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O2 during
cycling exercise in COPD patients
1 Centre de Recherche, Hôpital Laval, Institut Universitaire de Cardiologie et de Pneumologie de l'Université Laval, Sainte-Foy, Québec, Canada G1V 4G5; and 2 Department of Medicine, Division of Cardiology, Duke University Medical Center, Durham, North Carolina 27710
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Patients with chronic
obstructive pulmonary disease (COPD) usually stop exercise before
reaching physiological limits in terms of O2 delivery and
extraction. A plateau in lower limb O2 uptake (
O2) and blood flow occurs despite
progression of the imposed workload during cycling in some patients
with COPD, suggesting that maximal capacity to transport O2
had been reached and that it had been extracted in the peripheral
exercising muscles. This study addresses this observation.
Symptom-limited incremental cycle exercise was performed by 14 men
[62 ± 11 (SD) yr] with severe COPD (forced expiratory volume in
1 s = 35 ± 7% of predicted value). Leg blood flow was
measured at each exercise step with a thermodilution catheter inserted
in the femoral vein. This value was multiplied by two to account for
both working legs (
LEGS). Arterial and femoral
venous blood was sampled at each exercise step to measure blood gases.
Leg O2 consumption
(O2LEGS) was calculated
according to the Fick equation. Total body
O2
(O2TOT) was measured from
expired gas analysis, and tidal volume (VT) and minute
ventilation (E) were derived from the flow signal. In eight patients, O2LEGS
kept increasing in parallel with
O2TOT as external work rate
was increasing. In six subjects, a plateau in
O2LEGS and
LEGS occurred during exercise (increment of <3%
between 2 consecutive increasing workloads) despite the increase in
workload and O2TOT
[corresponding mean was 110 ± 38 ml (11 ± 4%)]. These
six patients also exhibited a plateau in O2 extraction during exercise. Peak exercise work rate was higher in the eight patients without a plateau than in the six with a plateau (51 ± 10 vs. 40 ± 13 W, P = 0.043). VT,
E, and dyspnea were significantly greater at
submaximal exercise in patients of the plateau group compared with
those of the nonplateau group. These results show that, in some
patients with COPD, blood flow directed to peripheral muscles and
O2 extraction during exercise may be limited. We speculate that redistribution of cardiac output and O2 from the lower
limb exercising muscles to the ventilatory muscles is a possible mechanism.
oxygen uptake; chronic obstructive pulmonary disease
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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PATIENTS WITH ADVANCED chronic obstructive pulmonary disease (COPD) stop exercise because of exertional discomfort (12); in many of them, psychological factors such as anxiety, fear of dyspnea, and poor motivation may contribute to exercise intolerance (2). In these individuals, exercise termination is thought to occur before the physiological limits, in terms of O2 delivery and O2 extraction of the exercising muscles, have been reached (6, 10).
In conducting a study on lower limb perfusion during cycling exercise
in patients with COPD, we noted that some individuals had a plateau in
lower limb O2 uptake (O2)
despite progression of the imposed workload (16).
According to the Fick principle, such a plateau in lower limb
O2 must be accompanied by a leveling off
in leg blood flow and O2 extraction. If true, this
observation suggests that, in some patients with COPD, lower limb
O2 may be physiologically limited during
whole body cycling exercise.
The primary objective of this study was to address the hypothesis that
the maximal ability to transport O2 to the peripheral muscles and extract it may be exhausted during whole body cycling exercise in a significant proportion of patients with severe COPD. This
phenomenon should be demonstrated by a plateau in lower limb O2 while external work rate is
increasing. As a secondary objective, we assessed the possible impact
of the plateau in lower limb O2 on work capacity.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Patient Populations
Fourteen men with severe COPD volunteered to participate in this study. Only one of these patients participated in our previous investigation of the hemodynamic response of the lower limb during exercise in COPD (16). The diagnosis of COPD was based on current or past smoking history, clinical evaluation, and pulmonary function tests (1). To improve the homogeneity of this group of patients, other inclusion criteria included resting arterial PO2 (PaO2) above 60 Torr and body weight between 90 and 110% of ideal body weight. Subjects were stable at the time of the study, and none suffered from other significant medical conditions that could limit their capacity to perform an exercise test. No patients were taking systemic corticosteroids or were involved in a regular exercise training program. All but one patient were retired, and none reported heavy recreational activity. The research protocol was approved by the institutional ethics committee, and a written consent form was obtained from each patient.Protocol
Catheter placements and leg blood flow measurements.
Single-leg blood flow (LEG) was measured with a
thermodilution catheter (model 93 A-105-5F, Edwards Laboratory, Santa
Ana, CA) as previously described and used in this laboratory (16, 24, 25). After the right groin was shaved, disinfected, and anesthetized with lidocaine, the catheter was inserted in the femoral
vein 2 cm below the inguinal ligament with the distal thermistor tip
positioned 10-12 cm above the inguinal ligament in the external
iliac vein. The catheter was interfaced with a Gould Statham SP 1435 cardiac output computer (Oxnard, CA), and boluses of 1-5 ml iced
or room temperature saline were injected to obtain two to four flow
measurements at rest and during each exercise step. Thermodilution
curves were displayed on the Gould recorder to ensure a monophasic
curve with an exponential decay. The validity and reproducibility of
the LEG measurements, using this equipment and
methodology, have been previously evaluated by Sullivan et al.
(24, 25). In these studies, a close relation (r = 0.98, P < 0.01) was found between
thermodilution flow measured with this catheter system and simultaneous
paired electromagnetic flow probe measurements in a perfused canine
preparation (24). The variability of this measurement in
healthy subjects and in patients with heart failure in whom duplicate
submaximal exercise tests were performed was 16 ± 9%
(25). To sample the femoral venous blood, an indwelling
catheter was also inserted in the right femoral vein 1 cm below the
thermodilution catheter. Finally, a cannula was placed in a radial artery.
Exercise test.
Subjects were seated on an electrically braked ergocycle and connected
to a gas-analysis system through a mouthpiece. This gas-analysis system
consisted of a pneumotachograph, O2 and CO2 analyzers, and a mixing chamber (Quinton QMC, Quinton, Bothell, WA).
After subjects rested for 5 min, a progressive and symptom-limited stepwise exercise test, with room air breathing and starting at a work
rate of 10 W, was performed. Each exercise step lasted 3 min, and
increments of 10 W were used. At rest and during exercise, five-breath
averages of O2 and minute ventilation
(E) were obtained, and respiratory rate (RR) and
tidal volume (VT) were derived from the flow signal.
Dyspnea and leg fatigue perception were rated during the last minute of
each exercise step using the Borg 10-point scale (3).
LEG measurements were obtained during the second
minute of each exercise step; the arterial and femoral blood were
sampled during the last minute. Because LEG measurements were obtained before blood sampling and probably before a
steady state was reached, a small error in leg
O2 calculation can be expected. Our
laboratory has previously estimated that this may lead to an ~5%
underestimation in leg O2
(16). Blood samples were placed in iced water until the
end of the exercise test and processed within 30 min of withdrawal.
Blood pressure was measured from the arm that was not cannulated during
the last minute of each exercise step using an automated stress-testing blood pressure monitor (Quinton Q412).
Calculation.
The alveolar-arterial PO2 difference
(A-aDo2) was calculated with the following formula
(PB 
PH2o × FIO2) PaCO2/RER, where PB is barometric
pressure, PH2o is water vapor pressure,
PaCO2 is arterial PCO2, and
RER is respiratory exchange ratio. Arterial and venous O2
contents (CaO2 and
CfvO2, respectively) were calculated with
the following formula: 1.39 × Hb × O2
saturation + 0.003 × PO2.
LEG measurements were multiplied by two to account
for both exercising legs (LEGS). Leg
O2
(O2LEGS) was calculated from
the arterial-femoral venous O2 content difference
(CaO2-CfvO2) multiplied by LEGS (Fick principle). The leg
O2 extraction ratio was calculated from
CaO2 divided by the difference between
CaO2 and CfvO2. Leg vascular
resistance was calculated as the ratio of mean blood pressure to
LEGS.
Statistical Analysis
Results are expressed as means ± SD. The predicted values used for spirometry, lung volume, and lung CO-diffusing capacity are those of Knudson et al. (13), Goldman and Becklake (7), and Cotes and Hall (5), respectively. The maximal voluntary ventilation (MVV) was estimated by multiplying forced expiratory volume in 1 s (FEV1) by 35 (4). A plateau inLEGS and
O2LEGS during exercise was
defined a priori by an increment of <3% between two consecutive
workloads (17). Changes in
O2LEGS,
LEGS, and
CaO2-CfvO2 during the course
of the exercise were compared between patients with and without a
plateau in O2LEGS using profile analysis (23). Resting and exercise
characteristics of patients with and without a plateau in their
O2LEGS were compared using
unpaired two-tailed Student's t-tests.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Patient Characteristics
Patient characteristics are presented in Table 1. On average, they had a normal body mass index (20-25 kg/m2), severe airflow obstruction with an FEV1 of 35 ± 7% of predicted, slight reduction in PaO2, and normal resting PaCO2. Each subject completed a symptom-limited incremental exercise test with peak power output ranging from 30 to 70 W. All subjects had classical evidence of ventilatory and gas-exchange limitation at peak exercise such as peakE-to-MVV ratio (peak E/MVV) > 1 (1.04 ± 0.25), arterial O2 desaturation (change
in arterial O2 saturation from rest to peak exercise of
5 ± 4%), and CO2 retention
(
PaCO2 from rest to peak exercise of +6 ± 4 Torr).
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O2LEGS
and Total Body O2
O2LEGS was found (Fig.
1). In these subjects, the changes in
O2LEGS between peak exercise
and the immediately preceding workload was 9 ± 9%. The remaining eight patients demonstrated a 24 ± 10% increase in
O2LEGS between peak exercise
and the immediately preceding workload.
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The average time courses of changes in total body
O2
(O2TOT),
O2LEGS,
LEGS, and
CaO2-CfvO2 during exercise for
patients with and without a plateau in
O2LEGS are provided in Fig.
2. As can be seen in the plateau group,
O2TOT was still increasing [mean O2TOT between the
last two workloads = 110 ± 38 ml (11 ± 4%)] despite
the occurrence of a plateau in
O2LEGS. The time course of
change in O2TOT during
exercise was similar between the two groups, with no evidence of a
plateau. Peak O2TOT achieved in both groups of patients was not statistically different (0.99 ± 0.19 vs. 0.96 ± 0.17 l/min in the plateau group and the
nonplateau group, respectively). In contrast, the time courses of
changes in O2LEGS,
LEGS, and
CaO2-CfvO2
during exercise were significantly different between the two
groups as indicated by the profile analysis (P = 0.001). As expected, the plateau in
O2LEGS (Fig. 2A)
was accompanied by a corresponding phenomenon in
LEGS (Fig. 2C) and in
CaO2-CfvO2 (Fig.
2E). The O2 extraction ratio also plateaued in
the plateau group to reach 68 ± 12%, whereas it increased
progressively throughout the exercise period in the nonplateau group up
to a value of 75 ± 9% (P > 0.05).
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Comparison Between the Plateau and Nonplateau Group
Peak workload achieved was greater in the nonplateau group than in the plateau group (51 ± 10 vs. 40 ± 13 W, P = 0.043) (Table 2). Work efficiency was significantly different between the two groups with a higherO2TOT-to-work rate
ratio in the plateau group (17.1 ± 3.6 ml O2/W)
compared with the nonplateau group (12.9 ± 2.7 ml
O2/W, P = 0.029). At peak exercise, the
O2LEGS-to-O2TOT ratio was significantly lower in the plateau group than in the nonplateau group, averaging 52 ± 21% and 72 ± 10%,
respectively (P = 0.040).
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Patients of the two groups could not be differentiated on the basis of
their pulmonary function, blood gases, and Hb concentration (Table 1).
Body mass index and resting A-aDO2 were smaller
in patients of the nonplateau group compared with those of the plateau group (P = 0.037 and 0.033, respectively).
LEGS and
CaO2-CfvO2 tended to be
greater at peak exercise in the nonplateau group (Table 2). As a
result, peak O2LEGS was
significantly greater in the nonplateau group than in the plateau group
(P = 0.036). Leg vascular resistance at peak exercise
was higher in the plateau group than in the nonplateau group
(P = 0.044). Both groups experienced similar degrees of
exercise-induced arterial O2 desaturation, CO2
retention, and acidosis. The time courses of changes in breathing pattern, symptom scores, and heart rate during exercise for both groups
are shown in Fig. 3. VT,
E, and dyspnea were significantly greater at
submaximal exercise in patients of the plateau group compared with
those of the nonplateau group. These values were similar at peak
exercise in both groups. The changes in RR and heart rate during
exercise were similar for the two groups.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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In this study, two behaviors of the
O2LEGS-work rate
relationship were found during cycling exercise in patients with COPD. In one subgroup of patients,
O2LEGS kept progressing in a
parallel fashion to O2TOT,
whereas external work rate was increasing. In other patients, a plateau
in O2LEGS occurred despite
the progression in O2TOT and
work rate. As expected from the Fick principle, this plateau in
O2LEGS was accompanied by a
leveling off in LEGS and in
CaO2-CfvO2. These results
indicate that, despite evidences of ventilatory limitation,
some patients with COPD exhaust their maximal ability to transport and
extract O2 in the peripheral muscles during whole body
cycling exercise. Furthermore, these limitations may have detrimental
effects on exercise tolerance, as indicated by the lower work capacity
in the plateau group compared with the nonplateau group despite similar peak O2TOT between the two
groups. Thus work efficiency was lower in patients of the plateau group.
In patients exhibiting a plateau in
O2LEGS, the increase in
O2TOT toward end-exercise
values could only be explained by an increase in metabolic activity
outside the legs. If we assume that total cardiac output did not
plateau, the only remaining physiological explanation for the plateau
in O2LEGS and in
LEGS is a redistribution of blood flow and
O2 from the exercising muscle toward another group of
muscles. Although measurements of total cardiac output would have been
necessary to exclude a plateau in total cardiac output, we believe that
this possibility is unlikely for two reasons. First, no patients
displayed any symptoms or signs of left or right ventricular
dysfunction and coronary heart disease, according to their past medical
history, physical examination, resting and exercise electrocardiogram,
and chest X-ray. Second, considering the parallel relationship between
O2 and cardiac output during exercise
(18), the fact that
O2TOT kept increasing until
end exercise suggests that total cardiac output was not limited in our patients.
Such a redistribution of blood flow between the lower limb and
respiratory muscles has been elegantly documented in elite athletes
(O2TOT = 64 ± 6 ml · kg
1 · min1) by Harms
and colleagues (8, 9). By manipulating the work of
breathing during near maximal exercise, these authors provided strong
evidence that, in elite athletes, cardiac output can be redistributed
between the exercising peripheral muscles and the ventilatory muscles.
Accordingly, we speculate that the most likely candidates for the
possible blood flow redistribution in our patients are the respiratory
muscles, with O2 during exercise that
might be sufficiently high in severe COPD to compete with the lower limb muscles for the available blood flow and O2
(15). Because each patient had severe airflow obstruction,
why then did only 6 of 14 patients exhibit a plateau in
O2LEGS? A potential
explanation is that there was a marked difference in work of breathing
between the two groups as suggested by the greater VT,
E, and dyspnea at submaximal exercise intensity in
patients of the plateau group compared with those of the nonplateau
group. This supports the idea that work of breathing and presumably
O2 and blood flow requirements of the ventilatory muscles
might have differed considerably between the two groups.
To provide a stronger conclusion on the concept of blood flow
redistribution, it would have been necessary to measure and compare
work of breathing between the two groups of patients and to evaluate
the effects of changing work of breathing (with noninvasive ventilatory
assistance for instance) on LEGS and the
O2LEGS-work rate
relationship during exercise (8). If our data
interpretation is correct, an increase in LEGS in
patients of the plateau group should occur with respiratory muscle
unloading. Richardson and colleagues (19) recently
evaluated the effects of the respiratory muscle unloading in COPD
patients who breathed a helium mixture during whole body cycling
exercise (high ventilatory requirement) and single-knee extension
exercise (low ventilatory requirement). Consistent with the concept of
blood flow redistribution, they found that breathing the helium mixture
was associated with higher peak O2 only
during whole body cycling exercise. Breathing a helium mixture during
single-knee extension exercise did not improve peak
O2 presumably because the maximum
ventilation and the demand placed on the respiratory muscles were lower
during this exercise modality, therefore reducing the potential of
blood flow redistribution from the respiratory to the knee-extensor muscles.
The mechanisms through which blood flow and O2 could be distributed preferentially to respiratory muscles or other muscles and not to peripheral muscles were not explored in the present study. It has been suggested that the diaphragm and other respiratory muscles may have a greater potential for exercise-induced vasodilatation compared with peripheral muscles because of their higher oxidative capacity (14). It has also been shown that increased respiratory muscle activity may increase systemic sympathetic activity, causing peripheral vasoconstriction at peak exercise (8). Such a mechanism may have occurred in our patients of the plateau group, which had a leg vascular resistance that was higher than in patients of the nonplateau group.
In addition to the plateau in LEGS, a limitation in
leg O2 extraction was necessary to obtain a plateau in
O2LEGS. In the presence of a
stable LEGS, this suggests that an impairment in
O2 transfer to the muscle may have contributed to the
limitation in O2LEGS in
patients of the plateau group (20). The analysis of the
muscle structure was beyond the scope of this study, but a possible
explanation for this is a reduction in muscle capillarization, which
has previously been reported in patients with COPD (26). An alternative mechanism for the impairment in muscle O2
conductance is a mismatch between the perfusion of the contracting
muscle units and their metabolic activity (21). The
limitation in O2 extraction during exercise supports the
concept of a peripheral component to exercise limitation, at least in
some patients with COPD.
Measurement of leg blood flow is technically difficult, and a key
question is whether the occurrence of a plateau in
O2LEGS was a true
physiological phenomenon or a technical artifact. The former
interpretation is supported by two evidences. First, in one patient,
the experimental procedure was performed on two separate occasions; in
addition to being involved in the present study, this patient also
participated in our previous investigation on leg blood flow
measurements in COPD (16). In both circumstances, O2LEGS plateaued at 40 W. Second, the work efficiency was lower in the plateau group compared
with the nonplateau group. This indicates, independently of
O2LEGS measurements, that a
greater proportion of O2TOT
was devoted to other muscles rather than to the lower limb muscles,
supporting our data interpretation that increased aerobic activity
outside the lower limb exercising muscles was occurring in our patients.
In the present investigation, blood-gas values were reported at 37°C
because changes in body temperature were modest at the level of
exercise reached by our patients (change in rectal temperature measured
with a thermocouple inserted 12-15 cm beyond the anal sphincter
<0.5°C; Maltais, LeBlanc, and Johnson, unpublished
observations). Assuming a similar change in arterial blood and
rectal temperature and a change in femoral venous blood temperature
0.5°C greater than rectal temperature (22), we
calculated that arterial and venous O2 saturation values
would be underestimated by ~2% and 6%, respectively
(11). Because both errors are in the same direction and
happened to be of similar absolute magnitude, they tend to cancel each
other out. As a result,
CaO2-CfvO2
and O2LEGS would be
underestimated by only 1-2% by avoiding to correct blood-gas values for body temperature changes during exercise.
In summary, the present results indicate that some patients with COPD
and severe airflow obstruction may reach their physiological limits in
terms of lower limb O2, blood flow, and
O2 extraction during cycling exercise. Exercise tolerance
was lower in patients exhibiting these limitations. The present results
are consistent with the possibility of a blood flow redistribution
between the respiratory and lower limb muscles in patients with COPD.
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ACKNOWLEDGEMENTS |
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We are grateful to Marthe Bélanger, Marie-Josée Breton, and François Whittom for collaboration. We thank Serge Simard for statistical assistance and colleagues from the Centre de Pneumologie de l'Hôpital Laval for supporting the research.
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FOOTNOTES |
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This study was supported in part by the Fonds de la recherche en santé du Québec, by la fondation JD Bégin, Université Laval, and by Bayer. F. Maltais is a clinician-scientist of the Fonds de la recherche en santé du Québec.
Address for reprint requests and other correspondence: F. Maltais, Centre de Pneumologie, Hôpital Laval, 2725 Chemin Sainte-Foy, Sainte-Foy, Québec, Canada G1V 4G5 (E-mail: medfma{at}hermes.ulaval.ca).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 1 May 2000; accepted in final form 12 September 2000.
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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 R. A. Rabinovich, R. Bastos, E. Ardite, L. Llinas, M. Orozco-Levi, J. Gea, J. Vilaro, J. A. Barbera, R. Rodriguez-Roisin, J. C. Fernandez-Checa, et al. Mitochondrial dysfunction in COPD patients with low body mass index Eur. Respir. J., April 1, 2007; 29(4): 643 - 650. [Abstract] [Full Text] [PDF]
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O. Georgiadou, I. Vogiatzis, G. Stratakos, A. Koutsoukou, S. Golemati, A. Aliverti, C. Roussos, and S. Zakynthinos Effects of rehabilitation on chest wall volume regulation during exercise in COPD patients Eur. Respir. J., February 1, 2007; 29(2): 284 - 291. [Abstract] [Full Text] [PDF]
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 L. M. Romer, A. T. Lovering, H. C. Haverkamp, D. F. Pegelow, and J. A. Dempsey Effect of inspiratory muscle work on peripheral fatigue of locomotor muscles in healthy humans J. Physiol., March 1, 2006; 571(2): 425 - 439. [Abstract] [Full Text] [PDF]
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J. D. Miller, D. F. Pegelow, A. J. Jacques, and J. A. Dempsey Effects of augmented respiratory muscle pressure production on locomotor limb venous return during calf contraction exercise J Appl Physiol, November 1, 2005; 99(5): 1802 - 1815. [Abstract] [Full Text] [PDF]
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 A Aliverti, K Rodger, R L Dellaca, N Stevenson, A Lo Mauro, A Pedotti, and P M A Calverley Effect of salbutamol on lung function and chest wall volumes at rest and during exercise in COPD Thorax, November 1, 2005; 60(11): 916 - 924. [Abstract] [Full Text] [PDF]
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 P. T. Macklem Cell and Molecular Biology Is not the Only Way to a Better Understanding of Pathogenesis of Lung Disease Am. J. Respir. Crit. Care Med., July 1, 2004; 170(1): ii - iii. [Full Text]
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A Aliverti, N Stevenson, R L Dellaca, A Lo Mauro, A Pedotti, and P M A Calverley Regional chest wall volumes during exercise in chronic obstructive pulmonary disease Thorax, March 1, 2004; 59(3): 210 - 216. [Abstract] [Full Text] [PDF]
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F. Laghi and M. J. Tobin Disorders of the Respiratory Muscles Am. J. Respir. Crit. Care Med., July 1, 2003; 168(1): 10 - 48. [Abstract] [Full Text] [PDF]
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M. J. Mador, O. Deniz, A. Aggarwal, and T. J. Kufel Quadriceps Fatigability after Single Muscle Exercise in Patients with Chronic Obstructive Pulmonary Disease Am. J. Respir. Crit. Care Med., July 1, 2003; 168(1): 102 - 108. [Abstract] [Full Text] [PDF]
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 M. Velloso, S. G. Stella, S. Cendon, A. C. Silva, and J. R. Jardim Metabolic and Ventilatory Parameters of Four Activities of Daily Living Accomplished With Arms in COPD Patients Chest, April 1, 2003; 123(4): 1047 - 1053. [Abstract] [Full Text] [PDF]
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M. J. Mador, E. Bozkanat, and T. J. Kufel Quadriceps Fatigue After Cycle Exercise in Patients With COPD Compared With Healthy Control Subjects Chest, April 1, 2003; 123(4): 1104 - 1111. [Abstract] [Full Text] [PDF]
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G. L. Snider Enhancement of Exercise Performance in COPD Patients by Hyperoxia: A Call for Research Chest, November 1, 2002; 122(5): 1830 - 1836. [Abstract] [Full Text] [PDF]
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F. Lotters, B. van Tol, G. Kwakkel, and R. Gosselink Effects of controlled inspiratory muscle training in patients with COPD: a meta-analysis Eur. Respir. J., September 1, 2002; 20(3): 570 - 577. [Abstract] [Full Text] [PDF]
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