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(Chest. 2003;123:1104-1111.)
© 2003 American College of Chest Physicians

Quadriceps Fatigue After Cycle Exercise in Patients With COPD Compared With Healthy Control Subjects*

M. Jeffery Mador, MD; Erkan Bozkanat, MD and Thomas J. Kufel, MD

* From the Division of Pulmonary, Critical Care, and Sleep Medicine (Drs. Mador and Bozkanat), State University of New York at Buffalo, Buffalo, NY; and the Veterans Affairs Western New York Healthcare System (Drs. Mador and Kufel), Buffalo, NY.

Correspondence to: M. Jeffery Mador, MD, Associate Professor of Medicine, Division of Pulmonary, Critical Care, & Sleep Medicine, Section 111S, State University of New York at Buffalo, Veterans Administration Medical Center, 3495 Bailey Ave, Buffalo, NY 14215; e-mail: mador{at}acsu.buffalo.edu


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: Quadriceps fatigue can occur in patients with COPD after exhaustive cycle exercise. The purpose of this study was to determine whether the degree of fatigue elicited by cycle exercise was greater in patients with COPD compared with matched control subjects.

Subjects: Nine male patients with COPD with a mean (± SE) age of 66 ± 3 years and mean FEV1 values of 1.31 ± 0.15 L and 36 ± 5% predicted were compared to nine healthy male subjects with a mean age of 66 ± 2 years.

Methods: Patients with COPD exercised at 60% of peak work capacity until exhaustion. Healthy elderly subjects exercised at a workload that was chosen to produce a similar absolute oxygen uptake (O2) during constant-load exercise as that obtained by the patients with COPD. Quadriceps fatigue was detected by measuring twitch force (unpotentiated twitch force [TwQu] and potentiated twitch force [TwQp]) before and after cycle exercise.

Results: Patients with COPD exercised for a mean duration of 8.4 ± 1.8 min. O2 during exercise was 50 ± 6% of predicted. The healthy elderly control subjects exercised for 10 min, generating a O2 of 48 ± 1% predicted. TwQu fell significantly postexercise in the patients with COPD but not in the matched control subjects. TwQp fell significantly postexercise in both groups, but the fall in TwQp postexercise was significantly greater in the patients with COPD.

Conclusion: For the same absolute O2 and duration of cycle exercise, the amount of fatigue elicited was significantly greater in the patients with COPD compared to age-matched healthy control subjects.

Key Words: COPD • exercise • muscle fatigue • skeletal muscle


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Following constant-workload cycle exercise to the limits of tolerance, contractile fatigue of the quadriceps muscle commonly occurs in patients with COPD.1 2 When elderly healthy subjects perform constant-workload cycle exercise to the limits of tolerance, contractile fatigue of the quadriceps muscle almost invariably occurs.3 However, patients with COPD have a considerably reduced exercise capacity. Thus, the amount of work performed by patients with COPD before they reach their symptomatic limits will be considerably lower than that achieved by healthy elderly subjects. Skeletal muscle dysfunction is common in patients with COPD4 5 6 and tends to involve preferentially either the lower limbs5 or proximal limb muscles.7 Muscle atrophy,5 muscle weakness,5 6 7 and reduced muscle endurance8 9 all have been observed in patients with COPD.

We hypothesized that for the same absolute oxygen uptake (O2) and the same duration of cycle exercise, the degree of contractile fatigue elicited by exercise would be greater in patients with COPD compared with matched healthy control subjects. It has been shown10 that fatigue of the quadriceps muscle can be detected with serial measurements of quadriceps twitch force (TwQ) during magnetic stimulation of the femoral nerve. A reduction in TwQ postexercise provides a quantitative estimate of the degree of contractile fatigue elicited by the exercise. Accordingly, we measured TwQ before and after high-intensity, constant-workload cycle exercise to the limits of tolerance in a group of patients with COPD. Healthy control subjects exercised at a workload chosen to produce the same O2 during exercise and for the same average amount of time as the patients with COPD. Similar to the patients with COPD, TwQ was measured before and after exercise. A significantly greater reduction in TwQ postexercise in the patients with COPD compared with the healthy control subjects would support our hypothesis.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Subjects
Nine patients with COPD and nine age-matched control subjects were studied. Anthropomorphic characteristics are summarized in Table 1 . The study was approved by the appropriate institutional review boards, and written informed consent was obtained from all subjects. The healthy control subjects underwent a screening history, physical examination, medication review, pulmonary function testing, and resting ECG to exclude significant underlying disease. The diagnosis of COPD was made using the criteria of the American Thoracic Society.11 Three patients were receiving home oxygen therapy. None of the patients were receiving oral steroid therapy. Seven patients were receiving inhaled steroid therapy, and one patient was receiving oral theophylline therapy.


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  		Table 1.. Patient Anthropomorphic Data*

 
Pulmonary Function and Exercise Testing
Pulmonary function was measured using standard techniques according to American Thoracic Society recommendations.12 Pulmonary function measurements are shown in Table 2 (reference values were derived from the work of Crapo and colleagues13 14 15 ). An incremental, symptom-limited maximal exercise test was performed on a cycle ergometer (CPE-2000; Medgraphics; St. Paul, MN) to estimate each subject’s maximal work capacity. During maximal incremental exercise testing, there was a 3-min acclimatization period followed by 1 min of pedaling at 0 W. The workload then was increased in 10-W increments each minute in the patients with COPD, and in 15-W increments in the healthy control subjects. The last workload a subject was able to complete 30 s of cycling was designated Wpeak.


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  		Table 2.. Pulmonary Function*

 
Expired gas was analyzed for O2 and CO2 by a zirconium electrochemical cell O2 analyzer and an infrared CO2 analyzer, respectively. Flow was measured with a pneumotachograph (preVent Pneumotach; Medgraphics). A microprocessor calculated breath-by-breath values of O2, CO2 production, and minute ventilation (E) and its components (ie, respiratory rate and tidal volume), and the results were averaged every 30 s. The anaerobic threshold was determined with the V-slope method.16 Reference values were derived from Wasserman et al.17

The pneumotachograph and gas analyzers were calibrated before each exercise test. The pneumotachograph was calibrated with a 3-L volume calibration syringe at widely varying flow rates. The gas analyzers were calibrated with two test gases of known composition (room air and 12.0% O2/5.0% CO2). The patients who were receiving oxygen breathed from a 200-L reservoir bag containing 35% O2. The inflow of O2 and room air to the bag was precisely controlled to keep the fraction of inspired oxygen (FIO2) in the bag at 35%. The FIO2 also was measured directly at the mouthpiece, and this FIO2 was used in the O2 calculations.

At least 2 days after the maximal exercise test, patients with COPD exercised at a constant workload of approximately 60% of Wpeak to the limits of tolerance. Elderly control subjects exercised at a workload that resulted in a O2 during exercise that was similar to that obtained by the patients with COPD. Elderly control subjects exercised for 10 min, which was slightly longer than the mean exercise time for the patients with COPD. All subjects had a 3-min warm-up period during which they exercised at a low workload before initiating exercise at the designated work rate. In the patients receiving home oxygen, exercise was performed while breathing supplemental oxygen.

Quadriceps Measurements
The femoral nerve was magnetically stimulated with a magnetic stimulator (Magstim 200; Magstim Co Ltd; Whitland, Dyfed, Wales, UK) using a 70-mm figure-of-eight coil.2 A 70-mm coil was used instead of the 45-mm coil that we have used in some previous studies because preliminary studies have demonstrated that maximal stimulation of the femoral nerve was achieved at lower power outputs with this coil particularly in obese individuals.2 Peak magnetic field intensity with this stimulating coil is 2.6 T. The coil was initially placed in the femoral triangle just lateral to the femoral artery and was repositioned systematically to determine the best location for subsequent stimulations. The position that resulted in the largest quadriceps twitch response was marked and used for the remainder of the study.1

A minimum of eight measurements of unpotentiated twitch force (TwQu) were obtained before exercise and at 10, 30, and 60 min postexercise. Following a vigorous voluntary contraction, the subsequent twitch is significantly increased in size (called twitch potentiation).18 Some studies19 20 have suggested that the potentiated twitch force (TwQp) is more sensitive at detecting fatigue than the TwQu, particularly when the amount of fatigue is small. Accordingly, we measured TwQ 5 s after a maximum voluntary contraction (MVC). Subjects maintained the MVC for 5 s, and visual feedback of the force signal was provided to the subject with an oscilloscope. The maneuvers were repeated a minimum of six times to obtain at least six TwQp measurements. However, because we showed in a prior study20 that the amount of potentiation was slightly less following the first MVC and, to a lesser extent, the second MVC, we discarded the first two measurements. Measurements of TwQp were obtained before exercise and at 10, 30, and 60 min postexercise. Measurements of TwQp always were obtained after the measurements of TwQu were completed.

The electromyogram was recorded with surface electrodes placed over the rectus femoris muscle. In some of the patients, magnetic stimulation of the femoral nerve elicited a large shock artifact that obscured the initial portion of the compound motor action potential (ie, the M wave). However, with careful positioning of the recording electrodes and ground, M waves were obtained in eight healthy control subjects and five of the patients with COPD.

To determine the degree to which our subjects could voluntarily activate their quadriceps muscle, twitches were obtained during the last two MVC maneuvers of each set of measurements.2 3 Measurements of superimposed twitches were compared to those of TwQp to determine the percentage activation during the MVC maneuver (100-superimposed twitch/potentiated twitch x 100).21

Measurements of all twitches were obtained at 100% of stimulator output. TwQ and quadriceps electromyogram were digitized and stored on disk (Windaq software; Dataq Instruments Inc; Akron, OH) at a sampling rate of 1,000 Hz.

Data Analysis
Changes in variables over time were analyzed by repeated-measures analysis of variance and paired t test with Bonferroni correction. Patients with COPD and healthy control subjects were compared by analysis of variance and unpaired t test. The data were expressed as the mean ± SE, unless otherwise stated.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
The results of the patients’ pulmonary function tests are shown in Table 2 . Our patients had moderately severe COPD with an FEV1 of 36 ± 5% of the predicted value, air trapping with a residual volume of 204 ± 25% of predicted, and severely impaired gas transfer with a diffusing capacity of 40 ± 6% of predicted. The maximal incremental exercise results are shown in Table 3 . Exercise capacity was severely decreased in our patients with COPD. The mean Wpeak was 63 ± 11 W, or 37 ± 4% of the predicted maximum. The peak O2 was 55 ± 8% of the predicted maximum. The end-exercise heart rate (HR) was 75 ± 4% of predicted, suggesting that there was some cardiac reserve at exercise termination. In contrast, peak exercise ventilation was 86 ± 9% of the predicted maximum voluntary ventilation (MVV; 40 x FEV1), suggesting that ventilatory limits were being approached at end-exercise. As expected, Wpeak was markedly higher in our sedentary control subjects (ie, 130 ± 8 W or 74 ± 5% of predicted). Exercise capacity was slightly decreased in our healthy elderly control subjects, likely reflecting deconditioning since we deliberately chose subjects who were sedentary to act as control subjects for our COPD patients (who were themselves quite sedentary). Our healthy control subjects appeared to give a reasonable effort, as reflected by their peak HR of 90 ± 4% of predicted and a respiratory quotient at end-exercise of 1.24 ± 0.03.


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  		Table 3.. Maximal Exercise Data*

 
The constant-workload exercise results are shown in Table 4 . The patients with COPD exercised at 37 ± 6 W (60 ± 1% of Wpeak), for 8.4 ± 1.8 min. O2 was 12.5 ± 1.4 mL/min/kg (50 ± 6% of predicted). The O2 during constant-load exercise was 95 ± 5% of the peak O2 obtained during the maximal exercise test. The peak HR was 77 ± 4% of predicted. Peak exercise ventilation was 43.4 ± 4.3 L/min, or 91 ± 15% of the predicted MVV. Our healthy control subjects exercised at 46 ± 2 W (36 ± 2% of Wpeak) for 10 min. The O2 was 13.7 ± 0.8 mL/min/kg (48 ± 1% of predicted). The O2 during constant-load exercise was 71 ± 4% of the peak O2 obtained during the maximal exercise test. The peak HR was 72 ± 5% of predicted.


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  		Table 4.. Endurance Exercise Data*

 
Quadriceps Measurements
TwQu measurements are shown in Figure 1 . TwQu fell significantly postexercise in the patients with COPD but not in the healthy elderly. The difference between the two groups was highly significant (p < 0.005). A representative example of the twitch response is shown in Figure 2 . TwQp measurements are shown in Figure 3 . TwQp fell significantly postexercise in both the patients with COPD and in the healthy elderly, but the fall in TwQp postexercise was significantly greater in the patients with COPD (p < 0.05). There was no significant change from baseline in the compound motor action potential at any time postexercise in either the patients with COPD or in the healthy control subjects for either TwQu or TwQp.



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  		Figure 1.. Quadriceps TwQu, expressed as a percentage of baseline before exercise and 10, 30, and 60 min postexercise, in the healthy elderly subjects and the patients with COPD is shown. * = significant difference from baseline; {dagger} = significant difference between the patients with COPD and the healthy elderly (by analysis of variance). TwQu fell after exercise in the patients with COPD but not in the healthy control subjects. The difference between groups was highly significant (p < 0.005).

 


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  		Figure 2.. Compound motor action potential (M wave) and TwQu from the quadriceps muscle before and after exercise in a representative patient with COPD (top, A) and in a healthy control subject (bottom, B) are shown. The preexercise data have been shifted slightly to the left to show the data more clearly. TwQ fell significantly after exercise in the patient with COPD but not in the healthy control subject, whereas M-wave amplitude remained unchanged in both groups.

 


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  		Figure 3.. Quadriceps TwQp, expressed as a percentage of baseline values before exercise and 10, 30, and 60 min after exercise, in the healthy elderly subjects and the patients with COPD is shown. * = significant difference from baseline; {dagger} = significant difference between the patients with COPD and the healthy elderly. TwQp fell after exercise in both the healthy control subjects and the patients with COPD, but the fall was significantly greater in the patients with COPD (p < 0.05).

 
The MVC at baseline was significantly smaller in the patients with COPD (40.3 ± 4.2 kg) than in the healthy elderly control subjects (58.8 ± 1.9 kg; p < 0.002). The MVC in patients with COPD averaged 68.5% of the values obtained in the healthy elderly control subjects. Both groups of patients were able to near maximally activate their quadriceps muscle during the MVC maneuvers, but the healthy control subjects achieved a slightly higher degree of activation than did the patients with COPD (Fig 4 ). The degree of activation during the MVC maneuvers did not change significantly postexercise in either group (Fig 4) . When the MVC was corrected for differences in activation, the MVC in patients with COPD still remained significantly decreased, averaging 72.9% of the values obtained for the healthy elderly control subjects.



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  		Figure 4.. Superimposed TwQ expressed as a percentage of the potentiated twitch before exercise and 10, 30, and 60 min after exercise in the healthy elderly and the patients with COPD is shown. = significant difference between patients with COPD and the healthy elderly. Superimposed TwQ did not change significantly from baseline at any time after exercise in either group, indicating that the degree of activation during the MVC maneuver was not reduced after exercise. The superimposed TwQ was significantly higher in the patients with COPD (p = 0.04), indicating that the healthy elderly control subjects achieved a higher level of activation during the MVC maneuver, although the absolute difference between groups was small.

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
The major finding of this study was that for the same exercise O2 and duration, patients with COPD displayed significantly greater contractile fatigue of the quadriceps muscle than did age-matched healthy elderly subjects.

Difference Between Patients With COPD and Control Subjects
In this study, we chose to match the two groups based on absolute workload. The patients with COPD exercised at a O2 that was near maximal during constant-load exercise. In contrast, the healthy control subjects exercised at a significantly lower O2 (as a percentage of peak O2) during constant-load exercise (Table 4) . Thus, the patients with COPD exercised at a higher relative exercise intensity. In healthy subjects at higher relative exercise intensities, the lactate and catecholamine responses are greater. However, the mechanisms for exercise limitation differ in patients with COPD and healthy subjects. Patients with COPD are often ventilatory-limited and thus may stop exercise before their circulatory and exercising muscle limits are met. At end-exercise at similar relative exercise intensities, we found that lactate levels were higher in healthy elderly patients than in patients with COPD.1 3 Similarly during maximal exercise, catecholamine levels did not go up as much in patients with COPD as in healthy control subjects.22 Thus, the results of comparing patients with COPD and healthy control subjects at the same relative exercise intensity are likely to be misleading. For this reason, we chose to compare the two groups at the same absolute workload. In addition, activities of daily living require a certain degree of effort to perform regardless of the patient’s capacity. At a given absolute workload, if patients with COPD develop greater fatigue of the exercising muscle, this would restrict their ability to perform tasks that require similar workloads.

We have not measured lactate and catecholamine levels in this study. It is quite possible that they and other humoral factors might be higher in the patients with COPD compared to the healthy control subjects. If so, this could influence our results. It is interesting to note that although acidosis can clearly promote the development of fatigue,23 we previously found no relationship in healthy elderly subjects between the degree of lactic acidosis and the degree of contractile fatigue induced by exercise.3

Was Exercise Matched Between Groups?
In this study, as outlined above, we planned to have our patients with COPD and healthy control subjects exercise at approximately the same absolute workload. Our patients with COPD appeared to exercise more inefficiently than did our control subjects, since at the same submaximal workload O2 was somewhat higher in the patients with COPD. To adjust for this, we asked our healthy control subjects to exercise at a slightly higher workload during constant-load exercise so that the average O2 during exercise was similar in the two groups.

In our study, exercise was sufficiently intense that O2 drifted upward over time in both the patients with COPD and the healthy control subjects (ie, steady-state conditions were not achieved). The amount of O2 increase from the end of the third minute of exercise (quasi-steady state) to the end of exercise was not significantly different between the patients with COPD and the healthy control subjects. O2 was well-matched in the two groups (50 ± 6% vs 48 ± 1% of predicted, respectively). Our healthy control subjects exercised for slightly longer than did the patients with COPD. Since our hypothesis was that patients with COPD would display more fatigue of the quadriceps muscle for the same O2 and exercise duration, we deliberately manipulated the exercise duration of the control group so that any difference would favor the patients with COPD. Despite this slight difference in exercise duration, the degree of fatigue elicited by exercise was significantly greater in the patients with COPD than in the control group supporting our hypothesis. If the groups had been perfectly matched, the difference we observed would only have been magnified.

Were Our Indexes of Fatigue Valid?
In this study, we used quadriceps TwQ as our index to quantify fatigue elicited by exercise. Ideally, fatigue should be assessed by obtaining a force-frequency curve before and after the potentially fatiguing task. Clearly, tetanic stimulation of the quadriceps muscle is not feasible in unanesthetized human subjects. Polkey and colleagues10 have shown that quadriceps TwQ can provide a reasonable estimate of the degree of contractile fatigue elicited by a potentially fatiguing task. TwQ can be measured after the muscle has been rested (ie, TwQu)1 10 or after an MVC (ie, TwQp).18 Some studies19 20 have suggested that the TwQp may provide a better estimate of the degree of fatigue elicited than the TwQu. In our study, the results were congruent. Differences between the patients with COPD and the healthy control subjects were observed with measurement of both the TwQu and the TwQp. However, the magnitude of the difference was less with the TwQp.

Potential Mechanisms
In patients with COPD, the quadriceps muscle is smaller and weaker compared to those of matched control subjects.5 In the absence of long-term steroid use, the reduction in strength is proportional to the degree of muscle atrophy.5 The quadriceps MVC in our patients with COPD was 32% lower than the MVC obtained in our matched control subjects. None of the patients had received any oral steroids in the 6 months previous to entering the study. Thus, it is quite likely that our patients had atrophy of their quadriceps muscle. When faced with the same absolute workload, a smaller, weaker muscle should fatigue more easily.

In one study,24 blood flow to the exercising legs appeared to plateau during exercise in some patients with COPD. In these patients, the total O2 continued to increase, implying that cardiac output also continued to increase.24 The authors speculated that the ventilatory muscles may compete with the exercising lower limb muscles for available oxygen, thus restricting the amount that blood flow can increase in the legs for a given increase in cardiac output. When blood flow to the legs plateaus, all of the additional blood flow produced by an increase in cardiac output must be going somewhere else, presumably the ventilatory muscles. This mechanism has been shown to be important in elite athletes,25 in whom the oxygen consumed by the respiratory muscles can be a significant fraction of total body O2 (13 to 15%),26 but it would not be as significant in sedentary healthy elderly subjects with modest peak exercise capacities like the healthy control subjects in this study in whom respiratory muscle O2 is a much smaller fraction of total body O2 (4 to 5%).26 If blood flow is in fact restricted to the legs in some patients with COPD, this could facilitate the development of fatigue.

Patients with COPD have a reduction in oxidative enzyme capacity,27 28 a reduction in muscle capillarity,29 and a shift in fiber type from type I to type II.30 31 Magnetic resonance spectroscopy studies also have suggested the presence of impaired oxidative metabolism in the exercising muscle in patients with COPD.32 These changes should all adversely affect the endurance properties of the muscle and increase its fatigability.

Clinical Implications
If patients develop contractile fatigue of their quadriceps muscles more easily than age-matched control subjects, this should impact on their activities of daily living. Two of our most severely affected patients with COPD exercised at 15 W for 1 and 4.5 min. Despite this very modest amount of exercise, significant contractile fatigue of the quadriceps muscle was observed. In contrast, we would expect healthy subjects to be able to exercise at this workload indefinitely without developing fatigue. The development of significant contractile fatigue of the quadriceps muscle will cause the muscle to generate less force for the same amount of neural activation, which could increase sensations of leg fatigue and discomfort,33 limiting subsequent exercise. Since low-frequency fatigue is long-lasting (ie, <= 24 h) the ability to perform exercise should remain impaired for a significant period of time following fatiguing exercise.19 34 The development of fatigue in the exercising muscle may also stimulate ventilation, thus increasing dyspnea.35

In conclusion, following cycle exercise for the same absolute O2 and duration, the quadriceps muscle fatigued to a significantly greater extent in patents with COPD than in age-matched healthy control subjects.


   Footnotes
 
Abbreviations: FIO2 = fraction of inspired oxygen; HR = heart rate; MVC = maximum voluntary contraction; MVV = maximum voluntary ventilation; TwQ = twitch force; TwQp = potentiated twitch force; TwQu = unpotentiated twitch force; E = minute ventilation; O2 = oxygen uptake; Wpeak = last workload a subject was able to complete 30 s of cycling

Received for publication February 12, 2002. Accepted for publication October 7, 2002.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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Exercise Induced Fatigue in COPD
Ketan K Dhatariya
Chest Online, 13 Apr 2003 [Full text]
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