
E
at
50% V
˙
O
2 max
in both the IMT and CON groups. There was no
significant change in PF
I
or PF
E
at 75% V
˙
O
2 max
or 100%
V
˙
O
2 max
in either the IMT or CON group.
Heart rate (HR) during voluntary hyperpnea, prior to train-
ing, increased to 77 ⫾ 8 and 79 ⫾ 7 beats/min at 75% V
˙
O
2 max
in the IMT and CON groups, respectively, and further in-
creased to 93 ⫾ 7 (IMT) and 88 ⫾ 11 beats/min (CON) at
100% V
˙
O
2 max
. Following IMT, HR significantly decreased
(P ⬍ 0.05) to 73 ⫾ 6 beats/min at 75% V
˙
O
2 max
and to 86 ⫾
4 beats/min at 100% V
˙
O
2 max
. There was no significant change
in HR at any level of voluntary hyperpnea following training in
the CON group.
DISCUSSION
To our knowledge this study is the first to investigate the
influence of IMT on the oxygen cost of voluntary hyperpnea.
The main findings of the present study are that the relationship
between increasing ventilatory workloads and the O
2
cost of
voluntary hyperpnea is curvilinear in trained cyclists and that 6
wk of pressure threshold IMT significantly reduced the O
2
cost
of V
˙
E
at high ventilatory workloads. Importantly, the finding
that V
˙
O
2RM
is reduced at a V
˙
E
above 50% V
˙
O
2 max
suggests that
IMT may reduce the energy requirements of the respiratory
musculature in maintaining a given V
˙
E
.
The oxygen cost of voluntary hyperpnea prior to training
ranged from ⬃4% of V
˙
O
2T
at low intensity exercise to ⬃11%
Fig. 3. Individual pre- and post-training V
˙
O
2RM
values obtained during maximal voluntary hyperpnea (100% V
˙
O
2max
) for both IMT (A) and CON (B) groups.
●, Individual IMT subjects; Œ, mean IMT values;
‘
, individual CON subjects; ⌬, mean CON values. *Significant difference (P ⬍ 0.05) from pre-IMT.
Table 4. Ventilatory parameters during voluntary hyperpnea
50% V
˙
O
2max
75% V
˙
O
2max
100% V
˙
O
2max
Pre Post Pre Post Pre Post
IMT (n ⫽ 8)
V
T
, l -BTPS
2.42 ⫾ 0.68 2.61 ⫾ 0.73 2.68 ⫾ 0.59 2.75 ⫾ 0.51 2.87 ⫾ 0.49 2.91 ⫾ 0.24
f
b
, breath/min
25 ⫾ 825⫾ 833⫾ 734⫾ 854⫾ 10 53 ⫾ 7
Ti/TT, % 44.3 ⫾ 5.1 43.1 ⫾ 6.6 43.7 ⫾ 5.0 44.96 ⫾ 4.6 48.5 ⫾ 3.5 46.8 ⫾ 3.5
EELV, %FVC 38.40 ⫾ 8.4 39.3 ⫾ 8.4 40.0 ⫾ 8.1 37.3 ⫾ 7.0 39.1 ⫾ 3.9 36.9 ⫾ 4.1
EILV, %FVC 77.7 ⫾ 10.3 80.7 ⫾ 15.8 88.3 ⫾ 8.4 86.1 ⫾ 6.0 89.8 ⫾ 4.6 87.0 ⫾ 5.5
PF
I
, l/s
3.51 ⫾ 0.98 5.33 ⫾ 0.78* 5.41 ⫾ 1.52 5.92 ⫾ 1.29 7.72 ⫾ 0.90 8.10 ⫾ 1.39
PF
E
, l/s
3.29 ⫾ 0.74 5.18 ⫾ 1.02* 5.14 ⫾ 0.99 6.02 ⫾ 0.95 8.77 ⫾ 1.79 8.23 ⫾ 1.21
Control (n ⫽ 8)
V
T
, l-BTPS
2.42 ⫾ 0.50 2.42 ⫾ 0.31 2.85 ⫾ 0.38 2.90 ⫾ 0.34 2.86 ⫾ 0.47 2.94 ⫾ 0.42
f
b
, breath/min
22 ⫾ 523⫾ 529⫾ 729⫾ 649⫾ 10 48 ⫾ 9
Ti/TT, % 45.9 ⫾ 2.1 47.0 ⫾ 2.7 45.2 ⫾ 2.6 46.1 ⫾ 2.8 48.2 ⫾ 4.1 45.4 ⫾ 3.1
EELV, %FVC 38.9 ⫾ 11.2 40.4 ⫾ 8.1 37.1 ⫾ 11.7 36.7 ⫾ 6.5 37.2 ⫾ 13.1 37.0 ⫾ 11.9
EILV, %FVC 79.1 ⫾ 13.3 80.7 ⫾ 8.3 85.3 ⫾ 8.3 85.0 ⫾ 5.4 85.4 ⫾ 8.6 86.0 ⫾ 8.4
PF
I
, l/s
2.87 ⫾ 1.01 4.78 ⫾ 0.73* 5.15 ⫾ 1.21 5.39 ⫾ 0.93 6.92 ⫾ 0.92 7.27 ⫾ 1.54
PF
E
, l/s
3.07 ⫾ 1.45 5.04 ⫾ 0.77* 5.36 ⫾ 0.83 5.54 ⫾ 1.43 7.67 ⫾ 1.18 7.43 ⫾ 0.79
Values are reported as means ⫾ SD. EILV, end-inspiratory lung volume; PF
I
, peak inspiratory flow rate; PF
E
, peak expiratory flow rate achieved at the
corresponding ventilation during the maximal incremental exercise test. *Significant difference (P ⬍ 0.05) from pretraining.
131INSPIRATORY MUSCLE TRAINING AND VOLUNTARY HYPERPNEA
J Appl Physiol • doi:10.1152/japplphysiol.00954.2011 • www.jap.org
of V
˙
O
2T
at maximal intensity exercise, thus supporting previ
-
ous evidence that the respiratory muscles require 10 –15% of
total oxygen consumption during maximal exercise (3, 17).
The increase in the percentage of V
˙
O
2T
devoted to the O
2
cost
of voluntary hyperpnea from low- to high-intensity exercise
demonstrates a curvilinear relationship (r ⫽ 0.88), with the O
2
cost per liter of V
˙
E
increasing with higher levels of hyperven
-
tilation. This finding is consistent with previous data that
showed that the respiratory muscle demand for O
2
is positively
correlated to V
˙
E
(r ⫽ 0.81) and the W
b
(r ⫽ 0.76) (1). At
submaximal ventilatory workloads (⬃75% V
˙
O
2max
), the pre
-
training O
2
cost per liter of V
˙
E
was 2.13 ⫾ 0.65 ml O
2
/l for all
subjects (n ⫽ 16) and significantly increased to 3.14 ⫾ 0.98 ml
O
2
/l (P ⬍ 0.05) at maximal ventilatory workloads (⬃100%
V
˙
O
2 max
). These findings are comparable to those reported in
the study by Aaron et al. (1) that reported mean values of 1.79
ml O
2
/l for V
˙
O
2RM
/V
˙
E
at moderate-intensity exercise (⬃70%
V
˙
O
2 max
) and 2.85 ml O
2
/l at high intensity (100% V
˙
O
2 max
).
Prior to training, the O
2
cost of V
˙
E
was significantly higher
in the IMT group compared with the CON group at ventilatory
workloads corresponding to 100% V
˙
O
2 max
. Importantly, the
level of V
˙
E
achieved during voluntary hyperpnea in the IMT
group was also significantly higher than the CON group, which
may explain the pretraining difference in the O
2
cost of V
˙
E
between the IMT and CON groups. Specifically, at higher
levels of V
˙
E
the increase in the O
2
cost of V
˙
E
is disproportion
-
ate to the increase in V
˙
E
, where small changes in V
˙
E
result in
greater changes in the O
2
cost of V
˙
E
; thus the higher levels of
V
˙
E
as demonstrated in the IMT would lead to greater O
2
cost.
The increase in energy expenditure as V
˙
E
increases can be
attributed to a variety of sources of respiratory muscle work,
including the elastic recoil of the chest and lung wall, airway
resistance (4, 15), increased EELV (9), and high muscle
shortening velocities (19, 23). It has been suggested that as
tidal breathing approaches the maximal limits for inspiratory
muscle pressure development and expiratory flow rates, energy
expenditure may increase to overcome the additional respira-
tory muscle work (3). Conversely, if one or more of the
additional sources of respiratory muscle work are reduced as a
result of IMT, it is reasonable to suggest that the increase in the
O
2
cost maybe attenuated.
In the present study, following 6 wk of IMT, V
˙
O
2RM
was
significantly reduced from pretraining values at submaximal
and maximal levels of ventilation. The O
2
cost of voluntary
hyperpnea expressed as a percentage of V
˙
O
2T
was reduced by
1.5% at a V
˙
E
corresponding to 75% V
˙
O
2max
following IMT.
The greatest reduction in the O
2
cost of voluntary hyperpnea
was observed at V
˙
O
2 max
, where V
˙
O
2RM
was significantly re
-
duced from 11% of V
˙
O
2T
to 8% V
˙
O
2T
following IMT. These
data therefore suggest that IMT may decrease the respiratory
muscle work associated with voluntary hyperpnea. Harms et al.
(17) showed that by unloading the respiratory muscles (via a
proportional-assist ventilator) and consequently decreasing the
W
b
by ⬃50%, whole body O
2
consumption was reduced by
⬃7% during exercise. Recently, Ray et al. (28) showed that 4
wk of respiratory muscle training (inspiratory and expiratory)
resulted in a significant decrease in both the inspiratory and
expiratory work of breathing during underwater swimming at
70% V
˙
O
2 max
, suggesting that an IMT-mediated reduction in
the W
b
may consequently lead to a reduction in O
2
consump
-
tion during exercise. The findings from this study provided
novel evidence to support this premise by demonstrating a
reduction in the O
2
demand of the respiratory muscles during
high levels of voluntary hyperpnea following IMT.
Oxygen consumption during exhaustive treadmill running at a
workload corresponding to ⬃80% V
˙
O
2 max
was previously shown
to be attenuated following respiratory muscle training (21, 24).
Reduced V
˙
O
2
during whole body exercise was associated with
reduced f
b
and V
˙
E
, indicating that IMT may reduce the W
b
and/or
improve ventilatory efficiency (21, 24). Increased ventilatory
demand was previously shown to elicit a sympathetically medi-
ated metaboreflex (33), which increases heart rate and mean
arterial pressure (MAP), reducing blood flow to the limb locomo-
tor muscles during exercise (16) and potentially reducing whole
body endurance performance (18). Furthermore, Witt et al. (37)
showed that IMT attenuates this increase in HR and MAP,
presumably by reducing or delaying the sympathetically mediated
reflex. The finding that IMT can reduce HR during voluntary
hyperpnea in the present study is consistent with previous studies
that demonstrated a reduced cardiovascular response following
IMT (13, 37). Furthermore, our data are novel in demonstrating
that IMT can reduce the O
2
demands of the respiratory muscula
-
ture in combination with a reduction in HR, indicating that IMT
may facilitate increased O
2
availability to the active limb loco
-
motor muscles through an attenuated metaboreflex.
Although the work of breathing was not directly measured in
the present study, we showed that IMT reduced the O
2
demand of
voluntary hyperpnea. One possible explanation for the IMT-
induced reduction in the O
2
cost of ventilation could relate to
changes in dynamic lung volumes during hyperpnea. Specifically,
if voluntary hyperpnea is performed at an increased EELV, the
respiratory muscles will likely operate at a less than optimal length
and thus increase the elastic work and elevate the O
2
cost of V
˙
E
(10). It is plausible that stronger respiratory muscles may operate
at a more optimal length of the force-tension spectrum and
therefore lower the O
2
cost of V
˙
E
. However, in the current study,
the mechanical parameters of voluntary hyperpnea were con-
trolled by matching V
T
and f
b
, which resulted in no significant
difference in EELV from pre- to post-IMT. Therefore, these data
suggest that changes in the O
2
cost of hyperpnea following IMT
did not occur as a function of changes in EELV.
The 22% increase in respiratory muscle strength shown in the
present study is similar in magnitude to those previously reported
using pressure-threshold IMT (11, 22, 30, 32, 37). Respiratory
muscle structure has also been shown to change following IMT,
with an increase in diaphragm thickness (11, 12) and hypertrophy
of type II muscle fibers of the external intercostal muscles (27)
being reported. Therefore, the relationship between muscle fiber
cross-sectional area and muscle strength may, in part, explain the
reduction in the O
2
cost of V
˙
E
. Specifically, for a given ventilatory
demand, an increase in inspiratory muscle strength may result in
the recruitment of fewer muscle fibers or delay the recruitment of
accessory respiratory muscles, thereby lowering the O
2
require
-
ment for voluntary hyperpnea.
While the present study has shown that IMT decreases V
˙
O
2
during voluntary hyperpnea, determining the mechanism respon-
sible for this reduction is complex, due to an array of factors that
contribute toward the energy requirements of ventilation. These
sources have been shown to include both maximal and operational
flow rates. Specifically, it was demonstrated that by increasing the
muscle shortening velocity for a given inspiratory pressure (in-
creased inspiratory flow rate) oxygen consumption was increased
132 INSPIRATORY MUSCLE TRAINING AND VOLUNTARY HYPERPNEA
J Appl Physiol • doi:10.1152/japplphysiol.00954.2011 • www.jap.org
(19, 23); thus it is possible that by decreasing the shortening
velocity of the respiratory muscle during contraction, O
2
con
-
sumption may be accordingly reduced. However, the findings
from the present study showed no change in inspiratory flow rates
at high levels of voluntary hyperpnea following IMT, indicating
that the reduction in V
˙
O
2
following IMT was not related to a
change in inspiratory muscle shortening velocity. It is possible
that the reduction in V
˙
O
2
following IMT may be related to a
change in resistance to airflow, where energy expenditure is
increased when tidal breathing encroaches on the maximal limits
for flow (3, 4, 15). Aaron et al. (3) demonstrated that individuals
who reached their reserve for expiratory flow and inspiratory
muscle pressure development required 13–15% of V
˙
O
2T
com
-
pared with ⬃10% of V
˙
O
2T
for non-flow-limited individuals. Thus,
an increase in maximal expiratory flow rates or inspiratory pres-
sure development would increase the ventilatory reserve, thereby
increasing the maximal limits for ventilation. The findings of this
study are consistent with previous studies that showed that max-
imal expiratory flow rates remained unchanged following a period
of IMT (14, 20, 21, 24). In contrast, some studies demonstrated an
increase in maximal inspiratory flow rates following IMT (24, 25,
35); however, this change would presumably be a consequence of
increased inspiratory muscle shortening velocity, which would
increase V
˙
O
2
(19, 23). Thus the findings of the present study
suggest that the observed reduction in V
˙
O
2
following IMT is not
related to a change in either inspiratory or expiratory flow rates.
Conclusion. The present study provides novel evidence that
IMT reduces the O
2
cost of voluntary hyperpnea in highly
trained cyclists. This IMT-mediated reduction in the O
2
cost of
voluntary hyperpnea suggests that reducing the O
2
require
-
ments of the respiratory muscles may facilitate an increase in
O
2
availability to the active muscles during exercise. Thus
these data may provide an insight into the possible mechanisms
underpinning the previously reported improvements in whole
body endurance performance following IMT.
DISCLOSURES
The inspiratory muscle training devices were provided by POWERbreathe,
HaB International Ltd., Southam, UK.
AUTHOR CONTRIBUTIONS
Author contributions: L.A.T., R.F.C., J.M.S., and T.D.M. conception and
design of research; L.A.T., S.L.T.-L., and D.P.W. performed experiments;
L.A.T., S.L.T.-L., R.F.C., J.M.S., D.P.W., and T.D.M. analyzed data; L.A.T.,
S.L.T.-L., R.F.C., J.M.S., and T.D.M. interpreted results of experiments;
L.A.T. prepared figures; L.A.T., S.L.T.-L., R.F.C., J.M.S., D.P.W., and T.D.M.
drafted manuscript; L.A.T., S.L.T.-L., R.F.C., J.M.S., D.P.W., and T.D.M.
edited and revised manuscript; L.A.T., S.L.T.-L., R.F.C., J.M.S., D.P.W., and
T.D.M. approved final version of manuscript.
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