Acute effects of incremental inspiratory loads on compartmental chest wall volume and predominant activity frequency of inspiratory muscle

Journal of Electromyography and Kinesiology 23 (2013) 1269–1277

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Acute effects of incremental inspiratory loads on compartmental chest wall volume and predominant activity frequency of inspiratory muscle Alana Elza Fontes Da Gama a, Larissa de Andrade Carvalho a, Larissa Andrade Feitosa a, Jasiel Frutuoso do Nascimento Junior a, Marilú Gomes Netto Monte da Silva b, César F. Amorim c, Andréa Aliverti d, Daniel Lambertz a, Marco Aurélio Benedetti Rodrigues b, Armèle Dornelas de Andrade a,⇑ a

Department of Physiotherapy of Universidade Federal de Pernambuco, Recife, Brazil Department of Electronics and Systems of Universidade Federal de Pernambuco, Recife, Brazil Universidade Cidade de São Paulo, UNICID, Brazil d Dipartimento di Elettronica, Informazione e Bioingegneria – Politecnico di Milano, Milan, Italy b c

a r t i c l e

i n f o

Article history: Received 19 December 2012 Received in revised form 26 July 2013 Accepted 29 July 2013

Keywords: Electromyography Plethysmography Breathing exercises Respiratory muscles

a b s t r a c t Aim: This research aims to analyze the acute effect of incremental inspiratory loads on respiratory pattern and on the predominant activity frequency of inspiratory muscle, taking into account differences in gender responses. Optoelectronic Plethysmography was performed during loads in 39 healthy subjects (20 women), placing 89 markers on the thoracic-abdominal wall to obtain total and regional volumes. Surface electromyography (SEMG) was taken simultaneously on the Sternocleidomastoid and Diaphragm muscles, to calculate the predominant muscle activity frequency through wavelet analysis. Inspiratory loads were performed using ThresholdÒ with 2 min of breathing at different levels, ranging from a load of 10 cmH2O plus 5 cmH2O to 40 cmH2O or fatigue. Results: Inspiratory Time increased during loads. Total and compartmental volumes increased with different regions, changing at different loads. These changes in volume occur earlier in women (20 cmH2O) than in men (30 cmH2O). The predominant activity frequency of Sternocleidmastoid muscle decreased at 30 cmH2O, while Diaphragm activity decreased at 40 cmH2O. Conclusion: The acute effects of incremental inspiratory loads are increases of total and regional volumes and inspiratory time. As for muscle activity, the predominant activity frequency declined in Sternocleidomastoid and Diaphragm muscles, but at different loads. Such respiratory and SEMG patterns and gender differences should be considered when clinical interventions are performed. Ó 2013 Elsevier Ltd. All rights reserved.

1. Introduction Loads are imposed on the respiratory system in order to increase respiratory muscle strength and endurance. (Lotters et al., 2002). Inspiratory Muscle Training is primarily used during respiratory treatment and rehabilitation of pulmonary patients (Dornelas de Andrade et al., 2005), but is also applied in cardiac patients (Brandão et al., 2012), healthy subjects (Enright and Unnithan, 2011) and athletes (Griffths and McConnell, 2007). It consists of imposing resistance on the respiratory system in order to increase muscle strength and flow capacity in the airways. These training-induced changes are associated with lung volume improvements, greater secretion mobilization (Chantham et al., 1999) and lung ventilation (Nobre et al., 2007). Additional benefits ⇑ Corresponding author. Address: Departamento de Fisiotérapia da UFPE, Av. Jornalista Anibal Fernandes, Cidade Universitária, Recife PE 50670-901, Brazil. Tel.: +55 81 21268496; fax: +55 81 21287042. E-mail address: [email protected] (A.D. de Andrade). 1050-6411/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jelekin.2013.07.014

include dyspnea reduction during rest or after exercise and enhanced physical capacity (Lotters et al., 2002). Alterations in muscle activity are important to take in account, mainly due to the fact that Inspiratory Muscle Training can induce fatigue, changing muscle recruitment of power fiber to endurance fiber, located mainly in the lower rib cage (Nobre et al., 2007). Furthermore, changes observed in Chronic Obstructive Pulmonary Disease (COPD) patients include an increase in the proportion of type I fibers and the size of type II fibers (Gosselink, 2003). Indeed, differences in muscle activity can be evaluated by Surface Electromyography (SEMG), enabling evaluation of respiratory muscle recruitment and comparison with other muscles (González-Izal et al., 2012; Perlovitch et al., 2007). During fatigue, changes in SEMG frequency may result from muscle fiber recruitment, since fast type fibers drop out earlier, leading to a decrease in SEMG frequency range. (González-Izal et al., 2012; Perlovitch et al., 2007; Shadgan et al., 2011). Changes in muscle activity affect chest wall movement and pulmonary ventilation. Optoelectronic Plethysmography is an

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accurate and noninvasive method to measure variations in volume (Cala et al., 1996). Optoelectronic Plethysmography, a system that enables us to evaluate chest wall volume and that of its compartments, measures regional ventilation without the need for nose clips or mouthpieces. (Aliverti et al., 2004). Assessing chest wall kinematics can help evaluate mechanical differences according to sex. Different pulmonary functions have been attributed to distinct gender traits, such as hormones (Card and Zeldin, 2009), smaller stature, torso size and posture (Romei et al., 2010). Gender differences play a major role in both healthy and diseased lung function and should therefore be considered a factor when designing pulmonary research studies. (Carey et al., 2007). Despite evidence of the effects of long-term Inspiratory Muscle Training, it is important in clinical practice to understand the acute consequences of incremental loads on pulmonary volumes as well as respiratory and muscle activation patterns. As such, this study aimed at evaluating the acute effect of incremental inspiratory load on ventilation distribution in the lungs using Optoelectronic Plethysmography, and on the frequency of inspiratory muscle activity, primarily the Diaphragm and Sternocleidomastoid muscles, through SEMG and its different response according to gender. These muscles were chosen because they are the main inspiratory (Diaphragm) and accessory muscle in forced inspiration (Sternocleidomastoid). This research hypothesis is that the incremental load imposition during inspiratory activity tends to raise ventilation. When ventilation is altered the ventilator pattern modifies by changes in compartmental distribution. In order to accompany these changes muscle activity probably reduces its predominant frequency due changes in fiber recruitments during continuum activities. 2. Methods This is a cross-sectional study with healthy subjects, approved by the human research ethics committee and conducted according to Declaration of Helsinki guidelines. A pilot study was carried out with eleven individuals in order to estimate the required sample size (N). N was measured by computing the square of 1.96 multiplied by the variable standard deviation divided by the maximum allowable error (10–20% of variable mean) (Bolfarine and Bussab, 1994). For Optoelectronic Plethysmography a 10% error and for SEMG data a 20% error was used due to its variability. The highest N computed (39) was considered for the study. The study was composed of healthy men and women, aged between 18 and 30 years with normal Body Mass Index (19 < Body Mass Index < 25 kg/m2). Exclusion criteria included changes in lung function or respiratory diseases, which were identified by clinical history and spirometry, where individuals whose Forced Expiratory Volume in one second/Forced Vital Capacity was less than 80% were excluded (Pereira, 2002). Active smokers, ex smokers, individuals with a history of cardiopathy, recent surgery, pregnant women, uncooperative individuals and those experiencing pain, infection, fever or any other discomfort were also excluded. 2.1. Study design Volunteers were initially submitted to anamnesis, a clinical evaluation of medical history and drug use, anthropometry (body mass and stature), hemodynamic measurements [arterial pressure (Tycos tensiometer), heart rate and peripheral oxygen saturation (Oximeter Onyx 9500)], lung function tests [spirometry (Micro Medical Microloop MK8) and Maximal Inspiratory and Expiratory Pressure, (MV-150 Marshal-Town Instrumentation Industry)]. All of these measurements were used to evaluate inclusion and exclusion

criteria. Next, the subjects were simultaneously prepared for Optoelectronic Plethysmography and SEMG evaluation simultaneously, at which time data on quiet breathing and incremental load breathing were collected using Threshold?. 2.2. Data collection 2.2.1. Lung function Spirometry was performed in accordance with the American Thoracic Society and European Respiratory Society protocol (Miller et al., 2005), where forced volumes and capacities were measured and presented as percentage forecast for the study population (Pereira, 2002). Muscle strength was evaluated using Maximal Inspiratory and Expiratory Pressure. The former was assessed with the subject performing forced inspiration starting from residual volume and the latter with forced expiration, beginning at total lung capacity (Neder et al., 1999). Maximal pressure should be maintained for at least one second without air escaping, with maximum variation of up to 20% between measures (American Thoracic Society and European Respiratory Society, 2002). 2.2.2. Optoeletronic plethysmography The Optoelectronic Plethysmography protocol for the orthostatic position was performed using 89 hemispheric markers, with infrared reflexive markers placed according to anatomical references and attached to the skin with anti-allergy adhesives (Aliverti et al., 2005). Eight infrared cameras placed around the subject were connected to the Optoelectronic Plethysmography system, enabling the computer to receive accurate three-dimensional coordinates of each marker and reconstruct the three-dimensional thoracic surface (SMART Capture software – BTS Bioengineering, Italy). Based on this model, chest wall volume was computed and divided into its different compartments in order to evaluate regional ventilation: Pulmonary Rib Cage (Vrc,p), Abdominal Rib Cage (Vrc,a) and Abdomen (Vab) (Cala et al., 1996). 2.2.3. Surface electromyography All SEMG capture procedures were carried out in line with International Society Electrophysiology Kinesiology recommendations (Williams, 1987). The SEMG signal was obtained through an eight channel signal amplifier (EMG System, Brazil) composed of analog signal capture with a 20–500 Hz band pass filter, 1000  gain and common mode rejection ratio >120 dB. The EMG system was connected to the input of an analog to digital converter of the Optoelectronic Plethysmography system at 960 Hz, enabling simultaneous capture of Optoelectronic Plethysmography and SEMG using the same software. The bipolar technique was used, with two surface silver/silverchloride (Ag/AgCl) electrodes (Cardiologic 3 M) placed 20 mm apart on the Sternocleidomastoid and Diaphragm muscle in the muscle fiber direction. An oval reference electrode (4 cm  3.5 cm) and differential amplifier were used to reduce external common mode interference. The subject’s skin was previously prepared and cleaned with alcohol to reduce impedance. Diaphragm electrodes were positioned on the 7th or 8th anterior intercostal space between the axillary and midclavicular line, in accordance with the best signal capture. To better position the electrode, deep inspiration may be required as well as on-screen analysis of the signal, to determine if it was properly captured. For the Sternocleidomastoid muscle, electrodes were placed 5 cm from the mastoid process (Dornelas de Andrade et al., 2005). The validity of surface electromyography for the Diaphragm used to be a questionable point. In an attempt at

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solving this question, Demoule et al. (2003) validated surface recordings using transcranial magnetic stimulation (Demoule et al., 2003). 2.2.4. Inspiratory load A spring device (Threshold?), which promotes inspiratory resistance from zero to 40 cmH2O, was used to evaluate the acute effect of incremental inspiratory loads, applying the protocol proposed by Johnson et al. (1997), and performed simultaneously with SEMG and Optoelectronic Plethysmography. In this protocol, subjects inspire through Threshold?, generating initial threshold opening pressure of 10 cmH2O. This pressure is raised by 5 cmH2O every 2 min until it fails to lift the plunger in two consecutive breaths. The user was instructed to breathe freely, that is, no inspiration and expiration pattern was required. In order to guarantee the same conditions between breathing with and without a load, an additional quiet breathing was evaluated using Threshold? without spring/resistance. After five minutes, quiet breathing was performed to restore the respiratory pattern to resting conditions. 2.3. Data analyses 2.3.1. Optoeletronic plethysmography analyses Based on chest wall movements, Optoelectronic Plethysmography equipped with BTS SMART-analyzer software (BTS Bioengineering, Italy) (BTS Bioengineering, Italy) was used to analyze volume variations from the total chest wall and compartments, providing Tidal Volume (Vt) and End Expiratory and Inspiratory Lung Volumes (EELV and EILV) of the chest wall and percentage of each compartment (%Vrc,p,%Vrc,a,%Vab), representing regional distribution. Additionally, Inspiratory and Expiratory Time, Total respiratory cycle time, relationship between Inspiratory Time and Total Time (Inspiratory Time/Total Time), Respiratory Rate and Minute Volume were computed. 2.3.2. Surface electromyography analyzes The captured SEMG signal was converted to text format using the SMART Analyzer (BTS Bioengineering, Italy), read by MATLABÒ, where the resulting algorithm read the text line by line to create the digital signal. In order to remove electrocardiogram interference from the signal, a high pass filter with a cut-off frequency of 30 Hz was applied (Butler et al., 2009). Fig. 1 shows the original (Fig. 1a) and filtered (Fig. 1b) signal. To study the frequency at which the muscle was working during activities and relate it with muscle fiber recruitment, a frequency spectrum of the SEMG signal was created using wavelet analysis and Continuous Wavelet Transform (CWT), enabling us to evaluate the behavior of muscle frequency activity as a function of time (Karlsson et al., 2000). For example, this procedure solves problems posed by the Fast Fourier Transform (FFT), which provides frequential information only, because Multi-Resolution analysis can be performed with wavelet, that is, analysis of different signal frequencies at different resolutions (Daubechies, 1990). Continuous Wavelet Transform obtained wavelet coefficients using the Daubechies4 (db4) mother wavelet (Daubechies, 1988), and subsequent transformation into pseudo-frequencies for SEMG analysis. The Daubechies4 was chosen for SEMG based on the literature (So et al., 2009) and preliminary tests according to signal characteristics. At each load, a portion of the signal, corresponding to one inspiration, was captured in the middle of the load. Each selected part was submitted to wavelet analysis, resulting in an energy spectral density graph. The energy spectral density graph provides information about the signal intensity found at a determinate frequency over time (Fig. 2). The image represents the energy spectral density of one

Fig. 1. Original and filtered signal.

inspiration of one volunteer at initial (Fig. 2a) and final loads (Fig. 2b). The red area represents frequency (in Hertz) with more energy density, i.e. the most predominant muscle activity frequency. The three highest frequency densities were selected as reference of predominant muscle activity frequency. Next, a mean value was computed to represent predominant muscle activity frequency. This information shows the muscle frequency behavior of the respiratory system during quiet breathing and incremental loads.

2.3.3. Statistical analysis Statistical Package for the Social Sciences software (SPSS 15.0) was used for statistical analysis. To determine whether changes in ventilation pattern were related with altered muscle activity, chest wall kinematics, Optoelectronic Plethysmography data were correlated with SEMG data, and analyzed using predominant muscle frequency. In order to verify if men and women responded equally to load-imposed changes, differences in chest wall kinematic modifications between genders were evaluated. To determine if ventilation changes were related with lung function, lung function tests, including Maximal Inspiratory and Expiratory Pressure, were also correlated with volume variation. Data were expressed as mean and standard error. The Kolmogorov–Smirnov test was conducted in order to check data distribution and categorize it as parametric or non-parametric. Since all study variables exhibited normal distribution, Pearson’s test was performed to test correlations between ventilation pattern, through volume variation, as well as lung function and muscle activity. To evaluate the behavior of chest wall kinematics with imposed loads, ANOVA with Tukey’s Post-hoc test was carried out to compare regional and total ventilation between loads. In order to determine the difference in ventilation changes between men and women, Vt variation (DVt = Vtfinal Vtinitial) was analyzed to compare its increase and the student t-test for independent samples was performed to test this difference.

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Fig. 2. Energy spectral density graph of one inspiration from one volunteer: (a) initial load and (b) final load.

The same tests to compare the difference between loads and genders were performed for SEMG data in order to evaluate muscle activity changes and relate them with volume changes. To establish the difference between genders in muscle activity, the variation in predominant activity frequency of each muscle (DSEMG = frequencystart frequencyend) was compared using student’s t-test for independent samples. A confidence interval of 95% (p < 0.05) was used to attest statistical significance.

3. Results A total of 39 subjects participated in the study (51.3% female). Anthropometric characteristics, lung function tests and ventilator pattern for each gender are given in Table 1. Regional volume distribution was different between genders, revealing a different ventilation pattern. Of the 39 subjects, 34 reached the maximal load of the protocol, while the other five became fatigued beforehand: one at 10 cmH2O, two at 20 cmH2O and two at 30 cmH2O. The inspiratory load promoted an increase in chest wall Vt and its compartments, with no change in respiratory pattern, that is, no percentage change in any of the compartments (Table 2). This increase in chest wall Vt and Vrc,p was significant from 20 cmH2O onwards, while with Vrc,a and Vab, it was significant from 30 cmH2O. After the load was removed, the volume started to return to baseline values in all compartments. There was also a rise

in Minute Volume, Inspiratory Time, Total Time and Inspiratory Time/Total Time. No changes in EELV or EILV were detected. The imposed load acted differently in men and women (Fig. 3). Men exhibited an increase in Vt at 30 cmH2O for Vrc,p and Vab, with no air mobilization changes for Vrc,a (Fig. 3b). Women showed an increase from 20 cmH2O on onwards for Vt and at 30 cmH2O for Vrc,p, with no significant changes in the other compartments (Fig. 3a). The Vt variation was greater in men than in women: 422.8 ± 133.2 ml vs. 284.9 ± 63.7 ml respectively (p = 0.042); primarily in Vrc,a: men: 81.3 ± 34.3 ml and women: 55.2 ± 11.5 ml (p = 0.024). The correlation test between maximal respiratory pressures and Vt variation showed a positive correlation between Maximal Expiratory Pressure and total Vt variation (r = +0.428/p = 0.023). Maximal Expiratory Pressure also presented positive correlation with compartmental variation at Vrc,p and Vrc,a (r = +0.418/p = 0.027 and r = +0.423/p = 0.025). In men this correlation was stronger for Vrc,p and Vrc,a variation (r = +0.581/p = 0.029 and r = +0.562/ p = 0.037 respectively), while for women there was no correlation between these variables. Simultaneous to volume changes, muscles responsible for this air mobilization show a decline in predominant activity frequency. The Sternocleidomastoid muscles exhibited a decrease in predominant activity frequency from 30 cmH2O and Diaphragm at 40 cmH2O. Fig. 4 illustrated these frequency changes for each

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*

Variable

Men

Women

p*

Age (years) Body mass (kg) Stature (cm) Expiratory Volume at first second/Forced Vital Capacity (% of predicted) Maximal Inspiratory Pressure (cmH2O) Maximal Expiratory Pressure (cmH2O) Heart rate (bpm) Saturation of Peripheral Oxygen (SpO2) (%) Systolic Arterial Pressure (mamHg) Diastolic Arterial Pressure (mmHg) Contribution of Pulmonary Rib Cage during quiet breathing (%) Contribution of Abdominal Rib Cage during quiet breathing (%) Contribution of Abdomen during quiet breathing (%)

25.50 ± 0.86 68.43 ± 4.23 176.X ± 0.02 95.05 ± 2.27 123.6 ± 43.7 97.3 ± 31.3 75.3 ± 10.24 95.71 ± 0.62 133.4 ± 2.52 89.21 ± 1.89 37.74 ± 2.72 22.61 ± 1.26 39.64 ± 3.18

22.70 ± 0.45 54.21 ± 3.13 162.X ± 0.01 105.06 ± 1.97 98.2 ± 37.4 82.6 ± 25.1 78.07 ± 13.58 97.92 ± 1.32 118.5 ± 2.04 74.98 ± 1.31 51.94 ± 2.41 20.26 ± 2.40 27.79 ± 2.45

0.082 0.955 0.056 0.424 0.267 0.345 0.329 0.149 0.212 0.132 <0.001 0.149 0.006

t-Student test for independent samples.

Table 2 Ventilation and lung distribution data during quiet breathing loads between 0 and 40 cmH2O and recovery from basal status with p-value of the ANOVA test. Variable Subjects

Quiet breathing 39

0 cmH2O 39

10 cmH2O 39

20 cmH2O 38

30 cmH2O 36

40 cmH2O 34

Recovery 39

P –

TVa (ml) Vrc, pb(ml) Vrc, ac(ml) Vabd (ml) %Vrc, pb (%) %Vrc, ac (%) %Vabd (%) EELVe EILVf MVg (L) RRh (rpm) TIi (s) TEj (s) Ttotk (s) Tij/Ttotk

601.2 ± 39.9 268.5 ± 197 133.2 ± 12.3 199 5 ± 18 6 45.3 ± 2.2 21.4 ± 0.8 33 3 + 2.2 19.7 ± 0.8 20.3 ± 0.8 8.5 ± 0.4 15.5 ± 0.7 1.8 ± 0.1 2.5 ± 0.1 4.3 ± 0.2 42.0 ± 1.0

698.9 ± 53.8 317.7 ± 96.8 152.0 ± 17.2 229 1 ± 9.02 46.1 ± 2.4 20.1 ± 0.9 30.8 + 2.4 19 2 ± 1.0 19.9 + 1.0 10.1 ± 0.6 15.6 ± 0.8 1.9 ± 0.1 2.3 ± 0.1 4.2 ± 0.2 45.8 ± 0.9

815.5 ± 64.9 381.0 ± 33.2 173.4 ± 19.8 263.2 + 26.3 47.2 ± 23 20.2 ± 0.9 32.6 + 2.5 19.5 ± 0.8 20.2 + 0.8 10.3 ± 0.9 13 5 ± 0.8 2.6 ± 0.2 2.6 ± 0.2 5.2 ± 0.5 49.9 ± 16*

904.7 ± 72.4* 434.3 ± 40.2* 187.8 ± 20.8 282.7 ± 31.8 49.6 ± 2.5 19 6 ± 1.1 31 7 + 2.7 19.4 ± 0.8 20.3 + 0.8 11.2 ± 1.0 13.4 ± 0.9 2.7 ± 0.3 2.8 ± 0.2 5.4 ± 0.5 47.8 ± 2.0

1007.3 ± 86.9* 477.5 ± 86.9* 209.6 ± 19.4* 320.3 ± 38.1 * 48.4 ± 2.3 20.9 ± 0.9 30.7 + 2.5 19.6 ± 0.8 20.7 + 0.8 12 3 ± 1.3 13 1 ± 1.1 * 2.9 ± 0.4 3.0 ± 0.3 5.9 ± 0.6 47.8 ± 2.2

964.6 ± 83.9* 444.0 ± 83.9* 204.2 ± 20.4 316.4 ± 35.7 46.6 ± 2.40 21.1 ± 0.9 32.3 + 2.6 19.6 ± 0.8 20.5 ± 0.8 12 3 ± 1.4 13 7 ± 12 2.8 ± 0.3 2.7 ± 0.2 5.5 ± 0.5 48.5 ± 2.6

812.5 ± 48.7 363.5 + 48.8 166.5 ± 13.9 281.6 ± 30.6 46.1 ± 2.5 19.9 ± 0.9 34.0 + 2.6 19 7 ± 0.8 20.5 + 0.8 12 3 ± 5.0 16 1 ± 11 1.9 ± 0.1 2.5 ± 0.2 4.4 ± 0.4 43.9 ± 0.3

0.000 0.000 0.031 0.035 0.946 0.807 0.968 0.996 0.997 0.033 0.090 0.004 0.398 0.021 0.019

a

Tidal volume. Pulmonary rib cage. Abdominal rib cage. d Abomem end expiratory lung volume. e End Expiratory Lung Volume. f End Inspiratory Lung Vclume. g Minute Volume. h Respiratory Rate. i Lnspiratory Time. j Expiratory Time. k Total Time. Significance at Tukey post hoc, p < 0.05 comparing with baseline). b

c

*

muscle and at each load. No correlation between myoeletrical activity and volume variation was detected. The reduction in predominant activity frequency using SEMG was computed by the variation of its measure (D SEMG) (Table 3). Women showed a tendency towards lower DSEMG, except for the right Sternocleidomastoid muscle. 4. Discussion The variation in chest wall volumes during acute incremental loads imposed on the respiratory system promoted an increase in air mobilization, which is dependent on the resistance level and can act differently in men and women. Changes were accompanied by altered muscle activity and reduced predominant activity frequency during high loads, while the decrease in both the Diaphragm changed at higher loads compared to both Sternocleidomastoids. The increase in air mobilization occurred mainly at high load levels, corroborating Nobre et al. (2007), who found an increase

in aerosol deposition with imposed loads from 20 cmH2O onwards and muscle activity, as evaluated by SEMG. A study conducted by Enright et al. (2006) submitted healthy subjects to Inspiratory Muscle Training for nine weeks with inspiratory load sustentation and found an increase in Vt, with morphologic changes (increased thickness) in the Diaphragm when compared to the control group. On the other hand, no ventilation changes were found by Griffths and McConnell (2007), who analyzed Inspiratory Muscle Training in rowing athletes for four weeks. Our study focused on the acute effects of incremental inspiratory loads and demonstrated that when resistance is applied, there is an increase in volume which is dependent of load intensity, showing different results from those reported in the literature regarding post-training volume changes. This may be due to the different intensities and frequencies of the applied loads. Considering the increase in volumes related to load intensity observed in clinical practice, the imposed load raises pressure generation capacity and flow, associated to a rise in secretion

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Fig. 3. Total and compartmental volumes: Pulmonary Rib Cage (Vrc,p), Abdominal Rib Cage (Vrc,a) and Abdomen (Vab) in women (upper graph) and men. (significance found with Tukey’s post hoc test compared with basal state). (Graph represented in milliliters and standard error).

Fig. 4. Comparison between loads (10–40 cmH2O) of predominant activity frequency of the muscles studied. [Sternocleidomastoid (SCMD)/Diaphragm (DI)] (p < 0.05) (Graph represented in Hertz and standard error).

A.E.F. Da Gama et al. / Journal of Electromyography and Kinesiology 23 (2013) 1269–1277 Table 3 Variation of predominant inspiratory muscle activity frequency in men and women (DSEMG = frequencystart frequencyend). Values expressed as means ± standard error.

*

Muscles

Men

Women

p*

Right sternocleidomastoid (Hz) Left sternocleidomastoid (Hz) Right diaphragm (Hz) Left diaphragm (Hz)

24.81 ± 5.96 42.68 ± 15.76 21.43 ± 16.17 15.06 ± 6.54

38.49 ± 10.75 14.79 ± 12.57 14.67 ± 9.37 8..11 ± 7.03

0.022 0.256 0.049 0.539

t-Student test for independent samples.

mobilization. This improvement in muscle strength and expectoration promotes an increase in lung volumes in patients with cystic fibrosis (Chatham et al., 1999). A recent meta-analysis regarding the effects of Inspiratory Muscle Training on COPD patients showed that it promotes an increase in inspiratory muscle endurance and strength, reducing the sensation of dyspnea after exercise; however, no volume changes were reported (Lotters et al., 2002). On the other hand, these changes in muscle activity corroborated the findings of the present study, since endurance and long activities are related to lower frequency of muscle activities. Changes in inspiratory muscle activity were concomitant with volume and ventilator modifications, where the Sternocleidomastoid and Diaphragm muscles exhibit a decrease in activation frequency from 30 cmH20 to 40 cmH20 onwards, respectively. The delay in Diaphragm alterations likely resulted from the tonic characteristics of this muscle (Sauleda et al., 1998), making it more adequate for endurance activity. By contrast, for the same study population as ours, Nobre et al. (2007) detected Diaphragm changes from 20 cmH20 onwards, with no alterations in the Sternocleidomastoid. Different signal analysis patterns may justify these differences, since this study evaluated predominant activity frequency, which is related to fiber type and recruitment, a different signal processing method from that employed by Nobre et al. (2007), who assessed Root Mean Square (RMS), which is correlated to muscle activity level. The decrease in predominant muscle activity frequency (González-Izal et al., 2012) to lower values and the number of subjects that became fatigued before the end of the protocol suggests a relationship between these changes and the onset of fatigue, in spite of the fact that fatigue effects cannot be differentiated from load effects in the current study. Neural changes in COPD subjects indicated an increase in the proportion of fiber type I and a rise in the number of mitochondria, thereby improving muscle resistance to fatigue (Gosselink, 2003). The reduction in predominant activity frequency observed in this study indicates that Inspiratory Muscle Training at high loads specifically impact type 1 resistance fiber, which has low discharge frequency (Sauleda et al., 1998), and that applying Inspiratory Muscle Training in COPD patients likely helps improve inspiratory muscle function. The predominant muscle activity frequency is related to the muscle fiber type that is being recruited (Reynaud-Gaubert et al., 2004). In the case of muscle fatigue, there is a decrease in activation frequency (Perlovitch et al., 2007); however, due to the different adaptation and physiological recruitment mechanisms during fatigue there is no decreased frequency value to define the fatigue level of the muscles studied. Further research is needed to determine the decrease in frequency values that indicates the fatigue status of these muscles. Taken together, the figures and tables show that lung volume behavior is accompanied by a tendency towards a reduced Respiratory Rate but at a determinate imposed load lung volume declines and Respiratory Rate increases. This inversion likely occurs when the subject reaches a high level of

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fatigue (McConnell and Griffths, 2010). However, the present study was conducted with healthy subjects and the Threshold? device did not enable a load higher than 41 cmH20. Thus, individuals may not have experienced complete inspiratory muscle fatigue, but rather submaximal fatigue, which precluded specific analysis at this stage. The predominant activity frequency exhibited different responses according to gender. Studies have demonstrated a similar proportion of type I and II fibers in men and women in different muscle groups (Staron et al., 2000). In spite of this proportion, a study conducted with the vastus lateralis of the quadriceps muscles (Staron et al., 2000) indicates that women have a tendency towards high activity and slow fiber hypertrophy, but no study has analyzed it for respiratory muscles. The frequency variation detected in men showed a decline from high frequency values to lower ones, that is, from fast to slow fibers, thereby changing recruitment. This may explain the lower variation in women due to their natural tendency to exhibit these slow fibers. Furthermore, the Diaphragm length–tension ratio changed according to the amount of lung volume interfering directly in its function (Hostettler et al., 2011) due this, the larger the volume during inspiration enable Diaphragm fiber a better length–tension promoting this way a higher the Maximal Inspiratory Pressure (Ribeiro et al., 2009). The higher air mobilization in men promotes more changes in the length–tension ratio of inspiratory muscles, which may also explain the higher variation in predominant inspiratory muscle frequency activity in this group. The Diaphragm muscle displays tonic physiology, whereas the Sternocleidomastoid is a phasic muscle that acts during forced inspiration (Sauleda et al., 1998). Given that the Sternocleidomastoid muscle has more fiber diversity, its predominant activity frequency showed greater variation between the start and end of the protocol when compared to the Diaphragm. 5. Conclusion The acute effect of incremental inspiratory loads, as used in Inspiratory Muscle Training, promotes an increase in Vt, primarily in the upper region of the chest wall, and Inspiratory Time. Muscle activity showed a decrease in predominant activity frequency in the Sternocleidomastoid and Diaphragm muscles, with declines occurring later in the latter. The physiological difference in muscles and respiratory pattern between men and women resulted in different responses to imposed loads. These differences should be considered during Inspiratory Muscle Training for pulmonary rehabilitation. Studies analyzing the effect of imposed loads on different pathologies should be carried out in order to provide better treatment for each specific group. Acknowledgement This studied received financial support from FACEPE (APQ0821-408/08-IBPG-1412-4.08/08) and CNPQ (3090672007-3) and CAPES PROCAD-NF-0792-2011. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.jelekin.2013.07.014. References Aliverti A, Stevenson N, Dellacà RL, Lo Mauro A, Pedotti A, Calverley PMA. Regional chest wall volumes during exercise in chronic obstructive pulmonary disease. Thorax 2004;59(3):210–6.

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Alana Elza Fontes Da Gama is a physiotherapist from the Federal University of Paraíba (2008), Brazil with M.Sc. (2011) in physiotherapy from Federal University of Pernambuco and actually she is Ph.D. candidate in Computer Science at Federal University of Pernambuco. Her two main research area are Respiratory Physiology and Biomechanics. In Respiratory Physiology her interests are focused on respiratory muscles, respiratory evaluation, electromyography of respiratory muscles and its signal process. In Biomechanics her studies are focused on biomechanical movement analysis with computer interaction for development of evaluation or rehabilitation systems based on virtual or augmented reality.

Larissa de Andrade Carvalho is graduated in Physicaltheraphy from the Federal University of Pernambuco in 2011. Her research interests include examining the effect of training on respiratory muscles, treating patients with respiratory and heart disorders. Her currently research about noninvasive ventilation in heart failure patients line of research to get her Masters degree in Physicaltheraphy from the Federal University of Pernambuco.

Larissa Andrade Feitosa is a physiotherapist from the Federal University of Pernambuco (2009), Brazil with M.Sc. (2012) in physiotherapy from Federal University of Pernambuco and actually she is Professor in cardiopulmonary area at Federal University of Sergipe. Her two main research area are cardiorespiratory Physiology and physiotherapy. Her main interests are focused on respiratory evaluation, asthma, cystic fibrosis, pediatric cardiopulmonary diseases and physiotherapy treatments.

Jasiel Frutuoso do Nascimento Junior is a physiotherapist from the Federal University of Pernambuco (2011), Brazil. Actually he is M.Sc. candidate in Physical Therapy at the same institution and his main research area involves Respiratory Physiology, Heart Failure and Cardiac Rehabilitation. Among respiratory physiology fields, his interests are focused on ventilatory patterns in health and disease, in terms of chest wall volume distribution. He also researches on respiratory muscles evaluation, especially diaphragmatic mobility. In Heart Failure and Cardiac Rehabilitation areas, his studies aim to asses exercise performance and cardiopulmonary interactions during aerobic exercise and training. His research is funded by grants from CNPq, Brazil.

A.E.F. Da Gama et al. / Journal of Electromyography and Kinesiology 23 (2013) 1269–1277 Marilú Gomes Netto Monte da Silva is graduated in Biomedical Engineering from the Federal University of Pernambuco (2008), Brazil, obtained her M.Sc. in Electrical Engineering at the same University in 2011, and actually she is doctor degree student in Electrical Engineering at the same University. Her two main research area are development of hardware and software for the medical area. In hardware, her interests are focused on acquisition of biomedical signals and images. In software, her interests are focused on processing of biomedical signals and images. Her current research is related to the development of brain machine interface. She is developing software that interprets the signal electroencephalography, and translates into real movements of some equipment to assist people with physical limitations.

César F. Amorim was born in São Paulo, Brazil. Graduated in Electronics Engineering from University of Vale do Paraiba - UNIVAP in 1992. He received his PhD in Biomedical Engineering from University of Vale do Paraiba - São Paulo, Brazil in 2009. He is professor of Biomedical Engineering Department and Physical Therapy Department. His areas of research interests are signal processing applied to biomedical signals, detection, processing and interpretation of surface EMG.

Andrea Aliverti is Associate Professor at the Politecnico of Milano (Dipartimento di Elettronica, Informazione e Bioingegneria) where he teaches Sensors and Instrumentation Technologies and Bioengineering of the Respiratory System.His research interests include respiratory mechanics in health and disease, physiological measurements, biomedical instrumentation and functional imaging.He is author of more than 90 full papers on peer reviewed journals and 10 patents. He is an active member of the European Respiratory Society (Chair of the Scientific Group Clinical Physiology, Exercise and Functional Imaging).

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Daniel Lambertz received his Dipl.-Ing. degree in physical engineering - biomedical engineering - from the University of Applied Science in Aachen (1995), Germany and his M.Sc. (1997) and Ph.D. (2002) degree in biomedical engineering from the University of Technology of Compiègne, France where he finished the postdoctoral training at the UMR CNRS 7338. His research interests are the understanding of the adaptive responses of neuromechanical properties of skeletal muscles due to hyper- and hypoactivity, rehabilitation, and maturation. Furthermore, modeling of the interaction between the mechanical and neurophysiological properties of skeletal muscles is within his interest. Actually he is a CNPq/FACEPE -DCR fellow at the Federal University of Pernambuco, Department of Sports Science-CAV, Vitória de Santo Antão, Brazil where he develops a biomechanics laboratory to quantify the neuromechanical properties in children.

Marco Aurélio Benedetti Rodrigues is Adjunt Professor IV from the Department of Electronics and Systems, Federal University of Pernambuco, Brazil. He is graduated in Electrical Engineering from the Catholic University of Pelotas (1994), M.Sc. and Ph.D. in Electrical Engineering from the Federal University of Santa Catarina (1997, 2002), both in the area of Biomedical Engineering. His current research in the areas of: Instrumentation applied in Physiotherapy, Prototyping of Hardware, Biomedical Signal Processing Techniques, IA and development of Artificial Neural Networks and Human Machine Interface.

Armèle Dornelas de Andrade is Associate Professor at the Universidade Federal de Pernambuco specializes in cardiorespiratory physiotherapy and physiology. Her professional training includes doctoral studies at the University of Aix Marseille, France, and postdoctoral studies at the University of British Columbia, Canada. In her University she is Director of Research, Coordinator of Cardiopulmonary Physiotherapy Laboratory, and Coordinator of Cardiorespiratory Physiotherapy Specialization. Her research interests include: respiratory muscles, respiratory mechanics in health and disease and physiological measurements. She has published in the importants scientific journals (peer reviewed journals). Her honors include: review panel member, Physiotherapy and Occupational Therapy for the prestigious Brazilian research-funding agency (CNPq, FACEPE, CAPES and others).