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(Chest. 2003;123:1794-1802.)
© 2003 American College of Chest Physicians

Exercise Training Improves Exertional Dyspnea in Patients With COPD*

Evidence of the Role of Mechanical Factors

Francesco Gigliotti, MD; Claudia Coli, MD; Roberto Bianchi, MD; Isabella Romagnoli, MD; Barbara Lanini, MD; Barbara Binazzi, MD and Giorgio Scano, MD, FCCP

* From Fondazione Don C. Gnocchi, IRCCS, Pozzolatico, Firenze.

Correspondence to: Francesco Gigliotti, MD, Section of Pulmonary Rehabilitation, Fondazione Don C. Gnocchi, IRCCS, Via Imprunetana 124, 50020 Pozzolatico, Firenze, Italy; e-mail: fgigliotti{at}dongnocchi.it


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Background: To our knowledge, no data have been reported on the effects of exercise training (EXT) on central respiratory motor output or neuromuscular coupling (NMC) of the ventilatory pump, and their potential association with exertional dyspnea. Accurate assessment of these important clinical outcomes is integral to effective management of breathlessness of patients with COPD.

Material and methods: Twenty consecutive patients with stable moderate-to-severe COPD were tested at 6-week intervals at baseline, after a nonintervention control period (pre-EXT), and after EXT. Patients entered an outpatient pulmonary rehabilitation program involving regular exercise on a bicycle. Incremental symptom-limited exercise testing (1-min increments of 10 W) was performed on an electronically braked cycle ergometer. Oxygen uptake (O2), carbon dioxide output (CO2), minute ventilation (E), time, and volume components of the respiratory cycle and, in six patients, esophageal pressure swings (Pessw), both as actual values and as percentage of maximal (most negative in sign) esophageal pressure during sniff maneuver (Pessn), were measured continuously over the runs. Exertional dyspnea and leg effort were evaluated by administering a Borg scale.

Results: Measurements at baseline and pre-EXT were similar. Significant increase in exercise capacity was found in response to EXT: (1) peak work rate (WR), O2, CO2, E, tidal volume (VT), and heart rate increased, while peak exertional dyspnea and leg effort did not significantly change; (2) exertional dyspnea/O2 and exertional dyspnea/CO2 decreased while E/O2 and E/CO2 remained unchanged. The slope of both exertional dyspnea and leg effort relative to E fell significantly after EXT; (3) at standardized WR, E, and CO2, exertional dyspnea and leg effort decreased while inspiratory capacity (IC) increased. Decrease in E was accomplished primarily by decrease in respiratory rate (RR) and increase in both inspiratory time (TI) and expiratory time; VT slightly increased, while inspiratory drive (VT/TI) and duty cycle (TI/total time of the respiratory cycle) remained unchanged. The decrease in Pessw and the increase in VT were associated with lower exertional dyspnea after EXT; (4) at standardized E, VT, RR, and IC, Pessw and Pessw(%Pessn)/VT remained unchanged while exertional dyspnea and leg effort decreased with EXT.

Conclusion: In conclusion, increases in NMC, aerobic capacity, and tolerance to dyspnogenic stimuli and possibly breathing retraining are likely to contribute to the relief of both exertional dyspnea and leg effort after EXT.

Key Words: COPD • dyspnea • exercise training • respiratory mechanics


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
The origin of exertional dyspnea in patients with COPD is multifactorial.1 2 The role of mechanical (physiologic) factors on exertional dyspnea has been clarified in a number of articles.1 2 3 4 5 6 7 8 Increased central respiratory motor output (CMO),9 impairment of respiratory muscle function,2 or abnormalities of neuromuscular coupling of the ventilatory pump,1 3 both associated with dynamic hyperinflation,3 6 have been reported to be involved in exertional dyspnea in patients with COPD.

In patients with moderate-to-severe airway obstruction, oxygen administration results in an increase in exercise performance and a decrease in exertional dyspnea, not directly related to changes in ventilatory mechanics such as inspiratory capacity (IC), or end-inspiratory lung volume.5 7 8 Likewise, exercise training (EXT) improves exercise capacity and exertional dyspnea, these changes being related neither to an increase in resting IC nor to inconsistent changes in IC during exercise.6 As yet, although EXT improves both exercise capacity and exertional dyspnea, the mechanical basis for both remains unexplained; however, it has been suggested that factors such as the development of increased symptom tolerance are also likely to play an important role in the reduced exertional dyspnea after EXT.5 10 11 12

To our knowledge, no data have been reported on the effects of EXT on CMO or neuromuscular ventilatory coupling (NMC) and the potential association with exertional dyspnea. The present study is an attempt to define this point. Accurate assessment of these important clinical outcomes is integral to effective management of breathlessness of patients with COPD.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Subjects
We studied 20 consecutive patients with stable moderate-to-severe COPD who were entering an outpatient pulmonary rehabilitation program. Patients satisfied the following criteria: (1) long history of smoking and moderate-to-severe chronic dyspnea; (2) clinically stable condition, with no exacerbation or hospital admission in the preceding 4 weeks; and (3) free from other significant disease(s) potentially contributing to dyspnea. Patients were all motivated to participate in the program and did not currently smoke.

Functional Evaluation
Routine spirometry and maximal inspiratory pressure obtained with subjects in a seated position was measured as previously described.13 14 15 Functional residual capacity (FRC) was measured by helium dilution technique. The normal values for lung volumes are those proposed by the European Respiratory Society.16 Before performing exercise, the ventilatory patterns were evaluated with subjects sitting comfortably in an armchair with a mass-flow sensor (max; SensorMedics; Yorba Linda, CA). The flow signal was integrated into volume.

For mechanical studies, an esophageal latex balloon (length, 10 cm; air volume, 0.5 mL) was introduced via the nose in six patients. A marker was placed on the polyethylene tubing 40 cm from the balloon tip.17 The catheter was connected to a differential pressure transducer (Validyne Engineering; Northridge, CA). The highest (most negative in sign) esophageal pressure during sniff maneuver (Pessn) was evaluated at FRC during a maximal sniff maneuver,15 18 which was repeated until three measurements with < 5% variability were recorded. The highest value of Pessn was used for subsequent analysis. Esophageal pressure (Pes) was also recorded during tidal breathing, and Pes swing (Pessw) was calculated as the difference between the Pes measured at end-expiration and at end-inspiration14 ; Pessw was expressed both as an absolute value and as a percentage of Pessn. The ratio of Pessw to %Pessn represents the force required for breathing relative to the maximal inspiratory force available, which is the inspiratory effort. From the spirogram, we derived the inspiratory time (TI), expiratory time (TE), total time of the respiratory cycle (TTOT), tidal volume (VT), mean inspiratory flow (VT/TI), and the timing (TI/TTOT). Respiratory rate (RR) [1/TTOT x 60] and minute ventilation (E) [VT x RR] were also calculated. The flow signal, integrated flow signal, and Pessw were recorded over a 10-min period on a personal computer hard disk using an eight-channel analog/digital board at 50 Hz sampling rate.

Exercise Testing
Incremental exercise testing (1-min increments of 10 W) was performed to a symptom-limited maximum on an electronically braked cycle ergometer (Ergo-Metrics 800s; SensorMedics). Patients were encouraged to keep exercising for as long as possible. Pedaling was held between 50 revolutions per minute and 60 revolutions per minute. The patients were made familiar with the apparatus on the days before the test. Expired gas was analyzed for E, oxygen uptake (O2), and carbon dioxide output (CO2) using breath-by-breath analysis from the max system. CO2 and O2 were expressed as standard temperature and pressure, dry, and as percentage of predicted maximum O2.19 The ventilatory equivalent for oxygen (E/O2), ventilatory efficiency (E/CO2), and maximal oxygen pulse (O2Pmax) were also calculated. For each run, changes in E, VT, and time components of breathing pattern (RR, TI, TE, TTOT) and Pes were continuously recorded. Anaerobic thresholds were assessed using the V-slope method.20

There was a continuous monitoring of 12-lead ECG and oxygen saturation by pulse oximetry (NPB 290; Nellcor Puritan Bennett; Pleasanton, CA). BP was recorded at rest and each 2 min during exercise and recovery to baseline levels.

The perception of dyspnea and leg discomfort was evaluated each minute during exercise by a 0 to 10 Borg scale. Dyspnea was described to the patients as sensation of labored or difficult breathing. Leg effort was described as the level of difficulty experienced during pedaling. The Borg scale is a vertical list with labeled categories (0 to 10) describing increasing intensities of dyspnea.21 Subjects were asked to rank the overall sensation of respiratory discomfort and leg effort by pointing to a score on a large Borg scale from zero (none) to 10 (maximal). The subjects were instructed that 0 signified no sensation at all and that 10 signified the most severe sensation that they had ever experienced.

Protocol
This was a single-center, two-period, controlled study in which subjects completed a 6-week nonintervention period before entering a 6-week pulmonary rehabilitation program involving regular EXT. In an initial screening, subjects were tested for pulmonary function and gas exchange, and esophageal (pleural) pressure. They were familiarized with exercise testing procedures and the various scale for rating symptom intensity, and they completed an incremental symptom-limited cycle exercise test. Three experimental visits were held at 6-week intervals immediately before the control period, after the control period (pre-EXT visit), and after EXT; therefore, subjects acted as their own controls. All visits were conducted at the same time of day for each subject.

Each patient attended a 6-week outpatient pulmonary rehabilitation program. The program included education, breathing retraining, and EXT. The training included cycle ergometer training, leisure walking, and unsupported arm exercise. For the training on the cycle ergometer, the workload corresponding to 80% of the peak work rate (WR) observed in the pretraining incremental exercise test was set as the training intensity. Sessions were closely supervised by a rehabilitation therapist; during the session, heart rate (HR) and arterial oxygen saturation were monitored. The study was approved by the ethics committee of the institution, and informed consent was obtained from all subjects.

Data Analysis
To compare responses to an identical level of exercise before and after the rehabilitation program, we selected the highest WR tolerated by a given patient during pre-EXT test (the standardized WR). To compare responses to identical level of ventilation, we selected the highest E tolerated by a given patient during the pre-EXT test (the standardized E). Values are mean ± SD. Nonparametric ratings of exertional breathlessness were compared before and after intervention using the Wilcoxon test. All other measurements made before and after EXT were analyzed using a paired t test. Pearson correlation coefficients were used to test the strength of the association between measured variables; p < 0.05 was considered significant.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Anthropometric and baseline function data of the 20 patients with moderate-to-severe airflow obstruction and hyperinflation, mild-to-moderate hypoxia, and mild carbon dioxide retention are shown in Table 1 . Data were not modified over the study.


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  		Table 1. Anthropometric Data and Lung Function*

 
Incremental Exercise Performance
A significant increase in exercise capacity was found after EXT but not over the control period: (1) peak WR (p < 0.001), E (p < 0.007), CO2 (p < 0.003), O2 (p < 0.001), and HR (p < 0.005) increased, while RR, O2Pmax, exertional dyspnea, leg effort, IC, E/CO2, and E/O2 did not significantly change (Table 2 ); (2) exertional dyspnea/O2 (p < 0.00001), exertional dyspnea/CO2 (p < 0.004), exertional dyspnea/E (p < 0.0005) [Fig 1 ], and leg effort/E (p < 0.05) decreased, while E/CO2, CO2/O2, and E/O2 did not change (Table 3 ).


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  		Table 2. Peak Exercise Response Before and After Rehabilitation*

 


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  		Figure 1. Slopes of exercise dyspnea (Borg ratings) relative to E significantly fell in response to EXT (p < 0.0005). Open symbols indicate before EXT; closed symbols indicate after EXT; circles indicate quiet breathing; triangles indicate standardized WR. See Table 2 for expansion of abbreviation.

 

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  		Table 3. Slopes of Exertional Dyspnea, Leg Effort, and E on Changes in O2 and CO2*

 
Changes at Standardized WR
Decrease in E (p < 0.0014) was accomplished primarily by an increase in VT (p < 0.001), TI (p < 0.0009), and TE (p < 0.004), and decrease in RR (p < 0.002) and RR/VT (p < 0.0002), with VT/TI and TI/TTOT remaining unchanged (p = not significant [NS]). HR (p < 0.01), CO2 (p < 0.001), exertional dyspnea (p < 0.0001), and leg effort (p < 0.0002) decreased while IC increased (p < 0.007) after EXT but not control (Table 4 ). At variance, changes in O2, E/O2, E/CO2, and O2Pmax were not significant after EXT. Individual changes in CO2 and RR after EXT at standardized WR are shown in Figure 2 .


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  		Table 4. Exercise Response at Standardized WR (70.5 ± 22.30 W)*

 


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  		Figure 2. Individual changes in CO2 and RR after EXT at standardized WR. pre/PRE = before EXT; POST/post = after EXT.

 
Changes at Standardized E
With EXT, WR (p < 0.0007) increased, and exertional dyspnea and leg effort decreased (p < 0.005 and 0.001, respectively), while IC, breathing pattern, O2, CO2, E/O2, and E/CO2 did not change (Table 5 ).


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  		Table 5. Exercise Response at Standardized E (36.7 ± 8.50 L/min)*

 
Pressure Changes
As shown in Table 6 , Pessw (p < 0.01) and Pessw(%Pessn)/VT (p < 0.03) did significantly change at standardized WR, the remaining changes being not significant. At standardized E, for a given VT, Pessw was lower after EXT (Fig 3 ).


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  		Table 6. Changes in Pessw, CMO, and NMC*

 


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  		Figure 3. Effect of EXT on NMC: changes in Pessw/VT ratio after EXT.

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
At a standardized WR, EXT increased IC, decreased exertional dyspnea, leg effort, E, CO2, and Pessw, and improved (reduced) Pessw(%Pessn)/VT, an index of abnormality of NMC of the ventilatory pump. Decrease in E was accomplished by decrease in RR both in actual value and per unit change in VT. At standardized E, exertional dyspnea and leg effort remained lower after EXT, while IC, breathing pattern, Pessw(%Pessn), an index of CMO, and NMC did not significantly change. Although the physiologic mechanisms involved in the reduction of dyspnea after EXT are likely complex, the following seem to play a major role: (1) cardiovascular factors, (2) decreased ventilatory demand, (3) decreased impedance to ventilatory muscle action, and (4) nonphysiologic factors.

Cardiovascular Factors
Morrison et al22 specifically linked cardiovascular and lung mechanical abnormalities. So did Montes de Oca et al,23 who found that the amount of oxygen delivery by the heart per beat (oxygen pulse) was the best predictor of maximal O2 in patients with COPD, implying that inadequate oxygen delivery was important in the impairment of exercise performance. Findings from studies by Venami et al24 and Nery et al25 are consistent with a low anaerobic threshold in both chronic heart failure and COPD due to right ventricular dysfunction leading to relative ischemia of exercising muscles. Had these factors played a role in increasing exercise performance with EXT, we would have observed an increase in O2Pmax, a noninvasive estimate of stroke volume26 ; therefore, we do not believe that in the circumstances of the present study, a cardiovascular effect was playing a major role in increasing exercise performance after EXT.

Decreased Ventilatory Demand
The abnormalities found in skeletal muscles,27 such as reduced oxidative capacity, contribute to exercise limitation in COPD. Oelberg et al28 suggested that the early lactate production could be related to a diminished capacity of exercising muscle in COPD to extract oxygen. Unlike the lack of changes in the slopes of E over O2 and CO2, the decrease in both E and CO2 at standardized WR indicates a decreased ventilatory demand (Table 4) . An increased aerobic capacity with EXT is in line with a decrease in lactate production reported in young patients with mild COPD29 and also in older severely obstructed patients.30 The variability we observed in CO2 individual changes at standardized WR (Fig 2) likely reflects the variability in ventilatory demand, aerobic capacity, and lactate production.

Decreased Impedance to Ventilatory Muscle Action
Despite an unaltered ventilatory equivalent for carbon dioxide, there was less Borg per-unit change in E after EXT. This would suggest an improved mechanical efficiency, which is usually accomplished by a decrease in dynamic elastance in association with decrease in dynamic hyperinflation. To the extent that total lung capacity (TLC) does not change appreciably during exercise in patients with COPD,31 a change in IC accurately reflects change in dynamic end-expiratory lung volume. The role of dynamic hyperinflation on dyspnea has been thoroughly investigated.1 32 Hyperinflation decreases maximal force-generating capacity (Pessn),2 33 34 thereby increasing the CMO to a weakened muscle. The decrease in Pessn along with the increase in inspiratory operational pressure (Pessw) increase the Pessw/Pessn ratio and thereby the sense of inspiratory effort.32 Furthermore, the association of an increased CMO with an increased respiratory system impedance increases the respiratory muscle load and may affect the coupling between inspiratory effort and volume, ie, the NMC1 ; therefore, a greater-than-normal sensation of dyspnea might be expected. According to this scenario, EXT reduced the slope of E to Borg (Table 3 , Fig 1 ); also, at standardized WR, EXT reduced breathlessness by reducing the inspiratory effort, end-expiratory lung volume, and RR, and improving NMC (Fig 3) . In this connection, Casaburi et al29 postulated that EXT improves ventilatory muscle endurance, causing a decrease in dynamic hyperinflation, explaining the slower and deeper pattern of breathing in severely obstructed exercising patients; however, improved skeletal muscle strength and endurance after EXT do not seem to be associated with change in breathing pattern, and neither do they correlate with improvement in breathlessness and leg effort.6 We provide evidence that for the same workload, maximal inspiratory output (Pessn) did not change while central respiratory output or effort (Pessw:%Pessn) decreased. Furthermore, the reduction in E, through the decrease in RR and the lengthening of TE, allowed more volume exhalation and decrease in dynamic hyperinflation.

Nonphysiologic Factors
Tolerance or desensitization to dyspnea may allow patients to reduce dyspnea and perform higher levels of work with reduced symptoms.35 36 We believe that an increased tolerance to dyspnea may have played an important role in the referred reduction of breathlessness at a standardized E (Fig 1) . Furthermore, breathing retraining may have actually improved the breathing pattern slowing RR.29 However, breathing retraining has not been shown to improve exercise tolerance37 or, as far as we know, to modify per se exertional dyspnea in patients with COPD, although breathing retraining could have contributed to increase the variability in RR decrease at standardized WR (Fig 2) .

Somewhat in line with previous reports,6 either dyspnea or leg effort, or both, limited exercise. Ventilatory and circulatory parameters were not significantly different in those limited by dyspnea (50%) or leg effort (27.5%), or a combination of both (22.5%) [Table 7 ]. This is consistent with the belief that the perception of effort to drive both respiratory and peripheral skeletal muscles plays an important role in limiting muscular performances.38 In this connection, it has been postulated that in conditions of moderate intensities of submaximal exercise when cardiac output is abnormally low and ventilatory work is high, the effect of the respiratory muscle load on maximal exercise performance might be due to the associated reduction in leg blood flow, which increases both leg fatigue and the intensity with which leg effort and inspiratory muscle effort (breathlessness) are perceived.39 Our data, showing that after EXT a similar decrease in exertional dyspnea and leg effort was associated with unchanged inspiratory effort and O2Pmax, indicate that in the circumstances of the present study other reasons for the decrease in perception of efforts should be sought.


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  		Table 7. Exercise Responses at Standardized WR in Two Subgroups of Patients*

 
We acknowledge that although changes in many variables were statistically significant, the consistency for some of them (eg, CO2, RR) was limited. This may provide weaker evidence to support our arguments, although not necessarily refute them.

In conclusion, reduced mechanical impedance along with increase in aerobic capacity help to explain, though not definitely, the decreased exercise breathlessness after EXT. Nonetheless, factors other than physiologic ones, such as development of increased tolerance to dyspnogenic stimuli and possibly breathing retraining, are likely to contribute to the relief of both exertional dyspnea and leg effort after EXT.


   Footnotes
 
Abbreviations: CMO = central respiratory motor output; EXT = exercise training; FRC = functional residual capacity; HR = heart rate; IC = inspiratory capacity; NMC = neuromuscular ventilatory coupling; NS = not significant; O2Pmax = maximal oxygen pulse; Pes = esophageal pressure; Pessn = esophageal pressure during sniff maneuver; Pessw = esophageal pressure swing; RR = respiratory rate; TE = expiratory time; TI = inspiratory time; TLC = total lung capacity; TTOT = total time of the respiratory cycle; VC = vital capacity; CO2 = carbon dioxide output; E = minute ventilation; O2 = oxygen uptake; VT = tidal volume; WR = work rate

This study was supported by a grant from the Fondazione Don C. Gnocchi ONLUS (IRCCS).

Received for publication December 21, 2001. Accepted for publication November 20, 2002.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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F. Gigliotti, C. Coli, R. Bianchi, M. Grazzini, L. Stendardi, C. Castellani, and G. Scano
Arm Exercise and Hyperinflation in Patients With COPD: Effect of Arm Training
Chest, September 1, 2005; 128(3): 1225 - 1232.
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 Am. J. Respir. Crit. Care Med.Home page
T. Troosters, R. Casaburi, R. Gosselink, and M. Decramer
Pulmonary Rehabilitation in Chronic Obstructive Pulmonary Disease
Am. J. Respir. Crit. Care Med., July 1, 2005; 172(1): 19 - 38.
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 Am. J. Respir. Crit. Care Med.Home page
N. S. Hopkinson, T. P. Toma, D. M. Hansell, P. Goldstraw, J. Moxham, D. M. Geddes, and M. I. Polkey
Effect of Bronchoscopic Lung Volume Reduction on Dynamic Hyperinflation and Exercise in Emphysema
Am. J. Respir. Crit. Care Med., March 1, 2005; 171(5): 453 - 460.
[Abstract] [Full Text] [PDF]

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 Eur Respir JHome page
G. Scano, L. Stendardi, and M. Grazzini
Understanding dyspnoea by its language
Eur. Respir. J., February 1, 2005; 25(2): 380 - 385.
[Abstract] [Full Text] [PDF]

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 BMJHome page
Minerva
BMJ, June 25, 2003; 326(7404): 1466 - 1466.
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