Abstract
Objective
The purpose of this study was to establish the test-retest reliability and concurrent validity with maximal oxygen uptake (VO2max) for three submaximal exercise tests in individuals with chronic stroke: 1) submaximal treadmill test, 2) submaximal cycle ergometer test and 3) six minute walk test (6MWT).
Design
Prospective study using a convenient sample
Setting
Freestanding tertiary rehabilitation centre
Participants
12 community-dwelling individuals who have had a stroke with moderate motor deficits; volunteer sample
Main Outcome Measures
Heart rate (HR), blood pressure (BP) and oxygen uptake (VO2) were assessed during the exercise tests.
Results
Test-retest reliability was good to excellent for the exercise tests (maximal and submaximal tests). VO2 for all submaximal measures related to VO2max (r=0.66 to 0.80). Neither the 6MWT distance, self-selected gait speed or hemodynamic measures related to VO2max.
Conclusion
The VO2 measures of the submaximal exercise tests had excellent reliability and good concurrent validity with VO2max. Submaximal exercise tests may be one potential method of monitoring effects of interventions following a screening test (e.g., symptom-limited graded exercise test, dobutamine stress echocardiograph).
Keywords: Cerebrovascular accident, Exercise test, Outcome assessment, Rehabilitation
Introduction
Cardiovascular disease is the leading prospective cause of death in individuals with chronic stroke.1,2 Inactivity and low cardiovascular fitness, a major occurrence in persons with stroke, is one of the modifiable risk factors associated with cardiovascular disease. Given the profoundly poor cardiovascular fitness in individuals with stroke,3 it would be ideal to develop reliable methods that relate to levels of cardiovascular fitness in these individuals.
Current measurement of cardiovascular fitness in individuals with stroke is fraught with difficulties. The symptom-limited graded exercise test is a protocol which accomplishes dual purposes: screening for cardiac disease and determining the maximal oxygen uptake. The VO2max (maximal oxygen uptake) is the criterion measure of cardiovascular fitness and is related to the functional capacity of the heart.4 However, stroke-specific impairments such as muscle weakness, fatigue, poor balance, contractures and spasticity can interfere with the ability to reach one’s maximum capacity using standard maximal exercise tests. A standard maximal exercise test may also eliminate a large number of potential clients; this test is not an assessment that is readily available to the community, and in addition, individuals who most need the assessment may not be able to tolerate the test. In fact, Peeters and Mets5 found that 22% of their elderly patients with chronic heart failure were unable to complete a standard maximal test.
A less challenging test, such as a submaximal exercise test, would be ideal to monitor levels of cardiovascular fitness. A submaximal test would also be an ideal complement to dobutamine stress echocardiograph, a nonexercise-dependent stress modality, which has been used recently in individuals with stroke as a cardiac screen prior to participation in an exercise intervention.6 Further, a submaximal test might also be better tolerated and increase the number of individuals with stroke who can be monitored and ultimately participate in cardiovascular training programs.
We evaluated three submaximal exercise tests for individuals with stroke using different exercise modalities. The first purpose of this study was to establish the test-retest reliability over separate days for the following submaximal exercise tests for individuals with stroke: 1) submaximal treadmill test, 2) submaximal cycle ergometer test and 3) six minute walk test (6MWT). Second, we determined the concurrent validity of these submaximal tests by quantifying the relationship of these tests with a gold standard criterion, VO2max, evaluated with a symptom-limited graded exercise test. Concurrent validity quantifies the relationship of one measure to another through the use of correlational statistics.7,8 Lastly, we measured the hemodynamic stress of subjects to these submaximal tests as assessed by the heart rate and myocardial exertion (i.e., the rate pressure product).
METHODS
Study Participants
Community-dwelling individuals with stroke and residual unilateral weakness were recruited on a volunteer basis. The initial screening criteria was queried with a telephone interview: 1) have a history of only one stroke of at least one year post stroke, 2) independent in walking (with or without assistive device), 3) medically stable (i.e., exclusion criteria were uncontrolled hypertension, arrhythmia, or unstable cardiovascular status, 4) no previous myocardial infarction, and 5) no significant musculo-skeletal problems from conditions other than stroke. Participants then attained written permission to participate in the study from a primary care physician who also confirmed the screening criteria (e.g., diagnosis of stroke). Participants provided their informed consent and approval was obtained from the university and hospital ethics committees.
Participants were then assessed in the lab to meet the next screening criteria which was to pedal a cycle ergometer and reach 60% of their age-predicted heart rate maximum (220 beats/min minus their age).
Protocol
Subject characteristics
Descriptive measures of the subjects were taken: age, duration of injury, type of stroke, severity of lower extremity impairment (Lower extremity score of the Chedoke-McMaster Stroke Assessment),9 and American Heart Association Stroke Functional Classification (AHASFC).10 In addition, gait and balance impairments were assessed with self-selected gait speed over an 8 m walkway (exact protocol described in Eng et al.11) and 14-item Berg Balance Scale.12,13
The lower extremity score of the Chedoke-McMaster Assessment (maximum 14) was evaluated from a structured physical assessment of the subject and consists of a leg score (1=no active movement and maximum 7=can complete normal age appropriate complex movements like rapid stepping) and foot score (1=no active movement and maximum 7=can complete normal age appropriate complex movements like rise on toes).9 The AHASFC provides a measure of independence in everyday activities where I= independent in basic activities of daily living (BADL) (e.g., self-care) and instrumental activities of daily living (IADL) (e.g., household management, using transportation) and V = completely dependent in BADL and IADL.10 The AHASFC was graded based on a structured interview with the subject. The Berg Balance Test consists of 14 tasks which challenge balance while sitting, standing or stepping (minimum score = 0 and maximum score = 56 with higher scores indicating better balance performance) and has been shown to be a valid and reliable measure.12,13
Measurement of cardiovascular fitness
The gold standard criterion of cardiovascular fitness (VO2max) was measured during a symptom-limited graded cycle ergometer test on an electronically braked upright stationary bike (Excalibre, Lode Medical Technology) in the presence of a physician, exercise physiologist and physical therapist. Subjects were attached to a 12-lead ECG (AT10i, Schiller) to monitor cardiovascular stability and wore a non-rebreathing face mask (Hans Rudolph Inc) for metabolic measurement. A Metabolic Cart (CPX-D Metabolic System, Medical Graphics Corp) measured oxygen consumption (VO2) continuously and recorded every 15 sec. Gas calibrations were performed on the metabolic cart using standard gases prior to each test. Subjects began pedaling at 0 watts with workload increments of 20 watts/min and were instructed to pedal at a comfortable rate which was generally between 50–70 rpm. Subjects were also monitored using Borg’s 16-point Ratings of Perceived Exertion scale.14 ACSM Guidelines15 were used to determine whether the exercise test should be terminated early and included: ST segment depression >2mm, increasing nervous system symptoms (i.e., ataxia, dizziness), sustained ventricular tachycardia, and chest discomfort. VO2max was the highest value attained during the test. Determination of whether maximal effort was achieved during this test followed the ACSM Guidelines15 where the following criteria needed to be met: 1) respiratory exchange ratio ≥ 1.15, 2) failure of HR to increase with further increases in exercise intensity, 3) a plateau in VO2 or < 1.5 ml/kg/min increase in VO2 following workload increases, or 4) volitional fatigue.
Submaximal tests
The submaximal tests were 1) 6MWT, 2) submaximal treadmill test and 3) submaximal cycle ergometer test. The exercise tests were undertaken on separate days. In addition, exercise tests were repeated on additional days for reliability measurement. Exercise VO2, HR and BP, in addition to the distance walked during the 6MWT, were measured during the three submaximal tests to use as potential predictors of VO2max.
The submaximal cycle ergometer test was assessed as part of the maximal cycle ergometer test and a submaximal VO2 measure of the cycle ergometer test was extracted as the VO2 corresponding to HR at 85% of age-predicted maximum (220 beats/min minus age). BP was not collected at the end of the submaximal cycle ergometer test as the maximal exercise test was still ongoing.
For the 6MWT and the submaximal treadmill test, subjects wore a HR monitor (Polar Electro Inc.) and a non-rebreathing face mask (Hans Rudolph Inc) for continuous VO2 measurement using a portable metabolic cart (KB1-C, Aerosport) and measurements were recorded every 20 seconds during the test. BP (A&D Engineering Inc) was measured and recorded at the beginning and end of the 6MWT and submaximal treadmill tests. We found the two metabolic cart systems used in this study to have less than a 5% difference in the measurement of VO2 when evaluating four healthy adults on each system (separated by one hour) using a constant submaximal workload protocol.
The 6MWT protocol is described in Eng et al.11 where subjects were instructed to “walk as far as possible around a 42 m rectangular path over six minutes”. The submaximal treadmill test was a six minute test designed to bring the subject up to a plateau at approximately 85% age-predicted HR maximum (of the maximal cycle ergometer test) within the first two minutes. All subjects held onto the front rail during the treadmill test. Subjects commenced walking at their comfortable pace on the treadmill which had been determined during a previous practice session. The comfortable treadmill speed was, on average, only 60% of the self-selected overground walking speed. During the first minute, the treadmill speed was increased three times (0.5 km/hr every 20 seconds). During the second minute, speed remained constant while the ramp increased three times (2% grade every 20 seconds). The speed and ramp were then held constant for the remainder of the test (i.e. minute two to minute six of the test). Eight of the 12 subjects used this protocol. From pilot testing, we found that individuals who had both poor Chedoke foot/ankle scores (less than 4 out of 6) and low Berg balance scores (less than 48/55) required a modified protocol with only two speed stages and the ramp was only incremented if the subject had not yet reached 85% of age-predicted HR maximum value at the end of each stage. Thus, four subjects used a modified version in which the treadmill speed was increased two times in the first minute (each increment was 0.5 km/hr) and the ramp increments (each 2%) ranged from zero to three increments.
Data reduction
All VO2 measures were normalized to body mass. The rate pressure product (RPP), a measure of myocardial oxygen demand, was calculated as the product of HR and systolic BP. VO2 for the 6MWT and submaximal treadmill test was the average over the last two minutes.
Statistical Methods
Descriptive statistics were performed for all variables measured. To assess the relative reliability between the two repeated test sessions, intraclass correlation coefficients (ICCs, [2, 1]) were calculated and provide a measure of the relative position of the measurements within a group on repeated measurements.16 The standard error of the measurement (SEM) quantified the absolute reliability in the units of the specific variable.17
The data was normally distributed (Shapiro-Wilks statistic) and Pearson Product Moment Correlations quantified the relationship between VO2max and 1) impairment measures (self-selected gait speed and Berg Balance Scale, 2) submaximal measures of VO2, 3) distance measure of the 6MWT and 4) HR and myocardial exertion (RPP) of the submaximal measures. Statistical analyses were performed with SPSS 9.0 (SPSS Inc.) using a significance level of p < 0.05 (two-tailed). Correlations were categorized by Munro et al.18 where 0.26–0.49=low correlation; 0.50–0.69=moderate; 0.70–0.89=high; 0.90–1.00=very high.
RESULTS
Twenty-seven individuals with stroke met the initial telephone screen criteria. Fifteen subjects were then excluded for a remaining 12 participants. The reasons for exclusion were: written permission from the family physician was not acquired because the subject’s physician found their patient to be medically unstable (n=2), unable to position leg on the cycle ergometer due to leg adductor spasticity, muscle weakness or reduced joint range (n=5), inability to generate sufficient leg force during cycling to elicit a HR of at least 60% age-predicted heart rate maximum (n=5), dysphagia which caused frequent coughing and disruption to the subject’s performance (n=1), unable to complete the submaximal treadmill test due to dizziness and subject subsequently requested to withdraw from study (n=1) and unable to complete all exercise tests due to time commitments (n=1). Subject characteristics are presented in Table 1. The 6MWT and self-selected gait speed were completed with the subjects using their usual assistive devices (n=1 walker, n=3 cane, n=3 ankle foot orthoses). Subjects were currently taking prescribed medications to control for hypertension (peripheral vasodilators, n=1; diuretics, n=1; ACE inhibitors, n=8) and depression (n=5).
Table 1.
Subject Characteristics (N= 12)
| Variable | Mean or # | SD | Range |
|---|---|---|---|
| Gender (Male/Female) | 11/1 | ||
| Type of stroke (ischemic/hemorrhage) | 8/4 | ||
| Hemiparetic side (Left/Right) | 5/7 | ||
| AHASFC (II/III) * | 8/4 | ||
| Chedoke-McMaster Lower Extremity Score (/14) † | 9.4 | 2.5 | 6–12 |
| Age (years) | 62.5 | 8.6 | 51–79 |
| Time since stroke (years) | 3.5 | 2.0 | 1–7 |
| Mass (kg) | 84.3 | 13.8 | 64.7–113.8 |
| Height (cm) | 174.1 | 7.1 | 164.2–185.7 |
| Body mass index (kg/m2) | 27.7 | 3.4 | 22.7–33.3 |
| Berg balance score‡ | 50.8 | 4.3 | 44 – 56 |
| Self-selected gait speed (m/s) | 1.00 | 0.30 | 0.51 – 1.41 |
AHASFC = American Heart Association Stroke Functional Classification
Maximum Chedoke-McMaster Lower Extremity Score is 14
Maximum Berg Balance Score is 56
The relative test-retest reliability of the maximal and submaximal exercise measures was very high (ICCs > 0.9) except for the submaximal treadmill test which was categorized as high (ICC=0.75) (Table 2). The standard error of the measurement (absolute reliability) demonstrated that 68% of the time, a repeated measure would be within 10% of the original measure, except for the submaximal treadmill test which was within 12% of the original measure. Given the high reliability, subsequent analyses were performed on the data from test session one.
Table 2.
Reliability of the exercise tests
| Test | Variable | ICC * | SEM † |
|---|---|---|---|
| Maximal cycle ergometer test | VO2max (ml/kg/min) | 0.93 | 1.0 |
| Submaximal cycle ergometer test | VO2 at 85% APHRM (ml/kg/min)‡ | 0.92 | 1.1 |
| Submaximal treadmill test | VO2 (ml/kg/min) | 0.75 | 1.6 |
| 6 minute walk test | VO2 (ml/kg/min) | 0.96 | 0.7 |
| 6 minute walk test | Distance covered (m) | 0.99 | 12.4 |
ICC = Intraclass correlation coefficient (2,1)
SEM = standard error of the measurement
APHRM = age-predicted heart rate maximum (220 beats/min minus age)
The physiological responses to the exercise tests are presented in Table 3. All subjects achieved maximal effort during the symptom-limited exercise test as defined by the criteria outlined by ASCM.13 Subjects reached a mean 95% of their age-predicted HR maximum during the symptom-limited graded exercise test and all but one subject’s actual HR maximum was within 10% of their age-predicted HR maximum. Subjects reached less than 80% of the age-predicted HR maximum for the submaximal treadmill test and 6MWT. The submaximal VO2 measures of the cycle, treadmill, and 6MWT were 81%, 77% and 70%, respectively, of the VO2max values. Myocardial exertion (i.e., RPP) for the treadmill and 6MWT were 73% and 69% of the maximal exercise test values.
Table 3.
Physiological responses to the exercise tests (N= 12)
| Test | Variable | Mean | SD | Range | |
|---|---|---|---|---|---|
| Max cycle ergometer test | VO2max (ml/kg/min) | 17.2 | 3.0 | 14.0 – 23.2 | |
| % APHRM at end of test * | 94.7 | 14.8 | 62.5–104.6 | ||
| HR at end of test (beats/min) | 148.0 | 24.7 | 100 – 188 | ||
| BP at end of test (mmHg) | Systolic | 174.9 | 19.0 | 150 – 200 | |
| Diastolic | 83.1 | 8.3 | 70 – 94 | ||
| RPP at end of test | 25.7 | 4.3 | 18 – 32.6 | ||
| Submax cycle ergometer measure | VO2 at 85% APHRM (ml/kg/min) | 14.0 | 3.0 | 8.2 – 19.1 | |
| HR at end of test (beats/min) | 134.0 | 8.1 | 118 – 144 | ||
| Submax treadmill test | VO2 (ml/kg/min) | 13.3 | 2.7 | 9.5 – 18.4 | |
| % APHRM at end of test | 77.9 | 10.4 | 56.2–95.4 | ||
| HR at end of test (beats/min) | 122.4 | 15.8 | 90 – 146 | ||
| BP at end of test (mmHg) | Systolic | 154.2 | 15.4 | 154 – 171 | |
| Diastolic | 81.8 | 12.1 | 71 – 98 | ||
| RPP at end of test | 18.8 | 2.9 | 13.9 – 23.4 | ||
| 6MWT | VO2 (ml/kg/min) | 12.0 | 3.3 | 8.3 – 17.7 | |
| % APHRM at end of test | 76.6 | 12.2 | 50.0–98.7 | ||
| HR at end of test (beats/min) | 120.3 | 18 | 80 – 148 | ||
| BP at end of test (mmHg) | Systolic | 146.9 | 27.3 | 109 – 202 | |
| Diastolic | 80.1 | 12.3 | 58 – 98 | ||
| RPP at end of test | 17.8 | 4.9 | 12.4 – 29.9 | ||
| Distance covered (m) | 378.3 | 123.1 | 208.5 – 574.0 | ||
APHRM = age-predicted heart rate maximum (220 beats/min minus age)
All submaximal VO2 measures correlated significantly with VO2max with the highest correlation with the submaximal cycle ergometer test. No significant relationship was found between VO2max and distance gait variables (6MWT distance, self-selected gait speed) or any of the hemodynamic values (HR, BP, RPP) measured at the end of the tests. Secondary analyses examined the relationship between VO2max and the change in hemodynamic measures (i.e., change in HR, BP and RPP) to control for baseline measures, however, none of these correlations were significant.
DISCUSSION
The presentation and severity of impairments vary widely in individuals with stroke and consequently, there is a need to develop valid exercise tests to monitor levels of cardiovascular fitness using a variety of exercise modalities. It would be useful in the future to also validate an arm ergometer test for those individuals who do not have adequate lower extremity function to tolerate a walking or cycling protocol. Since the study design required that subjects be able to complete both the walking and cycling exercise tests, this resulted in a sample of individuals with stroke who would not be considered to have severe impairments. We excluded a large number of subjects who could ambulate, but could not sufficiently pedal a cycle ergometer. Despite only moderate impairments, the cardiovascular fitness (as measured by the VO2max) of these subjects was less than half of the reference values demonstrated in healthy, similarly aged individuals.19,20 Our values were similar in range to those reported previously in individuals with stroke.3,21–23
Impairments resulting from stroke, such as muscle weakness, pain, spasticity and poor balance, in addition to a reduced tolerance to activity can result in further sedentary lifestyle and poor cardiovascular fitness. Mol and Baker24 found that 50% of their geriatric stroke patients demonstrated objective symptoms (e.g., failure of heart rate to return to baseline within three minutes following a 50 yard walk) and experienced subjective symptoms (e.g., shortness of breath, dizziness) of activity intolerance. Structural changes in muscle have been reported in individuals with stroke and include a proportionate increase of type I slow twitch fibres.25–27 Although these muscle changes could seemingly enhance endurance performance, these changes are accompanied by a reduction in the number of motor units28 and a reduced ability to generate force29 and consequently workload.
Although VO2max related to each of the submaximal VO2 measures, the highest correlation was attained using the submaximal cycle ergometer. This high correlation is in part due to the fact that the submaximal cycle ergometer test and maximal test were evaluated from the same event under the same conditions. It also verifies that a good prediction of VO2max could have been attained if the cycle ergometer test had been terminated at 85% of age-predicted HR maximum. The other two VO2 submaximal measures (treadmill test, 6MWT) may have resulted in slightly lower correlations because the tasks were different (i.e., required difference muscles, joint ranges and coordination) between the submaximal and maximal exercise tests. Furthermore, more accurate estimates of VO2max will be attained as the exercise intensity approaches the maximal protocol; the end-point HR and VO2 for the submaximal cycle ergometer test was higher than the submaximal treadmill test and 6MWT. It was disappointing that none of the hemodynamic or distance measures correlated with VO2max since it is these measures which could be easily implemented in the clinical setting as they do not require expensive oxygen measuring equipment. Distance measures of gait function may not necessarily relate to cardiovascular fitness, as other stroke-specific impairments may be more critical for walking function. We recently showed that the 6MWT distance and self-selected gait speed was related to balance, spasticity, and muscle strength in individuals with stroke.11 In contrast, Ryan et al.3 reported that VO2peak acquired from a treadmill protocol correlated moderately with self-paced walking speed (r=0.53). This discrepancy is likely due in part to the wide range of walking abilities in their study which increases the between subject variance and can substantially elevate the correlation. All our subjects were considered to be community ambulators with the slowest subject walking at 0.51 m/sec while Ryan et al.3 included three subjects who walked less than 0.22 m/sec and generally used a wheelchair for mobility.
This study was a preliminary attempt to establish reliability and concurrent validity of submaximal exercise measures in individuals with stroke which has not been undertaken previously. One of the major limitations of this study was the small sample size and the generalizability of this sample. Note that submaximal exercise testing cannot be used as the sole substitute for maximal exercise testing as the later provides many benefits, particularly in the medical screening of the subject and the determination of the subject’s actual HR maximum. We found that the age-predicted HR maximum could be plus or minus 10% of the actual HR maximum and thus, will not be as accurate as using the true HR maximum from a maximal exercise test. This may be less important if one is only examining changes over time and the age-predicted HR maximum is used as a constant. Submaximal exercise testing may not be as precise as maximal exercise testing, but it can provide a reasonably accurate reflection of an individual’s level of cardiovascular fitness at a reduced risk. Furthermore, submaximal exercise tests developed for different modalities may allow more individuals with stroke to participate in cardiovascular training.
Table 4.
Pearson Product Moment Correlations (R) with VO2max
| Task | Measure | R |
|---|---|---|
| Balance | Berg balance score | 0.38 |
| Gait | Self-selected speed | 0.32 |
| Submaximal cycle ergometer test | Relative VO2 at 85% APHRM * | 0.80† |
| Submaximal treadmilltest | Relative VO2 | 0.71‡ |
| Submaximal treadmill test | HR at end of test | 0.21 |
| Submaximal treadmill test | RPP at end of test | −0.13 |
| 6MWT | Relative VO2 | 0.66‡ |
| 6MWT | HR at end of test | 0.18 |
| 6MWT | RPP at end of test | 0.02 |
| 6MWT | Distance covered | 0.37 |
APHRM = age-predicted heart rate maximum (220 beats/min minus age)
p< 0.01
p <0.05
Acknowledgments
Financial Support: BC Health Research Foundation and Grant-in-Aid from the Heart and Stroke Foundation of BC and Yukon and career scientist award from the Canadian Institutes of Health Research to JJE (MSH-63617). We also thank Dr. Don McKenzie and Ms. Diana Jespersen for their expertise and use of the Allan McGavin Sports Medicine Centre.
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