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(Chest. 2002;121:1079-1084.)
© 2002 American College of Chest Physicians

Isokinetic Muscle Function in COPD*

Charles Haccoun, MD; Argyrios A. Smountas, BSc; William J. Gibbons, MD; Jean Bourbeau, MD and Larry C. Lands, MD, PhD

* From the Montreal Children’s Hospital-McGill University Health Centre (Drs. Haccoun and Lands, and Mr. Smountas), and Montreal Chest Institute-McGill University Health Centre (Drs. Gibbons and Bourbeau), Montreal, PQ, Canada.

Correspondence to: Larry C. Lands, MD, PhD, Division of Respiratory Medicine, Montreal Children’s Hospital, Room D-380, 2300 Tupper St, Montreal, PQ, H3H 1P3 Canada; e-mail: larry.lands{at}muhc.mcgill.ca


   Abstract
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 Abstract
Materials and Methods
 Results
 Discussion
 References
 
Aim: Exercise limitation in patients with COPD has been attributed to impaired ventilation and reduced skeletal muscle function. We have previously used a combination of FEV1 and leg muscle function (work achieved during a 30-s isokinetic sprint test) to predict progressive exercise capacity. However, the 30-s test may not be well tolerated in patients with advanced lung disease. We studied the relationship between progressive exercise capacity, FEV1, and isokinetic work in patients with COPD and in healthy control subjects to assess whether the work accomplished at time intervals of < 30 s could also be used to predict progressive maximal exercise capacity (Wmax).

Methods: Twenty-seven patients with COPD and 29 control subjects underwent anthropometric measures, spirometry, progressive cycle ergometry, and 30-s isokinetic cycling.

Results: There was no significant difference for weight, height, or body mass index between the groups. The COPD group was slightly older and had a significantly lower FEV1 than control subjects. They also had a lower Wmax (56 ± 28.3 W vs 141.9 ± 46.7 W) and isokinetic work accomplished over 10 s (W10), over 15 s (W15), over 20 s (W20), over 25 s (W25), and over 30 s (W30). Wmax correlated in both patients with COPD and in control subjects with W10, W15, W20, W25, W30, and FEV1. Combining FEV1 and isokinetic work (W10, W15, W20, W25, or W30) in a two-factor model to predict Wmax, the coefficients of determination (r2) for patients with COPD were 0.57, 0.57, 0.58, 0.59, and 0.58, and for control subjects were 0.69, 0.69, 0.71, 0.71, and 0.73, respectively. Wmax correlated with weight only in control subjects.

Conclusions: Both ventilatory function and leg muscle function contribute to exercise limitation, and a 20-s isokinetic test can be utilized to assess leg function in patients with COPD.

Key Words: COPD • exercise testing • skeletal muscle

Exercise limitation in patients with COPD results from multiple factors. It has been recognized that ventilatory limitation, particularly expiratory flow limitation, may be present in some patients. Expiratory flow limitation can lead to dynamic hyperinflation and contribute to increased work of breathing and dyspnea.1 2 While ventilatory limitation plays a significant role in the exercise limitation seen in patients with COPD, other factors such as abnormal skeletal muscle function are also involved.

The importance of peripheral muscle impairment in exercise limitation has been noted.3 4 5 Leg fatigue is often a major reason cited by these patients for stopping during maximum exercise testing.6 As this muscular impairment has the potential to improve with rehabilitation,7 8 it is useful to characterize peripheral skeletal muscle function and its relationship to exercise ability in this population. This information could then be used to guide rehabilitation strategies.

We have previously performed such an analysis on adolescents and young adults with cystic fibrosis and healthy subjects of similar age. We found that maximal exercise ability, as measured during progressive exercise testing on a cycle ergometer, could be predicted using a combination of lung function as characterized by FEV1 and leg muscle function as measured during a 30-s isokinetic cycle sprint.9 Furthermore, the decrease in isokinetic leg muscle power and leg work capacity in patients with cystic fibrosis could be attributed to their reduced muscle mass.9 In the present study, we performed a similar investigation of the relationship between exercise capacity and leg muscle function in older patients with COPD entering a pulmonary rehabilitation program and healthy adults in order to determine if such a method of characterizing exercise ability could be used. We also assessed whether a shorter measurement of isokinetic work ability, which may be more readily tolerated, could be used to characterize exercise tolerance in patients with COPD. Lastly, we examined if a two-variable model combining isokinetic work and FEV1 could be used in healthy older subjects and in patients with COPD, as in patients with cystic fibrosis to predict maximal exercise capacity (Wmax).


   Materials and Methods
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 Abstract
 Materials and Methods
Results
 Discussion
 References
 
Subjects
Twenty-seven patients with COPD and 29 healthy control subjects were studied. The patients were referred into the ambulatory pulmonary exercise program at the Montreal Chest Institute by their treating physician. All patients had received a diagnosis of COPD, defined as obstructive lung disease that was mostly irreversible. Patients were not excluded if they required supplemental oxygen (4 of 27 patients). The healthy control subjects were enrolled in an investigation into leg function and exercise ability. These subjects were between 50 years and 70 years of age, were free of any history of cardiac or recurrent lung disease, and had no knee, leg, or joint discomfort that would hinder cycling. Testing in the patients with COPD was part of the routine initial assessment for rehabilitation. The study in healthy subjects had the approval of the local ethics committee, and signed informed consent was obtained prior to commencement of investigations.

Procedures
As part of the initial assessment for rehabilitation, patients had their height measured without shoes on a portable stadiometer (Harpendem model; Holtain, LTD; Crymych, UK) and were weighed on an electronic scale (model UMC600; Lancaster Scales; Brantford, ON, Canada). They underwent expiratory spirometry (model 2130; SensorMedics; Yorba Linda, CA), and values were expressed in both absolute terms and as percentage of predicted.10 They then underwent a symptom-limited progressive exercise test on an electronically braked cycle ergometer (Ergometrics 800s; SensorMedics) with 1-min increments of 10 W. During the test, the patients were monitored with pulse oximetry, three-lead ECG, and BP measurements every minute. Patients normally receiving oxygen received a fraction of inspired oxygen of 28% during exercise testing. Tests were halted when the patient could no longer maintain a pedaling speed of 60 revolutions per minute, or had exercise-induced hypotension or arrhythmias. Patients breathed through a mouthpiece, and gas exchange was measured using 30-s averages of minute ventilation, tidal volume, breathing frequency, and mixed expiratory gas concentrations. From this test, the maximal workload achieved (in watts) was recorded and compared to predicted values.11

Within 2 weeks of this testing, all patients underwent isokinetic cycle testing for a clinical assessment of leg function. For this test, our previously described isokinetic cycle was used.12 Isokinetic cycling fixes the speed of pedaling, and the force on the flywheel axle strut is measured. From this torque, power and work for each revolution are calculated. If patients received ambulatory oxygen, this was used during the test at the flow prescribed by their treating physician for exertion. Patients made a 10-s all-out effort at 60 revolutions per minute to measure peak power (in watts). After a rest period of at least 2 min, patients then made a 30-s effort at 100 revolutions per minute to record 30-s work output (in kilojoules [kJ]). From the 30-s data, work for shorter time intervals was derived. Peak power and 30-s work capacity were compared to predicted values.12 Three of the 27 patients with COPD were unable to complete the 30-s sprints, but their values were recorded as the total work completed during the 30-s period.

The healthy subjects underwent the same anthropometric measures as the patients with COPD. Spirometry was performed (model 42; Vitalograph; Buckingham, UK) and expressed as both absolute values and as percentage of predicted. Symptom-limited maximal exercise was performed on an electronically braked cycle ergometer (Corival 300; Lode; Groningen, Netherlands) with 1-min increments of 16.35 W. Subjects were monitored using three-lead ECG and pulse oximetry. Subjects breathed through a mouthpiece using a one-way valve as previously described.13 Using a dry gas meter on the inspiratory line, and a mixing chamber adjusted to the vital capacity, mixed expired gases were analyzed by mass spectrometry (MGA-1100; Marquette; Milwaukee, WI). The maximal achievable workload was recorded in watts. After a rest period of 45 to 60 min, the subjects underwent isokinetic cycling as described above.

Data Analysis
Values were expressed as mean ± SD. Groups were compared using unpaired t testing, and proportions were compared with {chi}2 testing. Relationships between variables were assessed using the Pearson correlation coefficient (r) and forward stepwise linear regression analysis. A simple linear regression analysis was used to describe the relationship of Wmax and isokinetic work or FEV1 by the following expression: Wmax = a + bx, where a is the y intercept, b is the slope of the line, and x is isokinetic work at a given time interval or FEV1. A forward stepwise multiple linear regression analysis was performed to describe the relationship between Wmax, isokinetic work, and FEV1, using the following expression: Wmax = a + b1x1 + b2x2, where x1 is isokinetic work and x2 is FEV1. The adjusted coefficient of determination (r2) for the multiple linear regression equation was used an expression of the degree to which the variability in the dependent variable (Wmax) could be explained by the combination of the independent variables (isokinetic work and FEV1). A p value < 0.05 was considered as significant, and all analyses were performed using Statistica software (version 5.5; Statsoft; Tulsa, OK).


   Results
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 Abstract
 Materials and Methods
 Results
Discussion
 References
 
Patients with COPD were slightly older than control subjects, but there were no differences in height, weight, or body mass index (BMI) [Table 1 ]. There was a similar proportion of male subjects in both groups. Compared to the healthy subjects, the COPD group had a marked limitation of airflow with an FEV1 of 0.93 L (34.8% predicted) and a very low Wmax of 56 W (44.9% predicted). All measurements of isokinetic work accomplished over 10 s (W10), over 15 s (W15), over 20 s (W20), over 25 s (W25), and over 30 s (W30) were significantly lower than in the control group.


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  		Table 1. Comparison of Anthropometrics, Pulmonary Function, and Exercise Performance for Both Groups*

 
Univariate correlations for both groups revealed that Wmax correlated with all isokinetic work measurements as well as with FEV1 (Table 2 , Fig 1 ). For each group, more work was done during the full 30-s time interval than the shorter time intervals (Table 1) . This can account for the greater slopes (b) for shorter time intervals. This difference in slopes from the 30-s time interval reached statistical significance for time intervals < 20 s for the control group. In all cases, the intercept (a) for isokinetic work was significantly different from 0. The intercept for the FEV1 equation was not significantly different from 0 for either group. There was a significant correlation between FEV1 and isokinetic work of any time interval for the control group, but not for the COPD group (data not shown). Correlation between W30 and shorter duration work was always strong, with r values of between 0.96 and 1.0 for both patients with COPD and for control subjects (Table 3 ), suggesting that shorter durations of isokinetic exercise are accurate reflections of a 30-s effort.


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  		Table 2. Regression Equations and Correlation Coefficients Between Wmax and Isokinetic Work and FEV1

 


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  		Figure 1. Top, a: Wmax vs FEV1 for both groups. Bottom, b: Wmax vs W30 for both groups. Solid circles represent the COPD group; the control group is represented by open squares.

 

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  		Table 3. Correlation Between W30 and Shorter Durations of Isokinetic Work

 
The combination of FEV1 and isokinetic work of differing duration explained most of the variability (expressed as the coefficient of determination, or r2) in Wmax for both COPD patients and healthy control subjects (Table 4 ). In all cases, the intercept (a) was not significantly different from 0, while the coefficients (b1 and b2) were significantly different from 0, even though there was a significant correlation between FEV1 and isokinetic work for the control group.


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  		Table 4. Multiple Regression Analysis Using FEV1 and Isokinetic Work of Varying Durations as Predictors for Wmax

 
For the control subjects, Wmax correlated with weight (r = 0.52, p < 0 0.05). In patients with COPD, there was no correlation between Wmax and weight (weight r = 0.04, p > 0.05). Furthermore, isokinetic work of various duration correlated with weight in control subjects but not in patients with COPD (Table 5 ). However, there was a weak correlation between peak power and weight in patients with COPD. There was no correlation between exercise capacity or isokinetic work capacity with BMI in either patients with COPD or in healthy control subjects.


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  		Table 5. Relationships Between Weight and Peak Torque and Weight and Isokinetic Work*

 

   Discussion
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 Abstract
 Materials and Methods
 Results
 Discussion
References
 
Wmax is reduced in patients with significant airflow limitation. The two-factor model presented here demonstrates that this capacity can be determined by a combination of ventilatory capacity (FEV1) and skeletal muscle function, which can be characterized by measuring isokinetic work of various lengths of time between 10 s and 30 s. This model holds for both patients with COPD and for control subjects, although the correlation is stronger in healthy subjects.

Using smaller increments during the progressive exercise test for the patients with COPD may have underestimated the Wmax for this group.14 However, this does not detract from our finding that Wmax can be predicted from a two-variable model using lung function and skeletal muscle function.

Eltayara and colleagues15 showed that expiratory flow limitation is a major cause of exercise intolerance in patients with COPD that would not be fully reflected in FEV1 values. The variability in flow limitation may account for some of the increased variability seen in patients with COPD when predicting Wmax. It will be interesting to evaluate the impact of flow limitation on exercise capacity in upcoming studies.

These results are similar to what we have previously demonstrated in healthy adolescents and young adults and in patients with cystic fibrosis.9 It is interesting to note that in patients with cystic fibrosis and in both younger and older healthy subjects, W30 was largely a function of body mass,9 while in the patients with COPD, there was no correlation with weight. Although we did not measure lean body mass or muscle cross-sectional area in the subjects tested in the current study, the fact that the BMI was normal and similar in both the control subjects and the patients with COPD may suggest near-normal muscle mass. While a normal BMI might not always signify a normal muscle mass in patients with COPD,16 the fact that the patients with COPD participating in this study had lung function and Wmax similar to a previously studied17 group of patients with COPD with normal nutritional status suggests that our patients probably did not have very abnormal muscle mass, although we lack direct evidence of this. If our patients with COPD have, as we believe, near-normal muscle mass, the lack of correlation between W30 and weight seen in healthy control subjects and in patients with cystic fibrosis suggest that the muscle in patients with COPD might be dysfunctional.

Several studies have found abnormalities in lower-limb muscle of patients with COPD that have been postulated to be related to a variety of factors, including hypoxemia,18 19 malnutrition,20 age,21 disuse leading to deconditioning,22 altered electrolyte concentrations,23 24 impaired enzyme activity,25 26 27 reduced oxidative ability,28 29 and steroid-induced myopathy.30 While it would be interesting to know if regular steroid use in our patients with COPD contributed to the observed dysfunction, we do not have data on the dose and duration of corticosteroid therapy.

In contrast, a recent study published by Richardson and colleagues31 suggests that there may be a systemic cause, possibly due to vascular redistribution causing impaired oxygen delivery, for the apparent muscle dysfunction in patients with COPD independent of the respiratory system. They also suggest that the skeletal muscle in patients with COPD has a significant metabolic reserve and normal intrinsic muscle function. Further work with subjects receiving supplemental oxygen or helium-oxygen gas mixtures while performing short isokinetic sprints might help to establish the relative importance of the muscle metabolic reserve vs oxygen delivery in patients with COPD.

The ability to define exercise ability in terms of ventilatory and peripheral skeletal muscular factors might allow for rehabilitation to be targeted to those areas that can be improved on. Work in patients with coronary heart disease has shown that in these patients, strength and aerobic training have complementary effects on peripheral muscle function and exercise ability.32 Simpson and colleagues33 reported that 8 weeks of strength training produces an improvement in muscle strength and in submaximal exercise tolerance in patients with COPD. Clark and colleagues3 demonstrated a significant improvement in muscle function and whole-body exercise ability after a 12-week program of weight training. In contrast, Bernard and his colleagues8 showed a greater increase in muscle strength and mass but did not find any difference in exercise capacity as measured by the 6-min walk test in patients with more severe COPD after a combination of exercise and aerobic training when compared with aerobic training alone. These studies, while appearing to demonstrate different responses to strength training in patients with COPD, studied very different populations and used different end points to define change in exercise tolerance. It may be that submaximal exercise endurance as measured by Simpson and colleagues33 is a better marker for improvements in functional ability than endurance at maximal exercise levels. Identifying those patients who have greater reductions in strength than endurance will allow for more emphasis to be placed and intervention targeted at increasing strength, such as diet, growth hormone, anabolic steroids,34 and strength training.

While most patients with COPD can tolerate the 30-s test, it is an uncomfortable experience for most of the them. Shorter sprints would be better tolerated, and our results indicate that 20-s sprints could be used instead of the longer sprint. A 20-s sprint provides qualitatively similar information to the 30-s test, and when combined with FEV1 can predict progressive exercise capacity. The response of isokinetic muscle function during the course of rehabilitation may provide useful information on the impact of therapeutic interventions.


   Footnotes
 
Abbreviations: BMI = body mass index; kJ = kilojoule; Wmax = maximal exercise capacity; W10 = isokinetic work accomplished over 10 s; W15 = isokinetic work accomplished over 15 s; W20 = isokinetic work accomplished over 20 s; W25 = isokinetic work accomplished over 25 s; W30 = isokinetic work accomplished over 30 s

Dr. Lands is a chercheur-clinicien of the Fonds de Recherche en Santé du Québec.

Received for publication February 12, 2001. Accepted for publication October 3, 2001.


   References
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 Abstract
 Materials and Methods
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