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Respiratory Physiology & Neurobiology 188 (2013) 15–20

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Respiratory Physiology & Neurobiology

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Chest wall volumes during inspiratory loaded breathing in COPD patients

Mariana Alves Coutinho Myrrha a , Danielle Soares Rocha Vieira a , Karoline Simões Moraes a ,
Susan Martins Lage a , Verônica Franco Parreira a,b , Raquel Rodrigues Britto a,b,∗
Rehabilitation Science Graduation Program, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
Department of Physical Therapy, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: Chest wall volumes and breathing patterns of 13 male COPD patients were evaluated at rest and during
Accepted 15 April 2013 inspiratory loaded breathing (ILB). The sternocleidomastoid (SMM) and abdominal muscle activity was
also evaluated. The main compartment responsible for the tidal volume at rest and during ILB was the
Keywords: abdomen. During ILB patients exhibited, in addition to increases in the ratio of inspiratory time to total
Chest wall time of the respiratory cycle and minute ventilation, increases (p < 0.05) in the chest wall tidal volume
Breathing exercises
by an increase in abdomen tidal volume as a result of improvement of end chest wall inspiratory vol-
Chronic obstructive pulmonary disease
ume without changing on end chest wall expiratory volume. The SMM and abdominal muscle activity
Optoelectronic plethysmography
increased 63.84% and 1.94% during ILB. Overall, to overcome the load imposed by ILB, COPD patients
Respiratory muscle training improve the tidal volume by changing the inspiratory chest wall volume without modifying the pre-
dominant mobility of the abdomen at rest and without affecting the end chest wall expiratory volume.

© 2013 Elsevier B.V. All rights reserved.

1. Introduction To reduce these consequences, the Joint American College of

Chest Physicians/American Association of Cardiovascular and Pul-
The breathing patterns of patients with chronic obstructive pul- monary Rehabilitation recommend inspiratory muscle training
monary disease (COPD) are abnormal, especially in patients with (IMT) with inspiratory loaded breathing at least 30% of the maximal
pulmonary hyperinflation (Aliverti et al., 2004; McKenzie et al., inspiratory pressure (MIP) (Lotters et al., 2002) as part of rehabil-
2009). Airflow obstructions and mechanical disadvantages of the itation programs for patients with COPD (American Association of
diaphragm contribute to the changes in the breathing pattern Cardiovascular and Pulmonary Rehabilitation, 1997). The benefits
and thoracoabdominal motion observed in these patients (Sackner of IMT have been described by many authors and include increased
et al., 1984; Tobin et al., 1983). Most of these abnormalities suggest strength and endurance of the inspiratory muscles, reduced dys-
a malfunction of respiratory muscles, especially the diaphragm, pnea and fatigue, increased exercise tolerance and distance walked
with the use of sternocleidomastoid (SMM) and abdominal mus- during the six minute walk test, improved performance in daily
cle (ABD) being enhanced (Decramer, 1997; McKenzie et al., activities and an improved quality of life (Geddes et al., 2008;
2009). These patients also exhibit other adaptations, such as mod- Gosselink et al., 2011; Shoemaker et al., 2009).
ified chest wall and diaphragm shapes, which accommodate the Optoelectronic plethysmography (OEP) (Cala et al., 1996) can be
increased volume and adaptations of muscles fibers to preserve used to elucidate which chest wall (CW) compartment contributes
strength and increase endurance (Loring et al., 2009; McKenzie the most to the tidal volume and breathing pattern in different
et al., 2009). These abnormalities are associated with poor exer- situations. Recent reviews summarized the use of OEP in COPD
cise tolerance, dyspnea and lower functional capacity (Loring et al., patients (Parreira et al., 2012; Romagnoli et al., 2008). Aliverti et al.
2009). (2004) found different behavior to increase the tidal volume dur-
ing exercise: a decrease of end expiratory abdominal volume in
euvolemics patients and an increase of end inspiratory abdominal
∗ Corresponding author at: Department of Physical Therapy, Universidade Federal and rib cage volume in hyperinflated patients. Bianchi et al. (2004)
de Minas Gerais, Av. Antônio Carlos, 6627, Pampulha, Belo Horizonte, Minas Gerais also identified during pursed-lip breathing an increased tidal vol-
31270-901, Brazil. Tel.: +55 31 34094783; fax: +55 31 3409 4783. ume associated with increasing end inspiratory rib cage volume
E-mail addresses: (M.A. Coutinho Myrrha), and reducing end expiratory rib cage and abdominal volumes. (D.S.R. Vieira),
Hostettler et al. (2011) assessed the effect of ILB and identified asso-
(K.S. Moraes), (S.M. Lage), (V.F. Parreira),,
ciation between chest wall volume changes and respiratory muscle (R.R. Britto). strength in 12 healthy subjects. To the best of our knowledge no

1569-9048/$ – see front matter © 2013 Elsevier B.V. All rights reserved.
16 M.A. Coutinho Myrrha et al. / Respiratory Physiology & Neurobiology 188 (2013) 15–20

previous studies evaluated the chest wall volumes and breathing to overcome the load. There were no requirements for the breath-
pattern of COPD patients during inspiratory loaded breathing (ILB). ing pattern or the breathing frequency to be adopted during the
We hypothesized that COPD patients to overcome the load ILB.
imposed by the ILB will present an increase of chest wall tidal vol-
ume as a result of an increase of chest wall end inspiratory volume 2.2.3. Chest wall volumes and breathing pattern
by both compartments (rib cage and abdomen). We also hypoth- The chest wall volumes and breathing pattern were measured
esized that these changes will occur associated with increase by optoelectronic plethysmography (OEP-BTS, Milan, Italy) with a
activation of inspiratory accessories muscles. sampling frequency of 60 Hz. This non-invasive technique meas-
Therefore, the primary aim of this study was to evaluate the ures breath-by-breath changes in the volume of chest wall and
changes in the chest wall volumes and breathing patterns in COPD its compartments (Aliverti and Pedotti, 2003; Aliverti et al., 2009).
patients during ILB at 30% of MIP. As a secondary aim we also eval- Eighty-nine reflecting markers were placed over the front and back
uate the activity of accessories respiratory muscles. of the trunk along pre-defined horizontal and vertical lines. The
landmark coordinates were measured with a system consisting of
2. Methods six infrared cameras, three of which were positioned in front of the
participants and three of which were positioned behind the partici-
2.1. Participant characteristics pants (Aliverti and Pedotti, 2003; Aliverti et al., 2009). The recorded
images were transmitted to a computer, where a 3-D geometric
This cross-sectional study was approved by the institutional model was formed (Cala et al., 1996). The chest wall was modeled
ethics committee, and all of the participants gave written informed from the compartments: pulmonary rib cage (RCP), abdominal rib
consent. cage (RCA) and abdomen (AB). For this study, we considered the rib
The participants in the study met the following inclusion crite- cage (RC) as the sum of the RCP and the RCA.
ria: male, an age between 45 and 75 years, a body mass index The participants remained seated on a backless bench with their
between 18 and 30 kg/m2 , a clinical diagnosis of moderate to very feet flat on the floor and their upper limps abducted, externally
severe COPD (FEV1 /FVC < 0.70; FEV1 < 0.80) (GOLD, 2008), clinical rotated and flexed (for the visualization of the lateral markers) and
stability with no exacerbations in the last four weeks, a history of comfortably supported to minimize the activity of the accessory
smoking, the absence of any respiratory disease that could con- respiratory muscles both at rest and during ILB. The participants
tribute to dyspnea, no cardiovascular, neurological or psychiatric were instructed to look forward. To allow the cameras to capture
disorders, and no participation in a pulmonary rehabilitation pro- the lateral chest wall markers, the examiner held the inspiratory
gram. Participants were excluded if they were unable to understand threshold device at the participant’s right side.
and follow the procedures. The chest wall volumes were determined by analyzing the tidal
volumes based on the difference (VT) between the end-inspiratory
volume (Vei) and end-expiratory volume (Vee) of each compart-
2.2. Protocol
ment. The chest wall tidal volume (VTcw ) was the sum of rib cage
tidal volume (VTrc ) and abdomen tidal volume (VTab ). The breath-
Data were collected on two occasions within a one-week period.
ing pattern was analyzed by the contribution of each compartment
On the first day, lung function and muscle strength were evaluated.
to the chest wall volume. The ratio of the inspiratory time to the
On the second day, the chest wall volumes, breathing pattern and
total time of the respiratory cycle, the respiratory frequency and the
respiratory muscle activity were simultaneously recorded at two
minute ventilation were also assessed. These ventilator parameters
situations: (1) quiet breathing (resting), divided into three sets of
were obtained from chest wall volume variations measurements.
two minutes with a one-minute interval between sets, totaling six
minutes; (2) ILB at 30% of MIP for five minutes, without any specific
2.2.4. Respiratory muscle activity
requirements regarding the breathing pattern to be adopted.
Surface electromyography (EMG System do Brazil Ltd, São Paulo,
Brazil) was used to record the muscle respiratory activity. Because
2.2.1. Lung function and respiratory muscle strength a wireless device was not available, to avoid covering the OEP
A calibrated spirometer (Vitalograph 2120, Buckingham, markers by EMG electrodes and cables we evaluated only the ster-
England) was used to evaluate lung function according to the Brazil- nocleidomastoid (SMM) and abdominal (ABD) muscles. An EMG
ian recommendations (Sociedade Brasileira de Pneumolologia e system with a biological signal acquisition module consisting of
Tisiologia, 2004) and predicted values proposed for Brazilian eight channels, an amplifier gain of 1000× and a common mode
subjects (Pereira, 2007). Inspiratory muscle strength was evalu- rejection ratio >120 db was used for data acquisition. The data
ated using a calibrated manometer (GERAR® Classe B – SP/Brazil) were processed using specific acquisition and analysis software
connected to corrugated plastic tube and a mouthpiece with a (WinDaq® Acquisition Software, Akron, OH, USA) and an A/D 12
2-mm air leak orifice (Neder et al., 1999). Each patient performed bit signal converting plate, which was used to convert analog sig-
at least five maneuvers (considering a variation of up to 10%) nals to digital signals with an anti-aliasing sampling frequency of
to achieve MIP from residual volume to total lung capacity. The 2000 Hz for each channel and an input range of 5 mV. Active bipolar
highest value observed was recorded, as long as this value was not superficial electrodes consisting of two parallel rectangular Ag/AgCl
the last to be obtained. bars (1 cm in length, 0.78 cm2 of contact area) were used with an
internal amplifier to reduce the effects of electromagnetic interfer-
2.2.2. Inspiratory loaded breathing (ILB) ence and other noise. For SMM, the electrodes were fastened to the
ILB was performed using a threshold device (Threshold Inspira- lower third of the muscle belly, which was identified by palpation
tory Muscle Trainer, New Jersey, USA), which imposes a workload during manually resisted flexion of the neck (Falla et al., 2002).
on the inspiratory muscles, maintains a constant load during For ABD, the electrodes were placed 2 cm away from the umbili-
inspiration, and is flow-independent, with no resistance during cus on the rectus abdominal muscle (Duiverman et al., 2004). The
expiration. The patients breathed through the mouthpiece with ground electrode was fixed on the ulnar styloid process. All of the
their nose occluded by a noseclip for five minutes with a work- electrodes were fixed on the right side. The EMG signal collection
load of 30% of the MIP, the load frequently used in most studies and analysis were carried out as recommend by the International
(Lotters et al., 2002). The patients were instructed to breathe deeply Society for Electrophysiology and Kinesiology (Merletti, 1999). The
M.A. Coutinho Myrrha et al. / Respiratory Physiology & Neurobiology 188 (2013) 15–20 17

activity of the respiratory muscles was analyzed by the root mean Table 1
Participant characteristics.
square (RMS) method.
Characteristic n = 13
2.2.5. Dyspnea Age (yr) 65.15 (7.09)
The participants were asked to quantify their sensation of dys- Weight (kg) 62.88 (8.59)
pnea at rest and immediately after ILB on a scale of 0–10 using the Height (m) 1.64 (0.06)
modified Borg scale. BMI (kg/m2 ) 23.37 (2.61)
MIP (cm H2 O) 86.92 (29.97)
MIP (% pred) 81.13 (28.03)
3. Statistical analyses FEV1 (L) 1.07 (0.44)
FEV1 (% pred) 33.18 (10.91)
3.1. Sample size calculation FEV1 /FVC 0.46 (0.07)
MRC (a.u.) 2.31 (0.75)

The sample size was based on being able to detect at least a The data are presented as the mean and standard deviation (in parentheses). BMI:
body mass index, MIP: maximal inspiratory pressure, FEV1 : forced expired volume
difference of 300 ml in the chest wall tidal volume (Romagnoli et al.,
in the first second, FVC: forced vital capacity, MRC: medical research council scale,
2011). Considering our data of pilot study with six subjects (mean a.u.: arbitrary unit.
and standard deviation), a two-sided alpha of 0.05 and a statistical
power of 0.80, the target sample size was set at 13 individuals. Thus,
15 patients were selected to account for the possibility of dropouts. correlation was calculated from 12 participants, as artifacts in the
EMG signal analyses precluded the use of the data from another
3.2. Data analysis participant. Table 1 presents the anthropometric characteristics,
lung function and inspiratory muscle strength of the 13 patients
The chest wall volumes measured during the six minutes at rest included in the study.
and two minutes of ILB (90–210 s) were analyzed using specific
software. The mean rest values were compared to the ILB values 4.2. Chest wall volumes and breathing pattern
with Student’s t-test or Wilcoxon’s test, depending on the data
distribution. Table 2 and Fig. 1 show the changes in the patients’ chest
The EMG signals were processed according to the time-domain. wall volumes and breathing pattern during ILB. The VTcw signifi-
One minute of the signal (30–90 s) from the second set of two cantly increased from rest to ILB (p < 0.05) mainly by the increase
minutes at rest and one minute of the signal from the ILB of the VTab (Table 2). There was also a significant increase in
(120–180 s) were analyzed. We evaluated the change from rest to Veicw and Veirc . Regarding to end expiratory volumes, only the
ILB period expressed as percentage (relative change) analyzing by Veerc increased during ILB, but it was not sufficient to significantly
the Mann–Whitney test. increase the Veecw .
All of the statistical procedures were carried out using the Sta- The main compartment contribution for the VTcw at rest and
tistical Package for Social Science (SPSS, 15.0, Chicago, IL, USA). The during ILB was the abdomen, without difference in the two situa-
level of significance was set at p < 0.05. tions analyzed. The inspiratory time, the ratio of inspiratory time
to total time of the respiratory cycle and the minute ventilation
4. Results increased (p < 0.05) during ILB (Table 2).

4.1. Participants 4.3. Muscle activity and dyspnea

Fifteen patients with COPD were initially evaluated. Two of the From rest to ILB it was observed an improvement of 63.84%
patients were excluded because they were not able to complete (25.22 to 125.06) of the SMM muscle activity and 1.94% (−13.84
five minutes of ILB. Therefore, 13 participants were included in the to 21.96) of the ABD muscle activity (median, interquartile range,
analysis. However, the chest wall volume and muscular activity Fig. 2). The sensation of dyspnea according to the modified

Table 2
Chest wall volume and breathing pattern data obtained at rest and during inspiratory loaded breathing (n = 13).

Rest ILB ILB–Rest 95% CI P

VTcw (L) 0.51 (0.11) 0.84 (0.31) 0.34 0.16 to 0.51 0.002a
VTrc (L) 0.20 (0.05) 0.31 (0.20) 0.11 −0.22 to 0.002 0.046
VTab (L) 0.31 (0.10) 0.53 (0.20) 0.22 0.14 to 0.31 0.0001
%AB 60.33 (11.41) 64.32 (15.46) 3.99 −2.88 to 10.85 0.23
Ttot (s) 3.49 (0.64) 4.34 (1.40) 0.85 −0.09 to 1.78 0.071
Ti /Ttot 0.40 (0.28) 0.48 (0.08) 0.09 0.03 to 0.14 0.005
f (min−1 ) 18.55 (3.26) 15.53 (4.66) −3.02 −6.92 to 0.88 0.117
VE (L min−1 ) 8.85 (1.69) 12.30 (3.94) 3.46 0.79 to 6.13 0.015
Veecw (L) 22.53 (3.76) 22.74 (3.80) 0.21 −0.08 to 0.48 0.144
Veerc (L) 16.55 (2.31) 16.84 (2.31) 0.28 −0.50 to −0.07 0.012
Veeab (L) 5.99 (1.55) 5.90 (1.60) −0.09 −0.24 to 0.06 0.228
Veicw (L) 23.04 (3.79) 23.58 (3.93) 0.54 0.14 to 0.93 0.011
Veirc (L) 16.75 (2.30) 17.15 (2.33) 0.40 0.22 to 1.29 0.010
Veiab (L) 6.29 (1.60) 6.43 (1.73) 0.13 −0.06 to 0.33 0.156

The data are presented as the mean and standard deviation (in parentheses). ILB: inspiratory loaded breathing, CI: confidence interval, VTcw : tidal volume of the chest wall,
VTrc : tidal volume of rib cage, VTab : tidal volume of abdominal volume, %AB: contribution of abdominal compartment, Ti : inspiratory time, Ttot : total time of the respiratory
cycle, f: respiratory frequency, VE: minute ventilation, Veecw : chest wall end-expiratory volume, Veerc : rib cage end-expiratory volume, Veeab : abdomen end-expiratory
volume, Veicw : chest wall end-inspiratory volume, Veirc : rib cage end-inspiratory volume, Veirca : abdomen end-inspiratory volume.
Non-parametric variable. p values < 0.05 were considered significant.
18 M.A. Coutinho Myrrha et al. / Respiratory Physiology & Neurobiology 188 (2013) 15–20

0,8 *
∆Vcw (L)

- 0,2 Rest ILB

- 0,4

1 Fig. 2. Percentage (%) of changes on root mean square values from rest to inspiratory
load breathing for the sternocleidomastoid and abdominal muscles.
∆Vrc (L)

RMS: root mean square, SMM: sternocleidomastoid, ABD: abdominal, (䊉): outliers,
0,6 Mann–Whitney test.

0,4 *
0,2 5.2. Study limitations
While inspiratory muscle weakness was not considered as an
- 0,2 Rest ILB
inclusion criterion in this study, the inspiratory muscle strength
- 0,4 of the COPD patients was preserved, matching the predicted values
corrected for age and gender (Neder et al., 1999). There may be sev-
eral explanations for this observation: (1) the chronic adaptations
of COPD may reduce the length of the sarcomeres and increase the
oxidative capacity of mitochondria (Duiverman et al., 2004), (2) the
accessory respiratory muscles may adapt to overcome the load dur-
1 ing the respiratory cycle due to the diaphragm weakness (Souza,
∆Vab (L)

0,8 2002) and (3) the manovacuometer assesses the global inspira-
0,6 tory muscles, not solely diaphragm strength. Considering this, it
0,4 is possible that the load was not enough to change the breathing
0,2 patterns.
Another important limitation of the study is the EMG results.
The evaluation of only two respiratory muscles, considering both
- 0,2
inspiration and expiration for the quantitative evaluation of EMG,
- 0,4
reduces the specificity of the measurement and does not allow
Rest ILB studying the mechanisms underlying the variations in the displace-
ment of the different compartments of the chest wall. Also we did
Fig. 1. Changes in the chest wall and compartment volumes during inspiratory
not normalize the EMG using a maximal contraction as reference.
loaded breathing. The distance between two corresponding point is the tidal volume
of the considered compartment. We reported the EMG results as change of absolute values from
CW: chest wall, RC: rib cage, AB: abdomen, ILB: inspiratory loaded breathing, closed rest to ILB condition. Aware of these limitations we decided to
symbols: end-expiratory volume, open symbols: end-inspiratory volume. Dotted report the results to encourage future studies with more advanced
line: functional respiratory capacity. The bars indicate means ± SD. *p < 0.05.

Borg scale expressed as media (minimum–maximum) increased 5.3. Chest wall volumes and breathing pattern
(p = 0.005) from rest 0.4 (0.0–2.0) to after ILB 1.1 (0.5–3.0).
In our study, the abdominal compartment was responsible for
approximately 60% of the tidal volume in both situations. Our find-
5. Discussion ings are in accordance with other studies, which have also found
a major abdominal contribution to tidal volume (60%) at rest in
5.1. Major finding patients with COPD (Aliverti et al., 2009; Bianchi et al., 2004, 2007;
Romagnoli et al., 2011). On the other hand, other studies found a
This mainly results of this study are that (1) to overcome lower abdominal contribution to tidal volume (40%) at functional
the inspiratory load COPD patients improve the tidal volume by residual capacity (Binazzi et al, 2008) and during exercise (Vogiatzis
increasing the end inspiratory chest wall volume without change et al., 2005). The ratio of the inspiratory time to total time of the
the end expiratory chest wall volume, (2) this action did not affect respiratory cycle increased during ILB indicates more work from
the predominant displacement of the abdomen found in rest con- the inspiratory muscles (Decramer et al., 2005). The reduction of
ditions and (3) it was also observed an improvement of the SMM the expiratory time usually increases the hyperinflation in COPD
muscle activity. patients. However, although it was observed a higher rib cage end
M.A. Coutinho Myrrha et al. / Respiratory Physiology & Neurobiology 188 (2013) 15–20 19

expiratory volume during ILB, it did not lead to an increase on chest volume. This action seems to be related to inspiratory accessory
wall end expiratory volume, probably because of the concomitant muscle activity.
tendency to decrease the end-expiratory abdominal volume. The
improvement of the elastic recoil of the lung tissue would also Acknowledgements
be related to this result; however it needs to be evaluated by a
systematic research. This study was supported by grants from CNPq (Conselho
Studies about the chest wall volumes behavior of COPD patients Nacional de Desenvolvimento Científico e Tecnológico, number
during exercise and respiratory exercise showed that the responses 302913/2008-4), FAPEMIG (Fundação de Amparo à Pesquisa do
could be different depending on the characteristics of the patients estado de Minas Gerais, PPM00072-09) and PRPq (Pró-Reitoria de
in regard to dynamic hyperinflation response (Aliverti et al., 2004; Pesquisa – UFMG).
Bianchi et al., 2007; Vogiatzis et al., 2005). Brandão et al. (2012)
using ILB at 30% MIP in health and heart failure subjects observed
also an increase of tidal volume, however by increasing the rib cage
and abdomen tidal volume and with a reduced mobility in lower Aliverti, A., Pedotti, A., 2003. Opto-electronic plethysmography. Monaldi Archives
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