Relationship of Respiratory Effort Sensation to Expiratory Muscle Fatigue during Expiratory Threshold Loading 1 •2
SHUNSUKE SUZUKI, JUNNICHI SUZUKI, TOSHIKAZU ISHII, TADASHI AKAHORI, and TAKAO OKUBO Introduction
Respiratory effort increases under such conditions as increased ventilation, weakness of the respiratory muscles, increased impedance of the respiratory system, and mechanical disadvantage of the respiratory muscle (1). The sensory mechanism in the skeletal muscleof a limb is believed to be a conscious awareness of the outgoing motor command (2), but in the respiratory system, an increased motor output can be expected whenever the peripheral muscle becomes weakened or fatigued. During partial curarization, estimation of the size of an added load was overestimated and wasthought to depend in part on sensing the outgoing motor command (3). There is a difference of opinion concerning the relationship between the respiratory effort sensitization and the presence of inspiratory muscle fatigue. Gandevia and colleagues (4) and Supinski and coworkers (5) found that fatigue of the inspiratory muscles increased the sense ofeffort during breathing. Bradley's group, however, reported that respiratory sensation is independent of fatiguing contractions of the diaphragm but is directly related to the inspiratory intrathoracic pressure (6). Ward and colleagues found the development of diaphragmatic fatigue to be accompanied by a progressive increase in respiratory effort sensation; this change in sensory response was not related to a change in the intensity of diaphragmatic contraction (7). In patients with chronic obstructive pulmonary disease (COPD), the work of breathing is increased on both expiration and inspiration (8). Fatigue of the expiratory muscles develops in COPD, although it is less severe than that of the inspiratory muscles (9). However, the relationship between expiratory muscle fatigue and the respiratory effort sensation during expiratory loading has not been investigated. Accordingly,in this study weexamined how expiratory muscle fatigue would influence the respiratory effort sensation
SUMMARY We Investigated whether fatigue of the expiratory muscle, thst la, the abdominal muscle, may Beount for a change In the reeplratory effort sensation In nonnalaublecta during expiratory threshold loading. The respiratory effort sensation was scored using a modified Borg scale. expiratory muscle fatigue was_ _ d both from changes In the mexlmal static expiratory presaure and In the centroid frequency (fc) of the abdominal muscle electromyogram (EMG). Expiratory threshold loading (magnitude of threshold: 40 to 60% of the maximal expiratory praaaure at FRC, breathing 15Im/n, and duty cycle 0.5) was continued until exhaustion or for 30 mlfl. loading frequency was repeated following a 150mln I'IIC8Wry perIcKI after the end of the fIflIt ellJllratory 1eHIng. The maximal static expiratory presaure during loading (pm....,J decre88ed initially and then remained decreased. Decreases ware smaller with the 40% load (22 ± 6%, SEM) than with the 60% load (37 ± 3%) (p < 0.05). The decrease during the second run of the 60% load was greater than during the first (p < 0.01 by ANOVA). The maximal expiratory preaaure st TLC before the second run of the 60% load was decreasad by 9 ± 3% compared with the control (p < 0.02) but that with the 40% load was not. The fc with the 60% load decreased Initially by 8 ± 1% and then remalnad constant, although no change was observed with the 40% load. The sensory score at the 60% leed rose with time, and the increasing rate of ttle sensory score with time In the eecond Nfl exceeded that of the first (0.87 ± 0.25 veraue 0.62 ± 0.16 mln-', p < 8.85). The IncraaalAl ..te of the senMry score at the 40% load was Iowar then that ssen with the 10% lead (O.21 ± 0.87 veraus 0.12 ± 0.16 mln-', p < 0.02). The relationship between the sensory score end Pmmu was YlrtuaUy linear at all loadings. These four curves traced the same line, alt~ough the 10% IoadshIftINI to a higher _ tlon score than the 40% load and the second run shlftallt In a similar way. We conclude that the Increasad respiratory effort sensation during expiratory threshold loading Is closely related to expiratory muscle fatigue as Indlceted by the decrease In expiratory muscle force.
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AM REV RESPIR DIS 1992; 145:461-466
during the expiratory threshold loaded breathing. Weanalyzed this relationship by developing fatigue during loaded breathing using two magnitudes of expiratory threshold load and repeating the loadings in normal subjects. Methods Studies were performed in seven healthy nonsmoking men, aged 25to 32 yr, recruited from laboratory personnel. All were familiar with the respiratory maneuvers. The protocol was approved by the ethics committee of this institute, and informed consent was obtained before the study from all subjects. On the test days the subjects wereprohibited from drinking coffee or other caffeine-containing beverages. Spirometry was performed using a dry seal spirometer (OST-SO; Chest Co., Tokyo) and the lung volume was measured using a body plethysmograph (Autobox 2SOO, Gould, OH). During loaded breathing, airflow was measured using a Fleisch pneumotachograph (Fleisch #1, Lausanne, Switzerland) and a differential pressure transducer (Valildyne MP-45, Northridge, CA). Tidal volume was obtained by integration of
the airflow signal. Mouth pressure was monitored using a differential pressure transducer (Validyne MP-45, ±250 mm Hg) connected to the tap of the mouthpiece. A flanged mouthpiece was used to avoid air leakage around the lips during loading and the measurement of maximal expiratory pressure.The end-tidal carbon dioxide concentration was monitored by a mass spectrometer (WSMR1400;Westron Co., Chiba, Japan). Additionally, arterial oxygen saturation (Sao.) was obtained from a toe using a pulse oximeter (Biox 3700; Ohmeda, Boulder, CO).
Respiratory Pressures Respiratory muscle strength was evaluated by
(Receivedin originalform October 8, 1990and in revised form March 18, 1991) 1 From the First Department of Internal Medicine, Yokohama City University School of Medicine, Yokohama, Japan. 2 Correspondence and requests for reprints should be addressed to Shunsuke Suzuki, M.D., First Department of Internal Medicine, Yokohama City University School of Medicine, 3-9 Fukuura, Kanazawa-ku, Yokohama 236, Japan.
461
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measuring the maximal static mouth pressure obtained by maximally expiring against the closed valve. The maximal expiratory pressure (PEmax) was measured at total lung capacity (TLC) and functional residual capacity (FRC). The maximal expiratory pressure measurement was repeated until reproducible values were obtained in the control measurement. Toevaluate respiratory muscle fatigue, pressure measurements were done 15min following the end of threshold loading. Further, to evaluate changes in expiratory muscle fatigue during loading, wemeasured the maximal static expiratory mouth pressure at endexpiratoryvolumeeveryminute during loading (Pm max) and compared it with the control value measured at 1.0 Labove FRC. The latter was chosen based on a preliminary study in which the increase in FRC during loading was estimated to be 1.0 L.
Electromyogram The electromyographic (EMG) activity of the abdominal muscle was recorded from surface electrodes placed between the anterior iliac crest and the umbilicus. EMG signals were measured through a preamplifier (Model 1253A; San-eiNEC, Tokyo),bandpass filtered (FV-664; NF Electronic Instruments, Yokohama, Japan), and recorded on a magnetic tape with an FM data recorder (TEAC XR510, Tokyo). To obtain the electrical activities of the abdominal muscle, the EMG signals wererectified and integrated with a leaky integrator with a time constant of 100 ms (Model 1322,San-ei, NEC). Later, the EMG signalof'the expiratory phase of which the electrocardiographic (ECGFfree period was manually chosen was sampled at a rate of 1,000 Hz using a microcomputer (PC-9801 VM-4; NEC, Tokyo). The digitized EMG signal was analyzed by a fast Fourier transform (FFT). The centroid frequency (fc) was obtained according to Sieck and coworkers (10). The fc was expressed as a percentage of the average value of the first five breaths. Scaling of Respiratory Effort Sensation A category scale (lO-point modified Borg scale) (11, 12)was used to evaluate respiratory effort sensation. The Borg scale was displayed in front of the subject, who was asked to point to the position on the scale representing the magnitude of respiratory effort required to produce each breath at the time of the estimate. Estimates of respiratory effort sensation were obtained after the first 30 s of each loading to serve as the control value and repeated every minute until the subject could no longer reproduce the target mouth pressure. Threshold Loading The expiratory threshold load consisted of a spring-loaded poppet valve (threshold inspiratory muscle trainer; Healthscan Products, Inc., Cedar Grove, NJ) (13). We modified the spring of this valve to produce pressure loads ranging from 15 to 125 em H 20. This device was connected to the expiratory
SUZUKI, SUZUKI, ISHII, AKAHORI, AND OKUBO
port of a two-way valve (Hans-Rudolph #1400). The resistance through the valve on inspiration was approximately 1.1 em H 2 0 / L/s. On expiration the subject was required to produce a given mouth pressure to initiate and maintain airflow. During loading the subject breathed air through this two-way valve by supporting his cheeks with both hands while wearing a nose clip. The breathing cycle was 15 breaths/min, and the duty cycle of breathing (Ts/Ttot; Th, expiratory time; Ttot, total breathing cycleduration) was 0.5. To examine the effect of the magnitude of the load on the respiratory effort sensation, we used two magnitudes of threshold load, 40 and 60% of PEmax at FRC.
Protocol The study was done on two different days within a week and at the same time of day. The order of usage of threshold loads was randomized. After obtaining the control measurement of PEmax, we initiated expiratory threshold loaded breathing using either the 40 or 60070 load. The subject was asked to continue for 30 min or until exhaustion. Visual feedback of the mouth pressure signal displayed on the oscilloscope was used to restrict the breathing frequency to 15 breaths/ min and the expiratory duration to 2.0 s. The subject was encouraged to maintain a constant breathing frequency and duration of expiration. At the IS-min recovery period after the first run, the PEmax was measured; the second run, using the same expiratory threshold load, was started as with the first. During loaded breathing, the Pm max, sensory score, abdominal EMG, and end-tidal CO 2 concentration were assayed every minute. All signals were recorded on electromagnetic data tape (XR-5IO, TEAC) and on an eight-channel strip-chart recorder (Rectigraph 8K, San-ei NEC). Data were expressed as means ± SEM. Statistical analysis was done using two-way analysis of variance (ANOVA) for comparison of the two curves andWilcoxon signed-rank test for two values.
Results In both the first and second runs at the 600/0 load, three subjects were able to complete the fu1l30-min expiratory threshold loading. The endurance time of the four other subjects was shorter in the second run than the first (12.0 ± 3.8 versus 8.5 ± 2.3 min). The sensory score increased almost linearly with time (r = 0.95 ± 0.02 and 0.96 ± 0.02 for the first and the second runs) (figure 1). At the beginning of loading the increase in the sensory score with time was completely linear and then diminished, as seen in a negatively accelerating relationship. The sensory score-time curve of the second run with the 60% load shifted to a higher score compared with that of the first run (p < 0.01). Furthermore, the curve of the first run at the 60% load shifted
10 l!J
60% LOAD
8
0::
o U
(/)
6
o
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o
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CD
2
tsr Run VS. 2nd Run P
SHUNSUKE SUZUKI, JUNNICHI SUZUKI, TOSHIKAZU ISHII, TADASHI AKAHORI, and TAKAO OKUBO Introduction
Respiratory effort increases under such conditions as increased ventilation, weakness of the respiratory muscles, increased impedance of the respiratory system, and mechanical disadvantage of the respiratory muscle (1). The sensory mechanism in the skeletal muscleof a limb is believed to be a conscious awareness of the outgoing motor command (2), but in the respiratory system, an increased motor output can be expected whenever the peripheral muscle becomes weakened or fatigued. During partial curarization, estimation of the size of an added load was overestimated and wasthought to depend in part on sensing the outgoing motor command (3). There is a difference of opinion concerning the relationship between the respiratory effort sensitization and the presence of inspiratory muscle fatigue. Gandevia and colleagues (4) and Supinski and coworkers (5) found that fatigue of the inspiratory muscles increased the sense ofeffort during breathing. Bradley's group, however, reported that respiratory sensation is independent of fatiguing contractions of the diaphragm but is directly related to the inspiratory intrathoracic pressure (6). Ward and colleagues found the development of diaphragmatic fatigue to be accompanied by a progressive increase in respiratory effort sensation; this change in sensory response was not related to a change in the intensity of diaphragmatic contraction (7). In patients with chronic obstructive pulmonary disease (COPD), the work of breathing is increased on both expiration and inspiration (8). Fatigue of the expiratory muscles develops in COPD, although it is less severe than that of the inspiratory muscles (9). However, the relationship between expiratory muscle fatigue and the respiratory effort sensation during expiratory loading has not been investigated. Accordingly,in this study weexamined how expiratory muscle fatigue would influence the respiratory effort sensation
SUMMARY We Investigated whether fatigue of the expiratory muscle, thst la, the abdominal muscle, may Beount for a change In the reeplratory effort sensation In nonnalaublecta during expiratory threshold loading. The respiratory effort sensation was scored using a modified Borg scale. expiratory muscle fatigue was_ _ d both from changes In the mexlmal static expiratory presaure and In the centroid frequency (fc) of the abdominal muscle electromyogram (EMG). Expiratory threshold loading (magnitude of threshold: 40 to 60% of the maximal expiratory praaaure at FRC, breathing 15Im/n, and duty cycle 0.5) was continued until exhaustion or for 30 mlfl. loading frequency was repeated following a 150mln I'IIC8Wry perIcKI after the end of the fIflIt ellJllratory 1eHIng. The maximal static expiratory presaure during loading (pm....,J decre88ed initially and then remained decreased. Decreases ware smaller with the 40% load (22 ± 6%, SEM) than with the 60% load (37 ± 3%) (p < 0.05). The decrease during the second run of the 60% load was greater than during the first (p < 0.01 by ANOVA). The maximal expiratory preaaure st TLC before the second run of the 60% load was decreasad by 9 ± 3% compared with the control (p < 0.02) but that with the 40% load was not. The fc with the 60% load decreased Initially by 8 ± 1% and then remalnad constant, although no change was observed with the 40% load. The sensory score at the 60% leed rose with time, and the increasing rate of ttle sensory score with time In the eecond Nfl exceeded that of the first (0.87 ± 0.25 veraue 0.62 ± 0.16 mln-', p < 8.85). The IncraaalAl ..te of the senMry score at the 40% load was Iowar then that ssen with the 10% lead (O.21 ± 0.87 veraus 0.12 ± 0.16 mln-', p < 0.02). The relationship between the sensory score end Pmmu was YlrtuaUy linear at all loadings. These four curves traced the same line, alt~ough the 10% IoadshIftINI to a higher _ tlon score than the 40% load and the second run shlftallt In a similar way. We conclude that the Increasad respiratory effort sensation during expiratory threshold loading Is closely related to expiratory muscle fatigue as Indlceted by the decrease In expiratory muscle force.
=
=
AM REV RESPIR DIS 1992; 145:461-466
during the expiratory threshold loaded breathing. Weanalyzed this relationship by developing fatigue during loaded breathing using two magnitudes of expiratory threshold load and repeating the loadings in normal subjects. Methods Studies were performed in seven healthy nonsmoking men, aged 25to 32 yr, recruited from laboratory personnel. All were familiar with the respiratory maneuvers. The protocol was approved by the ethics committee of this institute, and informed consent was obtained before the study from all subjects. On the test days the subjects wereprohibited from drinking coffee or other caffeine-containing beverages. Spirometry was performed using a dry seal spirometer (OST-SO; Chest Co., Tokyo) and the lung volume was measured using a body plethysmograph (Autobox 2SOO, Gould, OH). During loaded breathing, airflow was measured using a Fleisch pneumotachograph (Fleisch #1, Lausanne, Switzerland) and a differential pressure transducer (Valildyne MP-45, Northridge, CA). Tidal volume was obtained by integration of
the airflow signal. Mouth pressure was monitored using a differential pressure transducer (Validyne MP-45, ±250 mm Hg) connected to the tap of the mouthpiece. A flanged mouthpiece was used to avoid air leakage around the lips during loading and the measurement of maximal expiratory pressure.The end-tidal carbon dioxide concentration was monitored by a mass spectrometer (WSMR1400;Westron Co., Chiba, Japan). Additionally, arterial oxygen saturation (Sao.) was obtained from a toe using a pulse oximeter (Biox 3700; Ohmeda, Boulder, CO).
Respiratory Pressures Respiratory muscle strength was evaluated by
(Receivedin originalform October 8, 1990and in revised form March 18, 1991) 1 From the First Department of Internal Medicine, Yokohama City University School of Medicine, Yokohama, Japan. 2 Correspondence and requests for reprints should be addressed to Shunsuke Suzuki, M.D., First Department of Internal Medicine, Yokohama City University School of Medicine, 3-9 Fukuura, Kanazawa-ku, Yokohama 236, Japan.
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measuring the maximal static mouth pressure obtained by maximally expiring against the closed valve. The maximal expiratory pressure (PEmax) was measured at total lung capacity (TLC) and functional residual capacity (FRC). The maximal expiratory pressure measurement was repeated until reproducible values were obtained in the control measurement. Toevaluate respiratory muscle fatigue, pressure measurements were done 15min following the end of threshold loading. Further, to evaluate changes in expiratory muscle fatigue during loading, wemeasured the maximal static expiratory mouth pressure at endexpiratoryvolumeeveryminute during loading (Pm max) and compared it with the control value measured at 1.0 Labove FRC. The latter was chosen based on a preliminary study in which the increase in FRC during loading was estimated to be 1.0 L.
Electromyogram The electromyographic (EMG) activity of the abdominal muscle was recorded from surface electrodes placed between the anterior iliac crest and the umbilicus. EMG signals were measured through a preamplifier (Model 1253A; San-eiNEC, Tokyo),bandpass filtered (FV-664; NF Electronic Instruments, Yokohama, Japan), and recorded on a magnetic tape with an FM data recorder (TEAC XR510, Tokyo). To obtain the electrical activities of the abdominal muscle, the EMG signals wererectified and integrated with a leaky integrator with a time constant of 100 ms (Model 1322,San-ei, NEC). Later, the EMG signalof'the expiratory phase of which the electrocardiographic (ECGFfree period was manually chosen was sampled at a rate of 1,000 Hz using a microcomputer (PC-9801 VM-4; NEC, Tokyo). The digitized EMG signal was analyzed by a fast Fourier transform (FFT). The centroid frequency (fc) was obtained according to Sieck and coworkers (10). The fc was expressed as a percentage of the average value of the first five breaths. Scaling of Respiratory Effort Sensation A category scale (lO-point modified Borg scale) (11, 12)was used to evaluate respiratory effort sensation. The Borg scale was displayed in front of the subject, who was asked to point to the position on the scale representing the magnitude of respiratory effort required to produce each breath at the time of the estimate. Estimates of respiratory effort sensation were obtained after the first 30 s of each loading to serve as the control value and repeated every minute until the subject could no longer reproduce the target mouth pressure. Threshold Loading The expiratory threshold load consisted of a spring-loaded poppet valve (threshold inspiratory muscle trainer; Healthscan Products, Inc., Cedar Grove, NJ) (13). We modified the spring of this valve to produce pressure loads ranging from 15 to 125 em H 20. This device was connected to the expiratory
SUZUKI, SUZUKI, ISHII, AKAHORI, AND OKUBO
port of a two-way valve (Hans-Rudolph #1400). The resistance through the valve on inspiration was approximately 1.1 em H 2 0 / L/s. On expiration the subject was required to produce a given mouth pressure to initiate and maintain airflow. During loading the subject breathed air through this two-way valve by supporting his cheeks with both hands while wearing a nose clip. The breathing cycle was 15 breaths/min, and the duty cycle of breathing (Ts/Ttot; Th, expiratory time; Ttot, total breathing cycleduration) was 0.5. To examine the effect of the magnitude of the load on the respiratory effort sensation, we used two magnitudes of threshold load, 40 and 60% of PEmax at FRC.
Protocol The study was done on two different days within a week and at the same time of day. The order of usage of threshold loads was randomized. After obtaining the control measurement of PEmax, we initiated expiratory threshold loaded breathing using either the 40 or 60070 load. The subject was asked to continue for 30 min or until exhaustion. Visual feedback of the mouth pressure signal displayed on the oscilloscope was used to restrict the breathing frequency to 15 breaths/ min and the expiratory duration to 2.0 s. The subject was encouraged to maintain a constant breathing frequency and duration of expiration. At the IS-min recovery period after the first run, the PEmax was measured; the second run, using the same expiratory threshold load, was started as with the first. During loaded breathing, the Pm max, sensory score, abdominal EMG, and end-tidal CO 2 concentration were assayed every minute. All signals were recorded on electromagnetic data tape (XR-5IO, TEAC) and on an eight-channel strip-chart recorder (Rectigraph 8K, San-ei NEC). Data were expressed as means ± SEM. Statistical analysis was done using two-way analysis of variance (ANOVA) for comparison of the two curves andWilcoxon signed-rank test for two values.
Results In both the first and second runs at the 600/0 load, three subjects were able to complete the fu1l30-min expiratory threshold loading. The endurance time of the four other subjects was shorter in the second run than the first (12.0 ± 3.8 versus 8.5 ± 2.3 min). The sensory score increased almost linearly with time (r = 0.95 ± 0.02 and 0.96 ± 0.02 for the first and the second runs) (figure 1). At the beginning of loading the increase in the sensory score with time was completely linear and then diminished, as seen in a negatively accelerating relationship. The sensory score-time curve of the second run with the 60% load shifted to a higher score compared with that of the first run (p < 0.01). Furthermore, the curve of the first run at the 60% load shifted
10 l!J
60% LOAD
8
0::
o U
(/)
6
o
0::
o
4
CD
2
tsr Run VS. 2nd Run P
