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Am. J. Respir. Crit. Care Med., Volume 156, Number 1, July 1997, 55-59

Reliability of Inspiratory Capacity for Estimating End-expiratory Lung Volume Changes during Exercise in Patients with Chronic Obstructive Pulmonary Disease

SHENG YAN, DARIUSZ KAMINSKI, and PAWEL SLIWINSKI

Montréal Chest Institute Research Centre, Montréal, Québec, Canada; and Institute of Tuberculosis and Lung Diseases, Warsaw, Poland

    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

The inspiratory capacity (IC) maneuver is increasingly used to monitor exercise-induced dynamic hyperinflation in patients with COPD. However, the reliability of this method in patients with COPD exercising to symptom limitation has not been systematically studied and presented. The purpose of the present study was therefore to evaluate the reliability of the IC maneuver in assessing changes in end-expiratory lung volume (EELV) by assessing the pressure developed during IC maneuvers, in patients with COPD during incremental bicycle exercise to exhaustion. Fifteen patients with stable COPD performed bicycle exercise to symptom limitation. During the experiment, the patients performed IC efforts during resting breathing and at the end of each exercise work load. Esophageal pressure (Pes) measured at peak inspired volume plateau (zero flow) was -13.5 ± 1.9 and -13.4 ± 1.9 cm H2O (p = 0.79) during IC maneuvers at resting breathing and during the final exercise work load, respectively. When the Pes values at the peak inspired volume plateau during IC efforts at each exercise level were expressed as a percentage of those during resting breathing, the great majority of the ratios were above 90% with the lowest at 84%, and these ratios were independent of exercise intensity. Despite a constant Pes during IC, there was a progressive decrease in IC with increasing exercise work load in most patients, suggesting an increase in EELV. At the highest exercise work load achieved, Delta EELV calculated as the decrease in IC was 0.26 ± 0.06 L (p < 0.001). We conclude that repeated IC maneuver is a simple and reliable method for estimating EELV changes during exercise to exhaustion in patients with COPD.

    INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Exercise limitation is one of the major features in patients with chronic obstructive pulmonary disease (COPD) and seriously affects the patient's quality of life. The impaired exercise performance in patients with COPD is largely due to failure of the available ventilatory reserve to meet increasing ventilatory demands (1, 2) as a result of increased ventilatory loads and impaired ventilatory muscle function (3, 4). During exercise, development of dynamic hyperinflation with progressive increase in end-expiratory lung volume (EELV) imposes additional elastic load to the ventilatory system and is closely related to exertional dyspnea, and it therefore contributes to exercise limitation in these patients (3, 5).

Repeated inspiratory capacity (IC) maneuvers have been used to estimate changes in EELV during exercise in patients with COPD (3, 5). Assuming a constant TLC (8), a decrease in IC indicates an equal increase in EELV. This method does not require complex equipment and can be performed easily during exercise in a pulmonary function laboratory. Therefore, Delta EELV could be included as a routine parameter for exercise testing in patients with COPD. TLC has been shown to be constant in normal subjects (9), in patients with interstitial lung disease (12) exercising to exhaustion, and in patients with COPD during submaximal exercise (8). The reliability of the IC method to evaluate EELV change in patients with COPD during exhaustive exercise has not been carefully assessed and presented since one may question whether or not TLC in patients with COPD remains constant and whether or not these patients are able to reach TLC by a brief IC effort during incremental exercise to exhaustion. The purpose of the present work was to systematically examine the reliability of the IC method to assess changes in EELV by recording esophageal pressure (Pes) at peak inspired volume plateau (zero flow) during incremental bicycle exercise to symptom limitation in patients with stable COPD. Although we did not measure TLC, our findings demonstrate that patients with stable COPD are able to consistently inspire to a constant peak lung volume presumably equal or close to TLC with IC maneuvers during exhaustive incremental exercise, and we therefore suggest that this method, albeit simple, is reliable in estimating changes in EELV in patients with stable COPD during this type of exercise testing protocol.

    METHODS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Patients

Fifteen clinically stable patients (13 male, two female) with variable degrees of chronic airflow obstruction were studied during an incremental bicycle exercise protocol after having given their informed consent. The protocol was approved by the appropriate Ethics Committee. All patients but four were smokers (average pack-year: 19.8 ± 3.4) and all had clinical and pathophysiologic evidence of chronic airway obstruction (Table 1), but without evidence of asthma, cardiovascular disease, and other diseases known to affect exercise performance. One patient underwent right upper lobectomy in 1987 because of lung cancer; thus this patient has a combined obstructive and restrictive mechanical abnormality of the respiratory system.

                              
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TABLE 1

PATIENTS' PULMONARY FUNCTIONS*

Procedures

During the experiment, each patient breathed through a mouthpiece while wearing a noseclip. Respiratory flow rate was measured by a Fleisch pneumotachograph-differential pressure transducer system (Validyne Engineering Corp., Northridge, CA). Tidal volume was obtained by integrating the flow signal. Pes was measured by a conventional balloon-catheter system, which was attached to a differential pressure transducer (Validyne). Mouth pressure (Pm) was also measured by a differential pressure transducer (Validyne). The esophageal balloon containing 0.5 ml air was positioned carefully at approximately the lower third of esophagus so that the cardiogenic oscillations were minimized and the difference between Delta Pes and Delta Pm during an occluded inspiratory or expiratory effort was zero (13).

Exercise Protocol

All the patients refrained from using bronchodilators at least 4 h prior to the exercise. The experiment was performed on an electronically braked cycle ergometer (Ergo-Metrics 800S; Ergo-Line, GmbH, Bitz, Germany). The cycling exercise was started at 10 or 20 W, and the load was progressively increased by 10 or 20 W every minute until exhaustion. During exercise, SaO2, arterial blood pressure, and electrocardiogram were monitored. During resting breathing and at the end of each level of exercise, an IC maneuver was performed such that the patients were asked to "make a further maximal effort on top of a maximal inspiration" (5, 14). No other specific training or coaching was made. Maximal inspiratory pressure (PImax) against an occluded airway was recorded at FRC during resting breathing and within 2 min after the termination of the incremental exercise.

Data Analysis

Flow and pressure signals were amplified, passed on an analog-to-digital converter, and recorded in a computer. Breathing parameters, including tidal volume (VT), breathing frequency (f), and minute ventilation (VE), were calculated from the flow signal. The data were analyzed in a computer by Anadat software (J.H.T. InfoDat Inc., Montréal, PQ). The mean Pes at maximal inspired volume plateau (zero flow) during each IC inspiration was measured. All values were expressed as means ± 1 standard error. For each participant, the variation of Pes values at the peak inspired volume plateau from each IC maneuver during exercise was expressed as a percentage of that obtained during resting breathing before exercise. The stability of these Pes values was examined by one-way repeated measures of ANOVA. The difference in PImax before and after exercise was compared by a paired t test. A p value less than 0.05 was considered to be statistically significant.

    RESULTS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

The peak exercise work load accomplished by our patients was 32.9 ± 4.1% of predicted (range, 17.0 to 69.4%). At the peak exercise work load, VT, f, and VE were 1.01 ± 0.12 L, 29.9 ± 1.9/min, and 28.13 ± 2.16 L/min.

The records of IC maneuvers performed during resting breathing and at the end of the peak exercise are shown in Figure 1. In phase with the period of zero flow at end-inspiration, a plateau of lung volume and Pes was observed during each IC effort. The duration of the volume plateau was 0.47 ± 0.09 s during the IC effort during resting breathing, which was reduced to 0.29 ± 0.04 s (p < 0.05) at peak exercise. This plateau with variable durations was observed in all patients during each IC effort.


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Figure 1.   Tracings of flow, lung volume, and esophageal pressure (Pes) from inspiratory capacity maneuvers taken during resting breathing and peak exercise from one representative patient. The arrows indicate the period of zero flow at end-inspiration, the peak inspired volume plateau, and corresponding Pes.

On average, the Pes values measured at peak inspired volume plateau during IC efforts at rest and during peak exercise were -13.5 ± 1.9 and -13.4 ± 1.9 cm H2O (p = 0.79), respectively. The Pes values at peak volume plateau during IC efforts plotted for each patient are shown in Figure 2. These values were essentially constant and independent of exercise intensity (p = 0.90). The within-subject mean standard deviation was 0.71 cm H2O. When the Pes values at peak volume plateau during IC efforts at different intensities of exercise were expressed as a percentage of those obtained from the IC effort during resting breathing, the majority of the ratios were above 90%, with the lowest ratio at 84% (Figure 3).


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Figure 2.   Individual esophageal pressure (Pes) values at peak lung volume plateau during inspiratory capacity maneuvers from rest to the highest exercise work load. It shows that the Pes values from any patient were constant and independent of exercise intensity.


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Figure 3.   Individual esophageal pressure (Pes) values at peak lung volume plateau during inspiratory capacity maneuvers during exercise are expressed as a percentage of those measured during resting breathing. The dashed lines show the 10 and 15% limits from unity.

Despite a constant Pes at peak volume plateau of the repeated IC maneuver, IC was progressively reduced with increasing exercise work load in most patients. As a result, as shown in Figure 4, the Delta EELV calculated from IC measurements was progressively increased during exercise. At the end of the exercise, the mean increase in EELV was 0.26 ± 0.06 L (p < 0.001).


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Figure 4.   Changes in end-expiratory lung volume (EELV) during exercise calculated from the changes in inspiratory capacity for each patient. QB = quiet breathing. The dashed line indicates the functional residual capacity during resting breathing.

Immediately after exercise PImax reduced by 9% compared with that before exercise (40.6 ± 3.3 versus 44.7 ± 4.1 cm H2O), but this did not reach a statistical significance (p = 0.064, one-tailed test).

    DISCUSSION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Previous studies have shown that TLC remains unchanged during both submaximal and maximal exercise in healthy subjects (9) and in patients with interstitial lung disease (12). Although Stubbing and coworkers (8) showed that TLC in patients with COPD did not change during exercise, the study was conducted in a small group of patients and the exercise was submaximal. Whether or not TLC changes in patients with COPD during exhaustive exercise is not known. The IC maneuver is a simple method to evaluate alterations in EELV. When this method is used during exercise in patients with COPD, it is assumed that these patients are able to generate a peak inspired volume during exercise that is the same as the TLC volume at rest. In order to evaluate the reliability of the IC maneuver in assessing dynamic hyperinflation during exhaustive exercise in patients with COPD, O'Donnell and Webb (5) tested the reproducibility of IC for a given exercise work load and found that it was quite reproducible. Because IC is determined by both EELV and TLC, both of which are likely to change during exercise, these data do not inescapably lead to the conclusion that TLC is constant or IC is reliable to measure Delta EELV in patients with COPD during exercise. Belman and coworkers (7) and Babb and colleagues (6) both measured transpulmonary pressure during repeated IC maneuvers during submaximal or maximal exercise, but neither of the groups reported the results. Therefore, reliability of the IC maneuver to monitor EELV in patients with COPD during exercise leading to exhaustion has not been carefully examined and reported. The current study systematically evaluated the reliability of IC maneuvers by comparing the Pes values at the peak inspired plateau volume during IC efforts in a group of patients with COPD during incremental exercise to exhaustion, and it showed that the Pes values were independent of exercise intensity. These results would suggest that in patients with COPD during incremental cycling exercise to exhaustion, TLC does not change and the IC maneuver is reliable in assessing Delta EELV caused by dynamic hyperinflation. However, since we did not measure the absolute TLC, we needed to assume that (1) during resting breathing the peak IC volume equals TLC, (2) the Pes value at the peak volume plateau during our IC effort reflects the elastic recoil pressure of the lung, and (3) the elastic properties of the lung do not change during exercise.

Younes and Kivinen (11) measured Pes at inspiratory plateau of the IC maneuvers during exercise in normal subjects, as we did in our patients, and found no significant change. Because a short period of zero flow was obtained at end-inspiration during those IC maneuvers, the Pes values at inspiratory plateau of the IC maneuvers were considered as reflecting the elastic recoil pressure of the lung at TLC (11). Because in the same experiment these investigators also showed no consistent change in TLC measured by a N2-washout technique, they concluded that the elastic recoil pressure of the lung does not change during exercise. In the present study, we also observed the end-inspiratory volume plateau during IC maneuvers even at the end of exercise prior to exhaustion. This was probably due partly to the fact that we asked our patients to make a further effort on top of the maximal inspiration during the IC maneuvers. In addition and more importantly, the average values of Pes at peak volume during the IC maneuvers in the present study (-13.5 and -13.4 cm H2O at rest and at exhaustive exercise, respectively) were numerically very close to those reported by Macklem and Becklake (14) (9.9 cm H2O), by Sharp and coworkers (15) (11 to 12 cm H2O, estimated from their Figure 2), and by Potter and colleagues (2) (11.5 cm H2O) for TLC static elastic recoil pressure of the lung. Therefore, we believe that our Pes values at peak inspired volume during IC maneuvers represent the pressure required to overcome the elastic recoil pressure of the lung at that volume.

It has been shown that the static lung compliance does not change during exercise in normal subjects (11). Whether or not the static lung compliance changes during exercise in patients with COPD is not clear. In this regard, the only published data that we are aware of are those reported by Stubbing and associates (8), who showed that during exercise the static lung compliance determined at midlung volume in patients with COPD decreased slightly, by approximately 14%. First of all, this slight decrease observed in static lung compliance did not reach the statistically significant level, and second, these investigators reported that the static lung compliance measured at 0.5 L above FRC at rest was 0.997 L/cm H2O, which is much higher than those reported by others for patients with COPD (14, 15). It would be possible that for unknown reasons they had overestimated the static lung compliance during resting breathing, leading to the observation of "a slight decrease" in static lung compliance during exercise. Thus, there has been no sufficient evidence to support changes in the static elastic properties of the lung during exercise in patients with COPD.

On the basis of the above, our present results, which demonstrated constant Pes values independent of exercise intensity at the maximal inspiratory plateau of the IC maneuvers, suggest that our patients were able to reproducibly inspire to an essentially constant peak lung volume, close or equal to TLC at different work loads. In other words, our results indirectly support the assumptions that TLC is constant and the repeated IC maneuvers are reliable in evaluating progressive EELV changes in patients with stable COPD under our experimental conditions. These results are consistent with the previous findings that (1) patients with stable COPD are able to nearly maximally activate their inspiratory muscles (diaphragm) during maximal inspiratory efforts (16, 17), and (2) severe inspiratory muscle fatigue leading to detectable reduction in the ability to generate pressure is not present after exhaustive exercise in these patients (18). Indeed, similar to the previous results (5), PImax in our patients was not significantly reduced after exhaustive exercise. As volume generation may be regarded as an ultimate goal of respiratory muscle contraction, IC would possibly be affected only when severe task failure of the inspiratory muscles occurs. This, however, is unlikely to happen during exercise, presumably because exertional breathlessness derived from heavy muscle loads and other confronting factors may terminate exercise (exhaustion) in these patients before severe fatigue develops (5, 18).

We found a progressive increase in EELV by a mean of 0.26 L at the end of exercise. This is very close to the 0.31 L reported recently for patients with COPD under a similar experimental protocol, supporting the notion that elevation of EELV is usually modest in patients with stable COPD during incremental exercise (5). However, the effect of such a change in operating lung volume on respiratory mechanics may be extremely detrimental to patients with COPD during exercise when one considers the significant reduction in ventilatory reserves in these patients, especially when compared with a usually reduced EELV to assist inspiration during exercise in normal subjects (5, 10, 19, 20). Hence, monitoring of changes in EELV during exercise testing in patients with COPD is desirable. Our data suggest that the indirect estimation of a progressive change in EELV can be reliably obtained by repeated IC maneuvers during incremental exercise in patients with stable COPD.

    Footnotes

Supported by the Association Pulmonaire du Québec, Montréal Chest Institute, and Polish State Research Committee.

Correspondence and requests for reprints should be addressed to Sheng Yan, M.D., Ph.D., Montréal Chest Institute Research Centre, 3650 St. Urbain Street, Room 526, Montréal, PQ, H2X 2P4 Canada.

(Received in original form August 29, 1996 and in revised form February 13, 1997).

    References
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

1. Clark, T. J. H., S. Freedman, E. J. M. Campbell, and R. R. Winn. 1969. The ventilatory capacity of patients with chronic airway obstruction. Clin. Sci. 36: 307-316 [Medline].

2. Potter, W. A., S. Olafson, and R. E. Hyatt. 1971. Ventilatory mechanics and expiratory flow limitation during exercise in patients with obstructive lung disease. J. Clin. Invest. 50: 910-919 .

3. Dodd, D. S., T. Brancatisano, and L. A. Engel. 1984. Chest wall mechanics during exercise in patients with severe chronic air-flow obstruction. Am. Rev. Respir. Dis. 129: 33-38 [Medline].

4. O'Donnell, D. E., R. Sanii, and M. Younes. 1988. Improvement in exercise endurance in patients with chronic airflow limitation using continuous positive airway pressure. Am. Rev. Respir. Dis. 138: 1510-1514 [Medline].

5. O'Donnell, D. E., and K. A. Webb. 1993. Exertional breathlessness in patients with chronic airflow limitation. Am. Rev. Respir. Dis. 148: 1351-1357 [Medline].

6. Babb, T. G., R. Viggiano, B. Hurley, B. Staats, and J. R. Rodarte. 1991. Effect of mild-to-moderate airflow limitation on exercise capacity. J. Appl. Physiol. 70: 223-230 [Abstract/Free Full Text].

7. Belman, M. J., W. C. Botnick, and J. W. Shin. 1996. Inhaled bronchodilators reduce dynamic hyperinflation during exercise in patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 153: 967-975 [Abstract].

8. Stubbing, D. G., L. D. Pengelly, J. C. Morse, and N. L. Jones. 1980. Pulmonary mechanics during exercise in subjects with chronic airflow obstruction. J. Appl. Physiol. 49: 511-515 [Abstract/Free Full Text].

9. Stubbing, D. G., L. D. Pengelly, J. L. C. Morse, and N. L. Jones. 1980. Pulmonary mechanics during exercise in normal males. J. Appl. Physiol. 49: 506-510 [Abstract/Free Full Text].

10. Babb, T. G., and J. R. Rodarte. 1991. Lung volume during low-intensity steady state exercise. J. Appl. Physiol. 70: 934-937 [Abstract/Free Full Text].

11. Younes, M., and G. Kivinen. 1984. Respiratory mechanics and breathing pattern during and following maximal exercise. J. Appl. Physiol. 57: 1773-1782 [Abstract/Free Full Text].

12. Marciniuk, D. D., G. Sridhar, R. E. Clemens, T. A. Zintel, and C. G. Gallagher. 1994. Lung volumes and expiratory flow limitation during exercise in interstitial lung disease. J. Appl. Physiol. 77: 963-973 [Abstract/Free Full Text].

13. Milic-Emili, J., J. M. Turner, and E. M. Glauser. 1964. Improved technique for estimating pleural pressure from esophageal balloons. J. Appl. Physiol. 19: 207-211 [Abstract/Free Full Text].

14. Macklem, P. T., and M. R. Becklake. 1963. The relationship between the mechanical and diffusing properties of the lung in health and disease. Am. Rev. Respir. Dis. 87: 47-56 .

15. Sharp, J. T., P. Lith, C. Nuchprayoon, R. Briney, and F. N. Johnson. 1968. The thorax in chronic obstructive lung disease. Am. J. Med. 44: 39-46 .

16. Similowski, T., S. Yan, A. P. Gauthier, P. T. Macklem, and F. Bellemare. 1991. Contractile properties of the human diaphragm during chronic hyperinflation. N. Engl. J. Med. 325: 917-923 [Abstract].

17. Similowski, T., A. P. Gauthier, S. Yan, P. T. Macklem, and F. Bellemare. 1993. Assessment of diaphragm function using mouth pressure twitches in COPD patients. Am. Rev. Respir. Dis. 147: 850-856 [Medline].

18. Polkey, M. I., D. Kyroussis, S. E. J. Keilty, C. H. Hamnegard, C. H. Mills, M. Green, and J. Moxham. 1995. Exhaustive treadmill exercise does not reduce twitch transdiaphragmatic pressure in patients with COPD. Am. J. Respir. Crit. Care Med. 152: 959-964 [Abstract].

19. Johnson, B. D., W. G. Reddan, D. F. Pegelow, K. G. Seow, and J. A. Dempsey. 1991. Flow limitation and regulation of functional residual capacity during exercise in physically aging population. Am. Rev. Respir. Dis. 143: 960-967 [Medline].

20. Sliwinski, P., S. Yan, A. P. Gauthier, and P. T. Macklem. 1996. Influence of global inspiratory muscle fatigue on breathing during exercise. J. Appl. Physiol. 80: 1270-1278 [Abstract/Free Full Text].





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Eur. Respir. J., June 1, 2003; 21(41_suppl): 19S - 28s.
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ChestHome page
V. Alvisi, A. Romanello, M. Badet, S. Gaillard, F. Philit, and C. Guerin
Time Course of Expiratory Flow Limitation in COPD Patients During Acute Respiratory Failure Requiring Mechanical Ventilation
Chest, May 1, 2003; 123(5): 1625 - 1632.
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ChestHome page
V. Alvisi, T. Mirkovic, P. Nesme, C. Guerin, and J. Milic-Emili
Acute Effects of Hyperoxia on Dyspnea in Hypoxemia Patients With Chronic Airway Obstruction at Rest
Chest, April 1, 2003; 123(4): 1038 - 1046.
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Am. J. Respir. Crit. Care Med.Home page
ATS/ACCP Statement on Cardiopulmonary Exercise Testing
Am. J. Respir. Crit. Care Med., January 15, 2003; 167(2): 211 - 277.
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Eur Respir JHome page
F. Di Marco, J. Milic-Emili, B. Boveri, P. Carlucci, P. Santus, F. Casanova, M. Cazzola, and S. Centanni
Effect of inhaled bronchodilators on inspiratory capacity and dyspnoea at rest in COPD
Eur. Respir. J., January 1, 2003; 21(1): 86 - 94.
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ChestHome page
T. E. Dolmage and R. S. Goldstein
Repeatability of Inspiratory Capacity During Incremental Exercise in Patients With Severe COPD
Chest, March 1, 2002; 121(3): 708 - 714.
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Am. J. Respir. Crit. Care Med.Home page
D. E. O'DONNELL, S. M. REVILL, and K. A. WEBB
Dynamic Hyperinflation and Exercise Intolerance in Chronic Obstructive Pulmonary Disease
Am. J. Respir. Crit. Care Med., September 1, 2001; 164(5): 770 - 777.
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ThoraxHome page
J Hadcroft and P M A Calverley
Alternative methods for assessing bronchodilator reversibility in chronic obstructive pulmonary disease
Thorax, September 1, 2001; 56(9): 713 - 720.
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Eur Respir JHome page
A. Somfay, J. Porszasz, S.M. Lee, and R. Casaburi
Dose-response effect of oxygen on hyperinflation and exercise endurance in nonhypoxaemic COPD patients
Eur. Respir. J., July 1, 2001; 18(1): 77 - 84.
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J. Appl. Physiol.Home page
V. Ugalde, S. Walsh, R. T. Abresch, H. W. Bonekat, and E. Breslin
Respiratory abdominal muscle recruitment and chest wall motion in myotonic muscular dystrophy
J Appl Physiol, July 1, 2001; 91(1): 395 - 407.
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Eur Respir JHome page
M.L. Ayers, R. Mejia, J. Ward, T. Lentine, and D.A. Mahler
Effectiveness of salmeterol versus ipratropium bromide on exertional dyspnoea in COPD
Eur. Respir. J., June 1, 2001; 17(6): 1132 - 1137.
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Am. J. Respir. Crit. Care Med.Home page
C. SINDERBY, J. SPAHIJA, J. BECK, D. KAMINSKI, S. YAN, N. COMTOIS, and P. SLIWINSKI
Diaphragm Activation during Exercise in Chronic Obstructive Pulmonary Disease
Am. J. Respir. Crit. Care Med., June 1, 2001; 163(7): 1637 - 1641.
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Am. J. Respir. Crit. Care Med.Home page
J. M. MARIN, S. J. CARRIZO, M. GASCON, A. SANCHEZ, B. GALLEGO, and B. R. CELLI
Inspiratory Capacity, Dynamic Hyperinflation, Breathlessness, and Exercise Performance during the 6-Minute-Walk Test in Chronic Obstructive Pulmonary Disease
Am. J. Respir. Crit. Care Med., May 1, 2001; 163(6): 1395 - 1399.
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Am. J. Respir. Crit. Care Med.Home page
D. E. O'DONNELL, C. D'ARSIGNY, and K. A. WEBB
Effects of Hyperoxia on Ventilatory Limitation During Exercise in Advanced Chronic Obstructive Pulmonary Disease
Am. J. Respir. Crit. Care Med., March 15, 2001; 163(4): 892 - 898.
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Am. J. Respir. Crit. Care Med.Home page
U. Hatipoglu, F. LAGHI, and M. J. TOBIN
Does Inhaled Albuterol Improve Diaphragmatic Contractility in Patients with Chronic Obstructive Pulmonary Disease?
Am. J. Respir. Crit. Care Med., December 1, 1999; 160(6): 1916 - 1921.
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Am. J. Respir. Crit. Care Med.Home page
S. YAN
Sensation of Inspiratory Difficulty during Inspiratory Threshold and Hyperinflationary Loadings . Effect of Inspiratory Muscle Strength
Am. J. Respir. Crit. Care Med., November 1, 1999; 160(5): 1544 - 1549.
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ChestHome page
B. D. Johnson, I. M. Weisman, R. J. Zeballos, and K. C. Beck
Emerging Concepts in the Evaluation of Ventilatory Limitation During Exercise: The Exercise Tidal Flow-Volume Loop
Chest, August 1, 1999; 116(2): 488 - 503.
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