Endurance training is regarded as a fundamentally important component of any pulmonary rehabilitation program. Evidence-based guidelines for pulmonary rehabilitation, published jointly by the American College of Chest Physicians (ACCP) and the American Association for Cardiovascular and Pulmonary Rehabilitation (AACVPR), identify only two modalities of treatment that have, to date, been shown by well-designed, prospective, placebo-controlled, clinical trials to be of value in pulmonary rehabilitation (38). These modalities are (a) endurance training using large muscle groups (i.e., aerobic leg exercise), and (b) strategies to assist with the mastery of dyspnea. Interestingly, aerobic exercise per se might be one of the most efficacious and time-efficient means of achieving mastery of dyspnea (6,16). A focused and well-designed aerobic exercise prescription is especially important when one considers that patients spend a limited amount of time attending pulmonary rehabilitation programs. On the basis of existing evidence, one could reasonably argue that most of that time should be spent undertaking supervised aerobic exercise.
Several issues are important when considering endurance training and aerobic exercise prescription for patients with chronic pulmonary disease: 1) At what stage in the progression of chronic pulmonary disease should endurance training (i.e., pulmonary rehabilitation) be implemented? 2) What is the potential for improvement with endurance training? 3) How should the aerobic exercise prescription be derived? 4) How do specific exercise limitations influence the aerobic exercise prescription? 5) What should be regarded as a successful (i.e., clinically meaningful) response to endurance training and how should this be measured? This article addresses each of these issues and offers practical recommendations. At the same time, it is important to recognize that most of our experience derives from patients with chronic obstructive pulmonary disease (COPD).
RECOMMENDED STAGE FOR THE IMPLEMENTATION OF ENDURANCE TRAINING (PULMONARY REHABILITATION)
Chronic pulmonary disease often results in a progressive decline in exercise capacity because of the vicious cycle of physical inactivity and deconditioning. Inevitably, these effects are superimposed on the natural decline in aerobic capacity (V̇O2max), lean body mass, and muscle strength that are expected with aging (32). As baseline exercise capacity declines, so does the potential for improvement in terms of absolute work capacity, if this is assumed to be a fixed percentage of the baseline function. This principle is illustrated in Figure 1, which assumes that endurance training is capable of improving some measure of functional capacity by 20%. The resulting gain in absolute terms declines as the subject ages. This gain could be expressed in terms of oxygen uptake, which relates directly to external work rate. In other words, as an individual ages, the potential gain from exercise training declines in terms of ability to perform additional external work.
In COPD, decline in physical function is accompanied by a steady decline of airway function (23). Hence, comparison of the forced expiratory volume in 1 s (FEV1) with its predicted value offers an opportunity to stage this disease. Three schemata have been proposed for staging COPD as shown in Table 1 (3,40,43). The American Thoracic Society (ATS) staging (3) proposes that the disease has reached a moderate as opposed to mild stage once FEV1 falls below 50% of its predicted value. The British Thoracic Society (BTS) (43) has similar proposals but categorizes moderate disease as less than 60% of predicted FEV1. Schemata such as these tend to be arbitrary. However, the BTS scheme deserves special attention because the categories were derived from patient surveys within the National Health Service. Those with mild disease were unlikely to be known to their primary care physicians as having significant if any pulmonary disease. Those with moderate disease were followed by their general practitioners. Those with severe disease were known to pulmonary specialists and often had histories of hospitalization for exacerbations of their disease. The real value in these proposed staging schemata is that they lend themselves as a framework on which to build treatment guidelines. The ATS recommends that patients with moderate disease should be evaluated by a pulmonary specialist and considered for pulmonary rehabilitation. British treatment guidelines are similar.
Thus, there is a consensus that patients with COPD should be referred for pulmonary rehabilitation once their FEV1 falls below 50–60% of its predicted value. This equates to the transition from mild to moderate disease and corresponds with the time when a patient should be first referred to a pulmonary specialist. Current experience in the United States would suggest that patients typically referred to pulmonary rehabilitation programs have FEV1 about 40% of the predicted value (11). Note that this equates to the transition from moderate to severe disease and will often correspond with the time when patients are first admitted to hospital with an exacerbation of their disease. Unfortunately, these patients are referred to pulmonary rehabilitation too late. On the basis of international guidelines and the likelihood of a better response to aerobic and other forms of exercise training, patients would benefit from earlier referral to pulmonary rehabilitation.
POTENTIAL FOR IMPROVEMENT WITH ENDURANCE TRAINING
Aerobic capacity or maximum oxygen uptake (V̇O2max) can be predicted for a given individual on the basis of age, gender, height, and body weight (17). Aerobic capacity is also influenced by physical fitness, and the conventional belief is that V̇O2max can be elevated by as much as 20% with several months of structured aerobic exercise training as illustrated in Figure 2. Åstrand and Rodahl (5) also described the “percentage of maximum aerobic power which may be taxed during prolonged work.” Nowadays, this entity is recognized as the exercise intensity above which a sustained increase in blood lactate cannot be prevented, and is commonly known as the lactate or metabolic threshold (V̇O2θ). In sedentary normal subjects V̇O2θ occurs at approximately 50% of V̇O2max. Interestingly, V̇O2θ may be elevated by as much as 100% of its sedentary value by successful aerobic training, according to Åstrand and Rodahl (5), thus increasing from 50% of the sedentary V̇O2max to as high as 80% of the trained V̇O2max (Fig. 2). V̇O2θ is reduced in deconditioning but is unlikely to fall below 40% of V̇O2max except in disease (18,46). A deconditioned individual thus has potential for significantly greater improvement in V̇O2max and V̇O2θ with exercise training.
There has been an evolving series of recommendations for the maintenance of physical fitness in normal human subjects. Perhaps those recommendations receiving greatest prominence are included in the report of the U.S. Surgeon General (44). The 1996 report recommends aerobic exercise of moderate intensity for 30 min·d−1 on most days of the week. The American College of Sports Medicine (2) recommends well-rounded exercise for 20–60 min·d−1 on 3–5 d·wk−1 at an intensity corresponding to 55–95% of maximum heart rate or 40–85% of V̇O2 reserve. The ACSM Position Statement further emphasizes the importance of the “overload principle,” and states that exercise of less than 10 min duration, on less than 2 d·wk−1 or at less than 40% of V̇O2 reserve is ineffective. Although these recommendations cannot necessarily be applied directly to the debilitated patient, they cannot be ignored when designing rehabilitation programs for patients with chronic pulmonary diseases.
Significant increases in exercise capacity with pulmonary rehabilitation have been shown in a number of controlled studies (4). A meta-analysis of 11 studies showed a small but positive effect size for exercise capacity with training (28). However, even among controlled studies there is marked inconsistency in the methods of endurance training, and it is questionable whether many of these studies used an optimal exercise prescription.
DERIVATION OF THE AEROBIC EXERCISE PRESCRIPTION IN CHRONIC PULMONARY DISEASE
Mode of exercise.
The evidence-based guidelines for pulmonary rehabilitation indicate scientific support in favor of aerobic exercise training using the large muscle groups of the legs (38). Arm endurance training is less effective than leg endurance training in improving functional capacity (29). Furthermore, when time for supervised endurance training is limited, it is clearly advantageous to focus on leg exercise. In 1995, Bickford et al. (8) reported the results of a National Pulmonary Rehabilitation Survey including 283 programs from 44 states. The mode of exercise used for endurance training was a treadmill ergometer in 37%, a cycle ergometer in 23%, and both in 40% of programs. Treadmill exercise is usually preferred by patients and rehabilitation therapists because of the readiness with which patients adapt to treadmill exercise and with which it translates to activities of daily living. Cycle ergometry can be used as a means of varying the exercise mode, provided intensity criteria are matched between the treadmill and cycle (see below). In some cases, such as patients with arthritis, joint deformities, or morbid obesity, the cycle ergometer will be preferred because of its low impact on the musculoskeletal system. Cycle ergometry might also be chosen if therapists find difficulty with monitoring, such as pulse oximetry or electrocardiography during treadmill exercise.
The majority of pulmonary rehabilitation programs seem to adhere to evidence-based guidelines in terms of exercise mode, although many programs spend additional time on arm endurance training that could be better used in prolonging leg endurance training or adding strength training as a component of the program.
Frequency and duration.
Experience with normal subjects suggests that, in order to be effective, endurance exercise should be performed for about 30 min·d−1 on 3–5 d·wk−1 (2,44). Furthermore, the ACSM opines that 2 d·wk−1 is insufficient (2). Similar guidelines are likely to be applicable in chronic pulmonary disease. Certainly, the greater the frequency and duration of endurance training, the better the outcome. The crucial question then becomes: What is the minimum participation required to produce a measurable and clinically meaningful response? The answer to this question is not precisely known; however, since pulmonary rehabilitation programs often struggle to produce measurable and clinically meaningful outcomes, it is better to err on the side of more frequent supervised endurance training. A recent randomized study of 24 patients with COPD showed an increase in 6-min walking distance of only 29 m after 8 wk of twice-weekly endurance training and led the authors to conclude that twice-weekly training was insufficient (39).
In summary, pulmonary rehabilitation should aim for an accumulation of 30 min of aerobic exercise on at least 3 d·wk−1 for at least 6–8 wk. The National Pulmonary Rehabilitation Survey showed a mean frequency of attendance of 2.5 d·wk−1, with a range from 1–7 days. Thus, many pulmonary rehabilitation programs offer a suboptimal frequency of supervised endurance training.
Perhaps the most contentious of all issues regarding exercise prescription in chronic pulmonary disease is the question of an appropriate exercise intensity. Several studies have indicated, as with normal subjects, that higher exercise intensity results in better training responses (10,35). In the study reported by Casaburi et al. (10), inpatients trained on cycle ergometers for 8 wk either at lower (30 W·min−1) or higher (71 W·min−1) intensity. The duration of the training sessions was adjusted between the two groups so that all subjects achieved the same accumulated work in training. Figure 3 shows that the group training at higher intensity demonstrated greater physiological training responses in terms of reduced lactate, minute ventilation, heart rate, and oxygen uptake for an identical constant work rate exercise test after training as compared with before training. Despite these and similar findings, it has never been proven that there is a threshold exercise intensity above which it is necessary to train in order to obtain benefit. By contrast, low-intensity training induces worthwhile training responses both in asthmatic subjects (13) and in those with COPD (14). Notwithstanding this knowledge, in order to obtain the most favorable response, patients in pulmonary rehabilitation should be encouraged to train at as high an intensity as tolerated with due consideration for various safety aspects (see below). The obvious concern is that unsupervised training is less likely to achieve and sustain the exercise intensity required to elicit a clinically meaningful improvement in functional capacity (34).
Determination of the optimal exercise intensity is the essence of the aerobic exercise prescription. An arbitrary approach (i.e., guessing the exercise intensity and making empirical adjustments) is unlikely to be the most effective strategy. However, unfortunately this is how many pulmonary rehabilitation programs operate. In order to advance the discipline of pulmonary rehabilitation and in order to optimize outcomes, the aerobic exercise prescription needs a firmer scientific basis.
Three important criteria should be considered in defining exercise intensity, as shown in Table 2. First, exercise intensity should have a “target” that represents the minimum intensity needed to produce a clinically meaningful response. This does not imply that exercise intensities below the target are ineffective but rather that any such effect would be insufficient to translate into clinical benefit. Second, exercise intensity should have a “range,” the upper limit of which is typically defined by patient acceptance and safety considerations. Third, an effective exercise prescription must take into account “progression,” necessitating careful adjustment of the exercise prescription to maintain the desired intensity in the presence of training adaptations. Again, it is self-evident that in order to attain these goals with any degree of precision requires some physiological measurement or monitoring.
There are several candidate variables with which to determine and adjust exercise intensity. These include external work rate (Ẇ), oxygen uptake (V̇O2), heart rate (fC), and rating of perceived exertion (RPE). Patients with COPD are known to be able to achieve greater than 80% of their initial maximum work rate as a training intensity (35). Most likely this is because these patients do not have conventional cardiovascular limitation and many do not have significant lactate accumulation (12). The diverse nature of limitation in COPD is likely to make it more difficult to predict what percentage of achieved maximum work rate constitutes an appropriate exercise prescription. Similar considerations are likely to apply to a percentage of measured V̇O2max.
The traditional and probably the commonest approach to aerobic exercise prescription for normal subjects uses a percentage of predicted maximum heart rate or heart rate range calculated from measured or predicted maximum heart rate (1). Again, in patients with chronic pulmonary disease, measured heart rate often does not bear the same relationship to exercise intensity that one expects with normal subjects. Furthermore, predictions of maximum heart rate are subject to errors. The standard deviation for measured maximum heart rate in cohorts of subjects of the same age is recognized to be 10 beats·min−1 (20). Effectively, this means that 5% of all normal subjects will have maximum heart rates less than 20 beats·min−1 below or greater than 20 beats·min−1 above the value predicted using a formula such as: fCmax = 220 − age. Clearly, this approach is susceptible to substantial errors in the calculation of exercise intensity.
One way around these difficulties is to use RPE rather than heart rate as a measure of exercise intensity. When using the RPE scale, it is helpful to establish some idea of the relationship between RPE and heart rate for a given individual. For a given subject in pulmonary rehabilitation, this can be achieved simply by making paired observations of heart rate and RPE during submaximal exercise. Also, the RPE scale (range, 6–20) is preferred to the CR-10 (range, 1–10) scale for reasons expounded by Gunnar Borg in his book about these scales (9) :
“The Borg RPE scale is the most commonly used scale for tests of perceived exertion. One main advantage of the RPE scale is that the given ratings grow linearly with exercise intensity, HR and VO2. Given ratings are then easy to compare with common measurements of exercise intensity.”
“A drawback of the Borg CR10 scale is that the number range, a bit smaller than that of the Borg RPE scale, is a bit too small. Also, for ratings of perceived exertion the Borg CR10 scale does not give the simple linear relationship to exercise intensity that the RPE scale does.”
Regular use of the RPE scale in the manner Borg intended leads to an appreciation of the appropriateness of RPE compared with the cardiovascular response to exercise. Our laboratory recognizes that a maximal cardiovascular response is normally associated with an RPE of 16–18, whereas the metabolic threshold usually occurs at an RPE of 12–14 (17). An RPE of 19 or 20 is unusual and, in the absence of cardiovascular limitation, most likely indicative of abnormal symptom perception. By similar reasoning, an RPE of 15 or greater is probably abnormal in the absence of evidence of lactic acidosis. When RPE is used to determine the aerobic exercise prescription for pulmonary rehabilitation, the desired threshold is likely to be 12 and the upper limit 16.
Many rehabilitation programs use a rating of breathlessness rather than perceived exertion as an intensity target for patients with chronic pulmonary disease. This approach seems understandable on the basis of the fact that breathlessness is often the dominant limiting factor in these patients. Two studies have examined the reliability of dyspnea ratings for attaining a chosen level of oxygen uptake in COPD patients (25,31). This approach seemed more accurate at higher exercise intensities and comparable with using target heart rate. Nevertheless, reliance on breathlessness alone may have pitfalls and not allow some patients to achieve a training intensity necessary for cardiovascular reconditioning. Breathlessness is a highly variable symptom between subjects and might not correlate with any physiological parameters of the exercise response. Alternatively, breathlessness might be loosely associated with the proportion of ventilatory capacity used for exercise, and although this might be an important limiting factor, it does not necessarily indicate a desirable training intensity in terms of the cardiovascular response. To appreciate these points, consider the patient who is highly fearful and symptomatic at very low exercise intensity. This type of patient requires therapeutic approaches to reduce breathlessness before being able to exercise at an intensity high enough to achieve a true reconditioning response.
APPROACH TO AEROBIC EXERCISE PRESCRIPTION DERIVED FROM THE REFERENCE VALUE FOR V̇O2max
Given the uncertainties regarding the relationship between achieved Ẇ and exercise intensity, the diverse factors that influence measured V̇O2 and the inaccuracy of predicting fCmax, a novel approach to aerobic exercise prescription might be considered. A reasonably dependable prediction concerning exercise performance for any given individual is the reference value for V̇O2max determined on the basis of age, gender, height, and body weight. Also, in sedentary normal subjects V̇O2θ approximates 50% of the reference value for V̇O2max. Furthermore, there is evidence to support the concept that the lower limit of normality for V̇O2θ attributable to deconditioning is 40% of the reference value for V̇O2max (18,46). These parameters can be used as the framework for the development of an aerobic exercise prescription. Figure 4 illustrates the rationale. First, a reference value for V̇O2max is calculated on the basis of age, gender, height, and body weight using whatever prediction equation is deemed best matched to the type of subject. Second, 40% of the reference value for V̇O2max is calculated as the initial “target intensity.” This target intensity can be converted to a target work rate on any given ergometer provided that the relationship between V̇O2 and work rate is known for that ergometer (Fig. 4 and Appendix A). Similarly, the target intensity can be converted to a target heart rate, provided the relationship between heart rate and V̇O2 is known for that particular individual exercising on a given ergometer. In practice, these relationships are easy to determine using a submaximal, incremental exercise testing with noninvasive gas exchange measurements. Finally, target work rate or target heart rate can be translated into a rating of perceived exertion, provided the relationships between these variables have been established for a given individual and a particular ergometer (Fig. 4). This approach uses the expected interrelationships between V̇O2, Ẇ, fC, and RPE to determine and adjust the target exercise intensity. The desired range of exercise intensity (i.e., its upper limit) must be carefully assessed on the basis of safety considerations. However, once this has been decided, Figure 4 can be used in a similar way as described above to obtain an intensity range in terms of Ẇ, fC, or RPE. Simple forms of exercise testing have a useful role in this approach to exercise prescription in that they help establish the relationships between the important intensity variables. These tests need not be maximal exercise tests.
INFLUENCE OF SPECIFIC EXERCISE LIMITATIONS ON AEROBIC EXERCISE PRESCRIPTION: ROLE OF MAXIMAL EXERCISE TESTING
An aerobic exercise prescription needs to be derived from an intensity target necessary to obtain a clinically meaningful change and also from an intensity range that allows the therapist to push for optimal outcome. The intensity range or upper limit is primarily influenced by patient tolerance and safety considerations. In this aspect of exercise prescription, exercise testing has a definite role in identifying specific exercise limitations and also thresholds that have a bearing on exercise adherence and safety. Maximal, incremental exercise testing with certain peripheral measurements can help identify specific limitations to exercise in patients with chronic pulmonary disease. The important specific limitations are listed in Table 3 along with the ways in which their identification influences the exercise prescription. The identification of one of these thresholds usually has important bearing on patient safety and whether or not a patient requires monitoring during exercise training. Also, the existence of certain thresholds might influence patient tolerance of a particular training intensity and thereby affect adherence to the exercise prescription.
IDENTIFICATION OF CLINICALLY MEANINGFUL RESPONSES TO ENDURANCE TRAINING: ROLE OF FUNCTIONAL AND SUBMAXIMAL EXERCISE TESTING
In order to be successful, endurance training must achieve a clinically meaningful difference that can be measured and documented objectively. This necessitates repeated exercise testing using methods that are deemed appropriate for this purpose. Unarguably, the most meaningful improvements from the perspective of the patient relate to functional exercise capacity and quality of life. Therefore, the methods of initial evaluation and reassessment used in pulmonary rehabilitation should focus on these parameters. For this specific purpose, functional exercise testing is preferred to formal clinical exercise testing because of its simplicity and translation to activities of daily living. The 6-min walking test has become a standard test, and is reproducible once a learning effect has been overcome (15,27) (Table 4). Furthermore, reference values have now been published (22). A simplified calculation for normal 6-min walking distance is as follows:MATHwhere dW6 is 6-min walking distance in meters and age is in years (17).
The shuttle walking test offers an alternative means of functional assessment with incremental properties that will allow estimation of V̇O2max (30). In patients with COPD, the 10-m shuttle test has been shown to correlate with 6-min walking distance (41) and V̇O2max (42). This test is also sensitive to changes induced by endurance training (37).
Various instruments exist for assessing quality of life. Their evaluation is beyond the scope of this article. However, in the assessment of patients with chronic pulmonary disease, it is usually recommended that a general, health-related, quality-of-life instrument is used in conjunction with a disease-specific instrument. Examples of general, health-related, quality-of-life instruments include the Sickness Impact profile (7) and the Medical Outcomes Trust SF-36 (45). Examples of pulmonary disease-specific questionnaires include the Chronic Respiratory Questionnaire (CRQ) (24) and the St George’s Respiratory Questionnaire (SGRQ) (26).
Attempts have been made to determine a clinically meaningful difference using some of these measures of assessment. Redelmeier et al. (36) studied 112 patients with stable COPD and found that a change in 6-min walking distance of 54 m was necessary for patients to subjectively notice a difference. Lacasse et al. (28) performed a meta-analysis of pulmonary rehabilitation studies with an analysis determined on the basis of effect size. These investigators demonstrated an average increase in 6-min walking distance of 56 m that was associated with perceived benefit by the patients in terms of dyspnea and mastery. The same investigators assigned a clinically meaningful difference of 0.5 to the dyspnea and mastery categories of the CRQ. Meanwhile, a difference in score of 4 is regarded as a clinically meaningful difference with the SGRQ (personal communication). These clinically meaningful differences are summarized in Table 4.
A clinically meaningful difference (CMD) is rarely achieved within a short time frame; therefore, when determining an aerobic exercise prescription, due consideration must be given to program length and progression (i.e., adjustment of exercise intensity in the face of adaptations to training). Experience suggests that older normal subjects over the age of 50 yr can achieve a 10% increase in function after about 4 wk of endurance training, whereas those over the age of 60 yr would achieve the same 10% increase after about 5 wk. In a longitudinal study of structured exercise training in COPD patients, Casaburi et al. (10) found that a target work rate of 80% of initial Wmax was achieved after about 12 wk (Fig. 5). Progression needs to be carefully considered with regards to the duration of the exercise prescription. The recommended duration for a single endurance training session is 30 min of accumulated aerobic exercise. However, as noted above, patients with COPD do not often achieve 30 min of continuous endurance training until several weeks into their rehabilitation program. In these circumstances, the aerobic exercise prescription should be applied in intervals for several weeks with the goal of achieving 30 min of cumulative aerobic exercise with each session. In normal subjects, interval training has been demonstrated to be equally effective at elevating V̇O2max (21) and V̇O2θ (33). Experience in patients with chronic pulmonary disease also seems to indicate that this is an effective strategy, although one study in severe COPD patients has shown different physiological responses (19).
In summary, the length of any program of endurance training for patients with chronic pulmonary disease should be judged by the progression of functional capacity and the achievement of clinically meaningful goals. It is unrealistic to expect that any program less than 6 wk will be effective on the basis of these criteria.
A program of structured aerobic exercise using the large muscles of the legs is clearly the most effective component of rehabilitation for patients with chronic pulmonary disease. The benefits that can be expected to accrue include increased exercise endurance and relief of dyspnea. However, in order to achieve optimal outcomes, the aerobic exercise prescription should be scientifically based with due consideration for the exercise mode, frequency, intensity, and progression.
Indirect evidence suggests that rehabilitative strategies should be implemented earlier in chronic pulmonary disease, when the potential for regaining meaningful function and quality of life is greater. In the case of the majority of the candidates who have COPD, this will necessitate earlier diagnosis and referral. In order to be deemed cost-effective, pulmonary rehabilitation programs must demonstrate the attainment of clinically meaningful differences primarily by functional exercise testing and assessment of quality of life.
Address for correspondence: Christopher B. Cooper, M.D., Professor of Medicine and Physiology, UCLA School of Medicine, 37-131 CHS, Box 951960, Los Angeles, CA 90095; E-mail: ccooper@ mednet.ucla.edu.
1. American College of Sports Medicine. General principles of exercise prescription. In: ACSM’s Guidelines for Exercise Testing and Prescription, 5th Ed. Philadelphia: Williams & Wilkins, 1995, pp. 153–176.
2. American College of Sports Medicine Position Stand. The recommended quantity and quality of exercise for developing and maintaining cardiorespiratory and muscular fitness, and flexibility in healthy adults. Med. Sci. Sports Exerc. 30: 975–991, 1998.
3. American Thoracic Society Statement. Standards for the diagnosis and care of patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 160: 1666–1682, 1995.
4. American Thoracic Society Statement. Pulmonary rehabilitation—1999. Am. J. Respir. Crit. Care Med. 159: 1666–1682, 1999.
5. Åstrand, P.-O., and K. Rodahl. Textbook of Work Physiology. Physiological Bases of Exercise, 3rd Ed. New York: McGraw-Hill, 1986, pp. 420–422.
6. Belman, M. J., L. R. Brooks, D. J. Ross, and Z. Mohsenifar. Variability of breathlessness measurement in patients with chronic obstructive pulmonary disease. Chest 99: 566–571, 1991.
7. Bergner, M., R. A. Bobbitt, W. B. Carter, and B. S. Gilson. The Sickness Impact Profile: development and final revision of a health status measure. Med. Care 19: 787–805, 1981.
8. Bickford, L. S., J. E. Hodgkin, and S. L. McInturff. National pulmonary rehabilitation survey. Update. J. Cardiopulm. Rehabil.
9. Borg G. Borg’s Perceived Exertion and Pain Scales. Champaign, IL: Human Kinetics, 1998, pp. 13–16.
10. Casaburi, R., A. Patessio, F. Ioli, S. Zanaboni, C. F. Donner, and K. Wasserman. Reductions in exercise lactic acidosis and ventilation as a result of exercise training in patients with obstructive lung disease. Am. Rev. Respir. Dis. 143: 9–18, 1991.
11. Casaburi, R., J. Porszarsz, M. R. Burns, R. S. Y. Chang, and C. B. Cooper. Physiologic benefits of exercise training in rehabilitation of patients with severe chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 155: 1541–1551, 1997.
12. Casaburi, R., and K. Wasserman. Exercise training in pulmonary rehabilitation. N. Engl. J. Med. 314: 1509–1511, 1986.
13. Clark, C. J., and J. E. Cochrane. Benefits and problems of a physical training program for asthmatic patients. Thorax 45: 345–351, 1990.
14. Clark, C. J., J. E. Cochrane, and E. Mackay. Low intensity peripheral muscle conditioning improves exercise tolerance and breathlessness in COPD. Eur. Respir. J. 9: 2590–2596, 1996.
15. Cooper, C. B. Methods of Rehabilitation in Chronic Obstructive Pulmonary Disease
. London, England: University of London, 1990, pp. 36–37. Doctoral Dissertation.
16. Cooper, C. B. Determining the role of exercise in chronic pulmonary disease. Med. Sci. Sports Exerc. 27: 147–157, 1995.
17. Cooper, C. B., and T. Storer. Exercise Testing and Interpretation. A Practical Approach. Cambridge: Cambridge University Press, 2001, pp. 217–219.
18. Cooper, D. M., D. Weiler-Ravell, B. J. Whipp, and K. Wasserman. Aerobic parameters of exercise as a function of body size during growth in children. J. Appl. Physiol. 56: 628–634, 1984.
19. Coppoolse, R., A. M. Schols, E. M. Baarends, et al. Interval versus continuous training in patients with severe COPD: a randomized controlled clinical trial. Eur. Respir. J. 14: 258–263, 1999.
20. Davies, C. T. Limitations to the prediction of maximum oxygen intake from cardiac frequency measurements. J. Appl. Physiol. 24: 700–706, 1968.
21. Debusk, R. F., U. Stenestrand, M. Sheehan, and W. L. Haskell. Training effects of long versus short bouts of exercise in healthy adults. Am. J. Cardiol 65: 1010–1013, 1990.
22. Enright, P. L., and D. L. Sherrill. Reference equations for the six-minute walk in healthy adults. Am. J. Respir. Crit. Care Med. 158: 1384–1387, 1998.
23. Fletcher, C., and R. Peto. The natural history of chronic airflow obstruction. BMJ. 25: 1645–1648, 1977.
24. Guyatt, G. H., L. B. Berman, M. Townsend, S. O. Pugsley, and L. W. Chambers. A measure of quality of life for clinical trials in chronic lung disease. Thorax 42: 773–778, 1987.
25. Horowitz, M. B., B. Littenberg, and D. A. Mahler. Dyspnea ratings for prescribing exercise intensity in patients with COPD. Chest 109: 1169–1175, 1996.
26. Jones, P. W., F. H. Quirk, C. M. Baveystock, and P. Littlejohns. A self-complete measure of health status for chronic airflow limitation. The St. George’s Respiratory Questionnaire. Am. Rev. Respir. Dis. 145: 1321–1327, 1992.
27. Knox, A. J., J. F. Morrison, and M. F. Muers. Reproducibility of walking test results in chronic obstructive airways disease. Thorax 43: 388–392, 1988.
28. Lacasse, Y., E. Wong, G. H. Guyatt, D. King, D. J. Cook, and R. S. Goldstein. Meta-analysis of respiratory rehabilitation in chronic obstructive pulmonary disease. Lancet 348: 1115–1119, 1996.
29. Lake, F. R., K. Henderson, T. Briffa, J. Openshaw, and A. W. Musk. Upper-limb and lower-limb exercise training in patients with chronic airflow obstruction. Chest 97: 1077–1082, 1990.
30. Leger, L. A., and J. Lambert. A maximal multi-stage 20-m shuttle run test to predict V̇O2
max. Eur. J. Appl. Physiol. Occup. Physiol. 49: 1–12, 1982.
31. Mejia, R., J. Ward, T. Lentine, and D. A. Mahler. Target dyspnea ratings predict expected oxygen consumption as well as target heart rate values. Am. J. Respir. Crit. Care Med. 159: 1485–1489, 1999.
32. Pollock, M. L., and J. H. Wilmore. Exercise in Health and Disease. Evaluation and Prescription for Prevention and Rehabilitation, 2nd Ed. Philadelphia: WB Saunders Company, 1990, pp. 349–350, 660–671.
33. Poole, D. C., and G. A. Gaesser. Response of ventilatory and lactate thresholds to continuous and interval training. J. Appl. Physiol. 58: 1115–1121, 1985.
34. Puente-Maestu, L., M. L. Sanz, P. Sanz, J. M. Ruiz de Ona, J. L. Rodriguez-Hermosa,and B. J. Whipp. Effects of two types of training on pulmonary and cardiac responses to moderate exercise in patients with COPD. Eur. Respir. J. 15: 1026–1032, 2000.
35. Punzal, P. A., A. L. Ries, R. M. Kaplan, and L. M. Prewitt. Maximum intensity exercise training in patients with chronic obstructive pulmonary disease. Chest 100: 618–623, 1991.
36. Redelmeier, D. A., A. M. Bayoumi, R. S. Goldstein, and G. H. Guyatt. Interpreting small differences in functional status: the six minute walk test in chronic lung disease patients. Am. J. Respir. Crit. Care Med. 155: 1278–1282, 1997.
37. Revill, S. M., M. D. Morgan, S. J. Singh, J. Williams, and A. E. Hardman. The endurance shuttle walk: a new field test for the assessment of endurance capacity in chronic obstructive pulmonary disease. Thorax 54: 213–222, 1999.
38. Ries, A. L., and the ACCP/AACVPR Pulmonary Rehabilitation Guidelines Panel. Pulmonary rehabilitation: joint ACCP/AACVPR evidence-based guidelines. J. Cardiopulm. Rehabil 17: 371–405, 1997.
39. Ringbaek, T. J., E. Broendum, L. Hemmingsen, et al. Rehabilitation of patients with chronic obstructive pulmonary disease: exercise twice a week is not sufficient. Respir. Med. 94: 150–154, 2000.
40. Siafakas, N. M., P. Vermeire, N. B. Pride, et al. Optimal assessment and management of chronic obstructive pulmonary disease (COPD): the European Respiratory Society Task Force. Eur. Respir. J. 8: 1398–1420, 1995.
41. Singh, S. J., M. D. Morgan, S. Scott, D. Walters, and A. E. Hardman. Development of a shuttle walking test of disability in patients with chronic airways obstruction. Thorax 47: 1019–1024, 1992.
42. Singh, S. J., M. D. Morgan, A. E. Hardman, C. Rowe, and P. A. Bardsley. Comparison of oxygen uptake during a conventional treadmill test and the shuttle walking test in chronic airflow limitation. Eur. Respir. J. 7: 2016–2020, 1994.
43. The COPD Guidelines Group of the Standards of Care Committee of the BTS. BTS guidelines for the management of chronic obstructive pulmonary disease. Thorax 52 (Suppl. 5): S1–S28, 1997.
44. U.S. Department of Health and Human Services. Physical Activity and Health: A Report of the Surgeon General. Atlanta: U. S. Department of Health, 1996, p. 10.
45. Ware, J. E. Jr., and C. D. Shebourne. The MOS 36-item short-form health survey (SF-36), I: conceptual framework and item selection. Med. Care 30: 473–483, 1992.
© 2001 Lippincott Williams & Wilkins, Inc.
46. Wasserman, K., B. J. Whipp, S. N. Koyal, and W. L. Beaver. Anaerobic threshold and respiratory gas exchange during exercise. J. Appl. Physiol. 35: 236–243, 1973.