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(Stroke. 1997;28:326-330.)
© 1997 American Heart Association, Inc.

Articles

Treadmill Aerobic Exercise Training Reduces the Energy Expenditure and Cardiovascular Demands of Hemiparetic Gait in Chronic Stroke Patients

A Preliminary Report

R.F. Macko, MD; C.A. DeSouza, PhD; L.D. Tretter, BS; K.H. Silver, MD; G.V. Smith, PhD; P.A. Anderson, PhD; Naomi Tomoyasu, PhD; P. Gorman, MD D.R. Dengel, PhD

the Neurology and Geriatrics Services and the Geriatrics Research, Education, and Clinical Center, Baltimore (Md) Department of Veterans Affairs Medical Center (R.F.M., L.D.T., K.H.S., N.T.); Departments of Neurology (R.F.M., K.H.S., P.G.), Physical Therapy (G.V.S., P.A.A.), and Medicine, Division of Gerontology (R.F.M., K.H.S.), University of Maryland School of Medicine, Baltimore; Department of Kinesiology, University of Colorado at Boulder (C.A.D.); and Division of Geriatrics and the Geriatrics Research, Education, and Clinical Center, Ann Arbor (Mich) Department of Veterans Affairs Medical Center (D.R.D.).

Correspondence to Richard Macko, MD, Department of Neurology, University of Maryland School of Medicine, 22 N Greene St, Baltimore, MD 21201-1595.

	Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Background and Purpose Elevated energy costs of hemiparetic gait contribute to functional disability after stroke, particularly in physically deconditioned older patients. We investigated the effects of 6 months of treadmill aerobic exercise training on the energy expenditure and cardiovascular demands of submaximal effort ambulation in stroke patients with chronic hemiparetic gait.

Methods Nine older stroke patients with chronic hemiparetic gait were enrolled in a 6-month program of low-intensity aerobic exercise using a graded treadmill. Repeated measures of energy expenditure based on steady state oxygen consumption during a standardized 1-mph submaximal effort treadmill walking task were performed before and after training.

Results Six months of exercise training produced significant reductions in energy expenditure (n=9; 3.40±0.27 versus 2.72±0.25 kcal/min [mean±SEM]; P<.005) during a given submaximal effort treadmill walking task. Repeated measures analysis in the subset of patients (n=8) tested at baseline and after 3 and 6 months revealed that reductions in energy expenditure were progressive (F=11.1; P<.02) and that exercise-mediated declines in both oxygen consumption (F=9.7; P<.02) and respiratory exchange ratio (F=13.4; P<.01) occurred in a strong linear pattern. These stroke patients could perform the same standardized submaximal exercise task at progressively lower heart rates after 3 months (96±4 versus 87±4 beats per minute) and 6 months of training (82±4 beats per minute; F=35.4; P<.002).

Conclusions Six months of low-intensity treadmill endurance training produces substantial and progressive reductions in the energy expenditure and cardiovascular demands of walking in older patients with chronic hemiparetic stroke. This suggests that task-oriented aerobic exercise may improve functional mobility and the cardiovascular fitness profile in this population.

Key Words: cerebrovascular disorders • energy metabolism • exercise • hemiplegia • rehabilitation

	Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Each year approximately 500 000 Americans suffer a stroke, nearly two thirds of whom have residual neurological deficits that persistently impair function.^{1 2} Principal among them are hemiparetic disturbances affecting gait, which impose excessive energy expenditures during walking.^{3 4 5} Elevated energy requirements of hemiparetic gait are of particular concern in the elderly, in whom advancing age and residual neurological deficits promoting a sedentary lifestyle lead to declining cardiovascular fitness, disuse atrophy, and weakness.^{6 7 8 9 10}

Recent studies show that gait recovery after ischemic stroke appears to plateau within several months.¹¹ This is consistent with the time frame of conventional stroke rehabilitation, which emphasizes therapies for optimizing recovery of activities of daily living in the early poststroke period. Aerobic exercise is not routinely prescribed for older stroke patients, in either the early or chronic phases of hemiparesis,¹² despite evidence that this population is physically deconditioned and has a high prevalence of cardiovascular disease risk factors potentially modifiable by exercise therapy.^{8 13 14 15 16} This may be a consequence of practitioners' concerns of fall risk, injury from repetitive exercise, or lack of evidence to date that exercise training can reduce the high energy expenditure or cardiovascular demands of walking in the chronic hemiparetic condition.

The present study investigated the safety and efficacy of graded treadmill as an aerobic exercise training modality in older stroke patients with chronic mild to moderate hemiparetic gait disturbance. Treadmill exercise was selected based on the hypothesis that task-oriented training may be most conducive to locomotion learning^{17 18 19} and that hemiparetic patients, although strictly limited with respect to gait velocity, can perform regular aerobic exercise training using a "low-velocity treadmill" at progressive workloads by advancing inclines.²⁰ We investigated the hypothesis that 6 months of low-intensity aerobic exercise on a graded treadmill will produce significant reductions in the energy expenditure and cardiovascular demands of hemiparetic ambulation.

	Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Patients 50 years of age or older with mild to moderate hemiparetic gait after ischemic stroke were recruited from the Stroke Clinic at the Baltimore Department of Veterans Affairs Medical Center. Mild to moderate hemiparetic gait was defined as a readily observable asymmetry of gait, with preserved capacity for independent ambulation with an assistive device as necessary. All patients had previously completed conventional rehabilitation therapy and had chronic residual hemiparetic deficits more than 6 months after index cerebral infarction. Baseline evaluations included medical history and examination, cardiac evaluation, and the Center for Epidemiologic Studies Depression Scale to screen for depression.²¹ Exclusion criteria included congestive heart failure, angina, peripheral vascular disease, orthopedic conditions, and other medical or neuropsychiatric conditions (eg, depression, significant dementia) limiting participation in a low-intensity treadmill exercise program. Patients already performing regular aerobic exercise were excluded to avoid prior training effect.

An entry treadmill ambulation screening test was designed to evaluate treadmill tolerance and to select a target velocity for subsequent maximal effort exercise testing. Exercise tests were performed with the use of a SensorMedics Max 1001 treadmill (SensorMedics) with continuous monitoring of electrocardiogram and vital signs. The entry treadmill screening test was initiated at 0.5 mph, and the velocity was advanced by 0.1-mph increments according to the patient's tolerance and observer-rated gait stability. All tests were conducted by the same physician familiar with gait evaluation (R.F.M.), and testing was terminated on the patient's request or if gait instability or cardiovascular decompensation was observed, according to the guidelines of the American College of Sports Medicine.²² Handrail support was allowed ad libitum, and patients were instructed to minimize handrail support to that necessary for stabilizing balance. A support belt was worn as a safety measure, but no support was provided unless gait difficulties were observed.

Patients capable of performing treadmill walking of at least 0.5 mph underwent subsequent maximal effort exercise testing in which a modification of the Balke protocol was used to screen for coronary artery disease.^{22 23} This constant-velocity graded treadmill test was performed at the target gait velocity previously determined from the entry treadmill screening test, with the same safety precautions and continuous monitoring of electrocardiogram and vital signs. Tests were terminated at the patient's request or according to American College of Sports Medicine criteria.²² Eligible patients included those achieving adequate exercise intensities without significant signs of myocardial ischemia or other contraindications to participation in a low-intensity aerobic exercise training program.

The 6-month low-intensity aerobic exercise training program consisted of three sessions of 40 minutes each per week of graded treadmill walking at 50% to 60% of heart rate reserve (HRR). HRR was determined according to the formula of Karvonen.²⁴ Maximal heart rate was defined as the highest observed during two separate maximal effort exercise tests. Handrail support was allowed ad libitum. Treadmill warm-up and cool-down periods of 5 minutes' duration at approximately 30% of HRR accompanied each training session. Training was started conservatively at 40% of HRR, with 10 to 20 minutes of exercise per session, and advanced as tolerated to the target 50% to 60% HRR.

A standardized submaximal effort treadmill task (1 mph, no incline) representative of typical slow hemiparetic gait was performed with open circuit spirometry to measure oxygen consumption (VO₂) under steady state conditions. Patients wore a nose clip and breathed through a mouthpiece or were fitted with a non-rebreathing mask (Hans Rudolph) to collect expired air; repeated testing maintained use of the same pulmonary attachments within individuals. All patients had performed prior submaximal and maximal treadmill exercise to ensure acclimatization to the treadmill. Inspired air volumes were measured with a Rayfield Equipment gas meter, and expired O₂ and CO₂ were analyzed every 30 seconds with Ametek S-3A/I and CD 3A analyzers, respectively. Ventilation, CO₂ production, and the respiratory exchange ratio (RER) (expired VCO₂/VO₂ consumed) were continuously measured by computer interfaced with gas analyzers. The initial 6 minutes of walking allowed for steady state VO₂ to be achieved. Mean VO₂ and RER were then determined from the ensuing 3 minutes of walking at steady state O₂ kinetics, and energy expenditure (in kilocalories per minute) was estimated with the use of the caloric equivalent for a liter of O₂ at the measured RER. A nonprotein substrate mixture was assumed. If VO₂ did not achieve steady state within the initial 6 minutes at 1-mph walking, submaximal exercise testing was terminated and repeated another day at a lower velocity. Exercise tests were repeated after 3 and 6 months of training; a treadmill calibrated to the same velocity was used, and patients wore the same shoes and/or orthotic devices.

Data analysis included calculation of VO₂ expressed relative to body mass (expressed in milliliters per kilogram per minute) and in absolute terms (expressed in liters per minute) to account for the factor of any weight loss during training. Repeated measures analysis was used to compare variables in those patients who underwent exercise testing at baseline and after 3 and 6 months of training. Polynomial contrast was further used to analyze the pattern of exercise-mediated adaptations over these three time points. All data are expressed as mean±SEM, with significance set at the P<.05 level.

	Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
We evaluated nine black and three white men. One patient without known cardiac disease failed exercise testing because of cardiopulmonary intolerance and was excluded. Two patients were lost to follow-up, including one who had completed baseline testing but did not enter training because of development of an unrelated podiatric disorder. The clinical and demographic features of nine patients entered in exercise training are shown in Table 1. All patients used a single-point cane at the time of study entry, and two patients used an ankle-foot orthosis. No patients had hemineglect syndromes, motor apraxia, cerebellar ataxia, or significant sensory deficits complicating gait performance. All were in normal sinus rhythm, and six were receiving antihypertensive medications during the period of training, including two patients receiving ß-blockers. The dosage of ß-blocker medications was unchanged throughout the period of exercise training and testing.

View this table: [in this window] [in a new window]   Table 1. Clinical and Demographic Features of Nine Stroke Patients Entered in Aerobic Exercise Training

Initial aerobic exercise training was performed at a mean of 40±3% of HRR for 15±2 minutes. This was progressively increased to 55±5% HRR for 31±1 minutes by 3 months and to 38±2 minutes at a mean of 54±3% HRR by the 6th month of training. Treadmill training was initiated at a mean of 1.6±0.1 mph (no incline) and gradually increased to a mean of 2.0±0.2 mph and 1.9±0.4% incline by 3 months. Training parameters were advanced to 2.2±0.2 mph at inclines of 2.2±0.5% by the 6th month. Patients attended 90% of training sessions, and there were no serious adverse experiences during treadmill testing or training. Two patients had intermittent foot cramping in the hemiparetic limb during treadmill walking. One patient consistently developed fatigue with cramping in the nonhemiparetic limb, which was preferentially worsened by advancing treadmill velocity rather than incline. None of these symptoms interfered with regular exercise training.

Six months of aerobic exercise training produced significant reductions in both the steady state VO₂ (0.69±0.05 versus 0.56±0.05 L/min; n=9; P<.01) and RER (0.90±0.02 versus 0.84±0.02; P<.005) during submaximal effort treadmill exercise testing. These exercise-mediated improvements accounted for a 21% reduction in the energy expenditure required to perform this standardized walking task (3.4±0.3 versus 2.7±0.3 kcal/min; P<.005). Most patients (7 of 9) demonstrated reduced energy expenditure during submaximal effort walking, with improvements occurring over a wide range (Figure). One patient was tested only at baseline and after 6 months of training. Results for repeated measures ANOVA conducted in the subset of patients (n=8) with complete data at baseline and after 3 and 6 months of training are shown in Table 2. Further analysis that included polynomial contrast revealed that these exercise-mediated reductions in energy expenditure (F=11.1; P<.02) and RER (F=13.4; P<.01) during submaximal effort walking were progressive and occurred in a strong linear pattern. Likewise, exercise training produced a progressive and linear reduction in the steady state VO₂ during submaximal effort treadmill walking whether expressed in absolute terms (liters per minute; F=9.7; P<.02) or relative to body mass (milliliters per kilogram per minute; F=11.6; P<.005).

View larger version (18K): [in this window] [in a new window]   Figure 1. Energy expenditure during a standardized 1-mph treadmill ambulation task in nine hemiparetic stroke patients at baseline and after aerobic exercise training.

View this table: [in this window] [in a new window]   Table 2. Results From 1-mph Submaximal Exercise Treadmill Ambulation Testing at Baseline and After 3 and 6 Months of Aerobic Exercise Training in Eight Stroke Patients

These stroke patients performed the same submaximal exercise task at progressively lower heart rates after 3 and 6 months of training (Table 2). Training-associated declines in heart rate were progressive and occurred in a strong linear pattern (F=35.4; P<.002) throughout the 6-month period. Polynomial contrast analysis also showed that in addition to the strong linear pattern in heart rate decline with training, there was a small but significant nonlinear (quadratic) pattern (F=6.6; P<.05) due to the decreased slope of heart rate decline noted between the 3rd and 6th months.

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Early studies recognized the high energy expenditure of hemiparetic gait after stroke. The energy expenditure required to perform routine ambulation is elevated approximately 1.5- to 2-fold in hemiparetic stroke patients compared with normal control subjects.^{4 5} Hemiparetic stroke patients, particularly those with advanced age, are often unable to maintain their most efficient walking speed comfortably, indicating that the elevated energy demands of walking and poor endurance further compromise functional mobility.^{5 25 26} The present study examined the effects of task-oriented aerobic exercise on submaximal effort walking performance in older hemiparetic stroke patients. The results show that aerobic exercise training produces a substantial reduction in the energy expenditure and cardiovascular demands of hemiparetic ambulation.

Few studies have examined the effects of exercise training in the chronic stroke population. In one study, 12 weeks of bicycle ergometry training improved the peak exercise workload capacity and Tennessee Self-Concept Scale scores in seven hemiparetic stroke patients.²⁷ However, there were no direct measurements of cardiovascular fitness, and motor function improvements were characterized by subjective descriptions rather than standardized functional evaluations. In the only randomized study, 10 weeks of modified bicycle ergometry training improved maximal exercise VO₂ by 14% in chronic hemiparetic patients, demonstrating that stroke patients can increase their cardiovascular fitness levels by a magnitude similar to that expected in healthy older patients performing similar endurance training programs.¹³ These investigators also showed that improvements in maximal workload capacity (43%) exceeded those expected based on the increase in VO₂max, suggesting that exercise training improved motor efficiency, at least as measured by a modified bicycle ergometry task.

In contrast to prior studies in which maximal exercise performance was the principal outcome, we measured VO₂ and RER during submaximal effort walking under steady state oxygen conditions, permitting estimates of the energy expenditure at a task representative of routine daily ambulation. Our findings that aerobic exercise training reduces energy expenditure of hemiparetic walking are consistent with the hypothesis that exercise-mediated neuromuscular adaptations lead to improved gross motor efficiency in the chronic hemiparetic condition. These results extend the observations of a potential benefit from task-oriented aerobic exercise training to the clinically relevant task of submaximal effort hemiparetic ambulation.

Total energy expenditure during walking consists of two components: (1) basal metabolic rate while standing and (2) energy expenditure directly attributable to the external work of walking.²⁸ Although we did not measure energy expenditure during standing rest, it is unlikely that this basal metabolic parameter would be reduced by our training paradigm.²⁹ If one considers that the observed 21% reduction in absolute energy expenditure was likely related only to the component of reduced energy cost for walking, the magnitude of training effect becomes even more substantial.

The reduced energy cost of hemiparetic walking is not attributable to lowered workload due to weight loss, since mean weights did not significantly change. However, in the absence of a control group, results of this study must be interpreted with caution. Treadmill is a simulated walking task, and estimates of energy expenditure are subject to bias from effects of handrail support and potential gait facilitation from the treadmill itself. Whether exercise-mediated improvements in the energy economy of treadmill walking translate into improved activities of daily living cannot be determined from the present study but remain a topic of ongoing investigation.

The mechanisms underlying the reduced energy expenditure of hemiparetic gait remain uncertain. Alterations in central gait patterning, spasticity, and reduced oxidative capacity in paretic musculature are hypothesized to explain the elevated energy costs of hemiparetic gait.^{26 30 31} Treadmill training with handrail support may improve gait biomechanics, as demonstrated after partial weight suspension treadmill training in nonambulatory hemiparetic patients.³² Alternatively, exercise may enhance muscle oxidative capacity in this sedentary older population, irrespective of neurological status or the task-oriented training modality. Older men have higher oxygen demands per distance traversed and a greater RER at a given submaximal workload than younger adults.^{33 34} Aerobic exercise training improves these parameters in healthy young and middle-aged adults.³⁵ We show for the first time that aerobic exercise therapy reduces energy expenditure of hemiparetic gait in older stroke patients with chronic neurological deficits. Further investigations are planned to determine whether these exercise-mediated adaptations are due to improved central gait patterning or skeletal muscle function.

The clinical implications are that aerobic exercise training may enhance functional mobility in stroke patients by improving cardiovascular fitness and enabling activities of daily living to be performed at a lower percentage of maximal aerobic capacity. Although the present study includes only older men, physiological effects of exercise conditioning are well documented in a diversity of nonstroke populations, including women and younger adults.^{35 36 37} Likewise, the benefits of a task-oriented exercise program in stroke patients may be expected to extend across genders and a broad age spectrum.

Training-associated declines in heart rate during submaximal exercise suggest a cardiovascular conditioning response. Cardiovascular comorbidity is a significant health concern present in approximately 75% of stroke patients, and cardiac disease remains the leading prospective cause of death in long-term stroke survivors.^{38 39} Thus, our findings support a rationale for regular aerobic exercise to improve cardiovascular health after stroke, consistent with recent consensus statements on exercise and public health.⁴⁰

In summary, the results of this study show that progressive graded treadmill with handrail support is a safe and effective modality for long-term aerobic exercise training in some older patients with mild to moderate hemiparetic gait disturbance. Six months of low-intensity training produces a progressive reduction in the energy expenditure and cardiovascular demands of a standardized submaximal effort walking task, suggesting improved cardiovascular fitness and gross motor efficiency in chronic hemiparetic stroke patients. Further studies are needed to define the characteristics of patients most likely to benefit from a structured aerobic exercise program and to determine whether treadmill training improves functional mobility and the cardiovascular health profile in the chronic stroke population.

	Acknowledgments

 
This study was supported in part by the Baltimore Veterans Administration Geriatrics Research, Education, and Clinical Center through a Veterans Health Administration Research Advisory Group grant (12A7A to Dr Macko). Drs Macko and Silver were recipients of a pilot grant from the Claude D. Pepper Older Americans Independence Center from the National Institute on Aging (P60-AG12583). The authors wish to acknowledge Dr Andrew P. Goldberg for his support in this project.

Received August 6, 1996; revision received October 28, 1996; accepted November 1, 1996.

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