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Respiratory Physiology & Neurobiology 173 (2010) 115117

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Respiratory Physiology & Neurobiology


journal homepage: www.elsevier.com/locate/resphysiol

Reply to Letter to the Editor


Assessment of respiratory muscle training effects
Dear Editor,
After reading with great attention the letter by Radtke and
Benden about the study we recently published on the effects of
respiratory muscle training (RMT) on maximum aerobic power
(V O2 max ) in humans (Esposito et al., 2010), we would like to comment on some points that have been raised. After having reminded
that the main focus of our study was to assess the effects of RMT
on V O2 max in normoxia and hypoxia, we point out the following.
1. Validity of maximal inspiratory mouth pressure (PImax )
determination maneuver
In our study, participants familiarized with PImax maneuver
46 times when they rst reported to the laboratory for familiarization purposes. The day of the rst test, after warm-up trials,
participants repeated PImax determination 3 times, with a period
of 3 min of rest in between. PImax was then assessed as the highest value among the 3 trials. After training, the same procedure
was followed. As a result of RMT, PImax increased signicantly
from 69 5 cm H2 O to 121 10 cm H2 O. We tried to keep intrasubject variability as small as possible by using the same operator
to perform all measurements, both before and after RMT. This
way, possible inter-technician bias, which can account for up to
12% of differences in PImax (Enright et al., 1994), could be possibly
avoided.
We measured PImax from functional residual capacity (FRC)
rather than from residual volume (RV), as stated in the methods section. Indeed, inspiratory muscle strength is overestimated at levels
below FRC due to the elastic recoil pressure of the thorax (Agostoni
and Rahn, 1960). Changes in the length-tension relationship of
the respiratory muscles might also contribute to these differences
(Windisch et al., 2004). In studies comparing both modalities, PImax
values obtained at RV were signicantly higher than those obtained
at FRC in the same subjects (Uldry and Fitting, 1995; Windisch et
al., 2004).
Radtke and Benden question the validity of this measure in our
study, stating that the pre-training values were far below of those
previously reported in healthy subjects (Leith and Bradley, 1976;
Uldry and Fitting, 1995; Windisch et al., 2004; Terzi et al., 2009). It
seemed to them, indeed, as if technical problems and/or a learning
effect, rather than a true training effect, contributed to the large
increase in this variable. In our study, PImax was determined by
a digital pressure monitor (S&M Instrument Company Inc., mod.
PortaResp, Doylestown, PA), which had a 1-mm orice to prevent
the subject from producing articially high inspiratory pressures

DOI of original article:10.1016/j.resp.2010.07.007.


1569-9048/$ see front matter 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.resp.2010.07.008

with the muscles of the buccal cavity (Black and Hyatt, 1969). The
device was carefully calibrated with a mercury manometer before
any testing session. Multiple regression analysis did not disclose
any signicant difference between pre- and post-RMT calibration
curves and no signicant differences were found between the
regression lines and the identity line, as shown in Fig. 1. Moreover,
two-way (trial time) analysis of variance (ANOVA) for repeated
measures showed a signicant difference between pre- and postRMT values (P = 0.002), but no differences among trials (P = 0.668)
and no interactions (P = 0.597). Thus, it can be reasonably concluded
that during the pre-RMT testing sessions a learning effect was either
not present, or at least minimal. Furthermore, during the training period, participants did not perform any PImax measurements,
which would exclude a learning effect due to pre-RMT maneuvers
in the post-RMT testing session. Concerning pre-training absolute
values, provided that the instrumentation was correctly calibrated
and the maneuvers supervised by experts, we agree that our PImax
values were lower than reported by others. However, they t into
the normal range dened by Evans and Whitelaw (2009), as shown
in Fig. 2. Also Hautmann et al. (2000) questioned what is the lower
limit of the normal range of PImax . They proposed a prediction equation for PImax , which takes into account age and body mass index
(BMI), both independent predictors of inspiratory muscle strength
(Hautmann et al., 2000). The formula for healthy male subjects is
the following:
PImax = (0.158 BMI) (0.051 age) + 8.22
the lower limit of the normal range being 60% of the value determined from the equation.
In our study, average age and BMI were 24 4 years and
23 3, respectively. Thus, resolving the equation described above,
our values are higher than the lower physiological limit (see
Fig. 2).
2. Effectiveness of respiratory muscle training
Radtke and Benden question whether the training volume was
sufcient to induce gains in respiratory muscle strength. Moreover,
they reported different functional respiratory muscle adaptations
for endurance RMT and inspiratory muscle training, with the latter training modality, but not the former, inducing increases in
PImax .
Our study involved nine healthy, moderately active, collegiate
students. They reported to the laboratory for each training session, which was always performed under expert supervision. The
training protocol lasted 8 weeks (5 training sessions per week,
1020 min each including warm-up) and was performed by means
of a specic device (SpiroTiger Medical, Idiag AG, Fehraltorf,
Switzerland), which allowed a personalized respiratory training
through deep inspirations and expirations without hypocapnia.
During the rst week, participants familiarized with instrumen-

116

Reply to Letter to the Editor / Respiratory Physiology & Neurobiology 173 (2010) 115117

tory workload was: volume of the bag 3.29 0.04 L (+9%; P < 0.05),
respiratory rate of 36.0 0.1 b min1 (+15%; P < 0.05), for a total
amount of time of 824 12 s (+109%; P < 0.05), per training session. According to the instrumentation working modality, to allow
a breathing pattern under isocapnic hyperpnea, tidal volume (VT )
during training was 30% higher than the respiratory bag volume.
Thus, at the beginning of RMT, VT was 76% of the vital capacity (VC),
while at the end of training VT was 79% of VC, making questionable
whether the training in our work was aimed to endurance and not
to strength performance, as supposed by Radtke and Benden. In
other studies, subjects trained with VT set at 5060% of VC, and
respiratory rate adjusted accordingly to maintain a certain amount
of ventilation per training session (Spengler et al., 1999; Verges
et al., 2009). It is likely that the differences in VT between those
studies and ours could explain different training session durations.
Moreover, underestimation of the training bag volume with respect
to VC, or other spirometric parameters, could have accounted for
longer training session in other studies.
Fig. 1. Calibration curves of the digital pressure monitor with the mercury
manometer, before () and after () 8 weeks of RMT. Multiple regression analysis, did not show signicant differences between the two calibration curves
(P > 0.05). Thus, a single regression line was drawn and plotted against the identity line (dashed line). No signicant differences were found (P > 0.05) between
the calibration line and the identity line. The mercury manometer unit (mm Hg)
was converted in cm H2 O according to the International System of Units
(1 mm Hg = 1.359506 cm H2 O).

tation and operators tried to identify the most efcient workload


to start with. Participants started RMT with the following average
initial workload: volume of the respiratory bag of 3.01 0.02 L, respiratory rate of 31.3 0.2 b min1 , for a total amount of time of
393 14 s per training session (warm-up excluded). The volume
and the frequency of respiratory cycles were increased progressively every week, according to participants response to training
workloads. At the end of the training period, participants respira-

3. Spirometric parameters
Pulmonary function tests, usually performed and reported also
in other studies, were carried out to assess the effectiveness of the
RMT protocol. After RMT, while total lung capacity (TLC) did not
change, VC increased signicantly by 7% and RV decreased signicantly by 20%. Moreover, forced expired volume in the 1st s
(FEV1 ) and forced inspiratory ow rate at 50% from the beginning
of the inspiration (FIF50% ) increased signicantly by 9 and 47%,
respectively. Lastly, after RMT, a signicant decrease in total airway resistances (RAW ) by 17% took place. Together with the large
increase in PImax previously discussed, these results clearly suggest that the training protocol did have an effect on pulmonary and
respiratory function.
Although previous reports did not show changes in pulmonary
function after RMT (Lindholm et al., 2007; Verges et al., 2008, 2009;

Fig. 2. Relationship between reference and lower limit of normal (LLN) in male maximal inspiratory pressure (MIP) versus age (from Evans and Whitelaw, 2009). Average
PImax values from Esposito et al. study (2010), before () and after () RMT are drawn over the graph.

Reply to Letter to the Editor / Respiratory Physiology & Neurobiology 173 (2010) 115117

Keramidas et al., 2010), other authors found signicant improvements after training (Sonetti et al., 2001; Wells et al., 2005; Enright
et al., 2006; Wylegala et al., 2007).
4. Conclusions
In conclusion, we can reasonably reject the hypothesis that the
results of Esposito et al. (2010) were biased by a learning effect
and/or measurement errors. However, we agree with Radtke and
Benden that more precise guidelines are needed to non-invasively
assess the effects of RMT on pulmonary and respiratory function.
Indeed, differences in training devices (isocapnic hyperpnoea or
resistive) and modalities, in training intensity and duration, in initial workload assessment and workload adjustments throughout
the training period could signicantly affect RMT outcome.
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Fabio Esposito
Eloisa Limonta
Giampiero Alberti
Arsenio Veicsteinas
Department of Sport, Nutrition and Health Sciences,
University of Milan, Via G. Colombo 71, I-20133
Milan, Italy
Guido Ferretti a,b
Department of Biomedical Sciences and
Biotechnologies, University of Brescia, V.le Europa 11,
I-25123 Brescia, Italy
b Department of Basic Neuroscience, University of
Geneva, 1 rue Michel Servet, CH-1211 Geneva 4,
Switzerland
a

Corresponding

author. Tel.: +39 02 5031 4649;


fax: +39 02 5031 4630.
E-mail address: fabio.esposito@unimi.it
(F. Esposito)

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