Treadmill Exercise Rehabilitation Improves Ambulatory
Function and Cardiovascular Fitness in Patients With
Chronic Stroke
A Randomized, Controlled Trial
Richard F. Macko, MD; Frederick M. Ivey, PhD; Larry W. Forrester, PhD; Daniel Hanley, MD;
John D. Sorkin, MD, PhD; Leslie I. Katzel, MD, PhD;
Kenneth H. Silver, MD; Andrew P. Goldberg, MD
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Background and Purpose—Physical inactivity propagates disability after stroke through physical deconditioning and
learned nonuse. We investigated whether treadmill aerobic training (T-AEX) is more effective than conventional
rehabilitation to improve ambulatory function and cardiovascular fitness in patients with chronic stroke.
Methods—Sixty-one adults with chronic hemiparetic gait after ischemic stroke (⬎6 months) were randomized to 6 months
(3⫻/week) progressive T-AEX or a reference rehabilitation program of stretching plus low-intensity walking (R-CONTROL).
Peak exercise capacity (VO2 peak), O2 consumption during submaximal effort walking (economy of gait), timed walks,
Walking Impairment Questionnaire (WIQ), and Rivermead Mobility Index (RMI) were measured before and after 3 and 6
months of training.
Results—Twenty-five patients completed T-AEX and 20 completed R-CONTROL. Only T-AEX increased cardiovascular
fitness (17% versus 3%, ␦% T-AEX versus R-CONTROL, P⬍0.005). Group-by-time analyses revealed T-AEX
improved ambulatory performance on 6-minute walks (30% versus 11%, P⬍0.02) and mobility function indexed by
WIQ distance scores (56% versus 12%, P⬍0.05). In the T-AEX group, increasing training velocity predicted improved
VO2 peak (r⫽0.43, P⬍0.05), but not walking function. In contrast, increasing training session duration predicted
improved 6-minute walk (r⫽0.41, P⬍0.05), but not fitness gains.
Conclusions—T-AEX improves both functional mobility and cardiovascular fitness in patients with chronic stroke and is
more effective than reference rehabilitation common to conventional care. Specific characteristics of training may
determine the nature of exercise-mediated adaptations. (Stroke. 2005;36:2206-2211.)
Key Words: exercise 䡲 hemiplegia 䡲 rehabilitation 䡲 stroke
S
troke is a leading cause of disability, resulting in chronic
deficits that persistently impair function in approximately
two thirds of cases.1 Conventional rehabilitation focuses on
the subacute recovery period with therapy targeted across
initial months toward improving basic mobility and activity
of daily living skills.2 Most patients are discharged without
complete recovery, often with no recourse beyond generic
advice to stay active and continue stretching.2,3 This model is
reinforced by studies showing recovery in ambulatory function plateaus within 11 weeks in 95% of individuals receiving
conventional rehabilitation care.4 Although physical inactivity can propagate disability through deconditioning and
learned nonuse after stroke,5–7 there are no evidence-based
recommendations to promote regular therapeutic exercise in
this population.
Based on animal studies8 and increasing clinical evidence
that task-repetitive training can induce adaptive neuroplasticity,9 treadmill training has emerged as a strategy to promote
locomotor recovery after stroke. However, efficacy of this
modality is not established with a Cochrane Review reporting
no significant effects from treadmill training.10 There are no
randomized studies that establish whether exercise training
can improve both functional mobility and aerobic fitness in
the chronic phase of stroke.
We investigated T-AEX as a task-oriented modality to
optimize locomotor relearning while providing cardiovascu-
Received March 2, 2005; accepted March 29, 2005.
From the Veterans Affairs Medical Center Geriatrics Research, Education, and Clinical Center (R.F.M., F.M.I., J.D.S., L.I.K., A.P.G.); the Departments
of Neurology (R.F.M.), Gerontology (R.F.M., F.M.I., L.I.K., A.P.G.), and Physical Therapy (L.W.F.), University of Maryland School of Medicine,
Baltimore, Md; the Departments of Neurology, Division of Brain Injury Recovery (D.H.) and Physical Medicine and Rehabilitation (K.H.S.), Johns
Hopkins University, Baltimore, Md; and Good Samaritan Hospital of Baltimore (K.H.S.), Baltimore, Md.
Correspondence to Richard F. Macko, MD, University of Maryland School of Medicine, 22 S Greene St, Baltimore, MD 21201. E-mail
[email protected]
© 2005 American Heart Association, Inc.
Stroke is available at http://www.strokeaha.org
DOI: 10.1161/01.STR.0000181076.91805.89
2206
Macko et al
lar conditioning in chronic stroke.11 Initial noncontrolled
studies provide evidence that T-AEX improves fitness, leg
strength, and gait while reducing spasticity and energy costs
of hemiparetic ambulation.12–14 This randomized, controlled
trial investigates the hypothesis that T-AEX is more effective
than a rehabilitation regime including components of conventional care (R-CONTROL) to improve ambulatory function
and cardiovascular fitness in chronic stroke.
Materials and Methods
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Men or women ⬎45 years of age with chronic (⬎6 months)
hemiparetic gait after stroke were recruited from the Baltimore VA
and University of Maryland Hospitals. The protocol was Institutional
Review Board-approved and all patients provided written informed
consent. Baseline evaluations included a medical history and examination, electrocardiogram, blood chemistries and counts, Mini
Mental Status examination, Center for Epidemiological Studies
Depression Scale, and a customized exercise stress test.15,16 Exclusion criteria included heart failure, unstable angina, peripheral
arterial occlusive disease, aphasia, dementia, untreated major
depression, and other medical conditions precluding participation
in exercise.17,18
Exercise Testing
A treadmill tolerance test was first performed to assess gait safety.
Those completing ⱖ3 consecutive minutes treadmill walking at
ⱖ0.22 m/sec (ⱖ0.5MPH) proceeded to peak exercise testing.17
Subjects achieving adequate exercise intensities without signs of
myocardial ischemia or other contraindications to training were
enrolled.18 Exercise testing was performed to measure economy of
gait and VO2 peak at baseline and after 3 and 6 months training.12
Economy of gait was calculated to estimate metabolic demands of
hemiparetic ambulation.11 Measures of VO2 peak were used to index
cardiovascular fitness.17
Ambulatory Performance Measures
Timed 30-ft walks and 6-minute walks were performed at the 3 time
points. Gait velocity during timed walks is an established metric of
hemiplegic recovery,19 with 30-ft walks simulating short distances
that typify home-based mobility. Six-minute walks were performed
to assess sustainable walking capacity; an outcome representative of
greater distances required for more sustained activity of daily living
tasks.20
Functional Mobility
Rivermead Mobility Index (RMI) and Walking Impairment Questionnaire (WIQ) were analyzed to examine effects of training on
mobility. RMI includes 14 questions and an observation characterizing basic mobility.21 WIQ assessed effects of exercise on selfreported walking distance, speed, and stair climbing.22
Randomization and Blinding
After baseline testing, volunteers were randomized to either T-AEX
or R-CONTROL using a computer-based system. Because deficit
severity and age affect stroke outcomes, stratified randomization was
necessary to balance entry into groups.3 Accounting for attrition,
enrollment of 30 per group was targeted to complete 21 per group.
Preliminary power analysis based on pilot studies12 suggested that
this number would result in sufficient power to detect between group
differences in VO2 peak (0.80 power, ␣⫽0.05). Questionnaires,
surveys, and functional gait testing were conducted by blinded
technicians unaware of treatment assignment under standardized
conditions at a location (Geriatrics Research Education and Clinical
Center) separate from the training site. As a result of staffing
limitations and institutional safety regulations, treadmill exercise
testing was conducted by the same staff under physician supervision
(RFM) that provided medically supervised training. Hence, metabolic fitness tests were unblinded, but we attempted to minimize bias
Treadmill Exercise After Stroke
2207
using scripted exercise testing protocols with defined physiological
end points.11,18
Exercise Training
T-AEX training target was 3 40-minute sessions per week at target
aerobic intensity of 60% to 70% heart rate reserve (HRR).12,18
Training started at low intensity (40% to 50% HRR) for 10 to 20
minutes and increased approximately 5 minutes every 2 weeks as
tolerated. Aerobic intensity was similarly progressed by 5% HRR
every 2 weeks.
R-CONTROL provided matched duration exposure to staff implementing common components of conventional therapy. Subjects
performed 13 supervised stretching movements lasting 35 minutes2
and 5-minute low-intensity treadmill walking at 30 to 40% HRR,
approximating the aerobic stimulus of conventional rehabilitation.23
Hence, both groups were scheduled to receive 72 training sessions,
equaling 48 hours of training across 6 months.
Data Analyses
Repeated-measures analysis of variance (ANOVA) was used to
predict values of outcome variables across time. Each analysis
controlled for serial autocorrelation using one of three correlation
structures: unstructured, compound symmetry, or first-order autoregressive. Akaike’s Information Criterion and Schwarz Bayesian
Criterion were used to select among correlation structures. In cases
in which group-by-time interaction was significant, within-group
time point comparisons were made. Data are expressed as
mean⫾standard error standard deviation. A 2-tailed P⬍0.05 was
considered significant. Data analysis includes calculation of VO2
peak was expressed in absolute terms (L/min), and corrected for
body mass, and in (mL/kg/min). We compared between groups with
an unstructured covariance matrix (SAS proc mixed). Regression
and median split analyses examined whether clinical, demographic,
or training parameters were related to the treatment response.
Results
Screening evaluations were performed on 111 subjects and
61 enrolled. Fifty were excluded at baseline for neurologic
(n⫽23, 46%) or medical reasons (n⫽17, 34%), loss to follow
up (n⫽7, 14%), or psychosocial factors (n⫽3, 6%). Neurologic exclusions included diagnosis of intracranial hemorrhage (n⫽5), severe deficits (n⫽4), deficits too mild (n⫽2),
dementia (n⫽2), severe aphasia (n⫽3), depression (n⫽4),
recurrent vertigo (n⫽1), and carotid stenosis (n⫽2). There
were no significant differences in clinical or demographic
characteristics between groups (Table 1).
Training Data
Twenty-five of 32 (78%) subjects completed 6 months T-AEX.
Dropouts were the result of medical reasons unrelated to
exercise (N⫽4) or compliance issues (n⫽3). Twenty of 29
(69%) R-CONTROL completed, with dropouts resulting from
study-unrelated medical reasons (n⫽6) or compliance issues
(n⫽3). Among the dropouts in T-AEX (n⫽7) and CONTROL
(n⫽9), there were no baseline group differences in floor walking
velocity (0.51⫾0.09 versus 0.58⫾0.1 m/s, P⫽0.60), VO2 peak
(1.14⫾0.12 versus 1.22⫾0.12 L/min, P⫽0.60), 6-minute walk
distance (600⫾120 versus 742⫾157 ft, P⫽0.50), WIQ distance
(27⫾15 versus 35⫾12, P⫽0.70), RMI scores (10⫾1 versus
11⫾1, P⫽0.30), age (58⫾4 versus 65⫾3, years, P⫽0.15),
gender ratio (6:3 versus 5:2, male:female), or hemispheric lesion
location (4:5 versus 4:3, right:left). Fifteen T-AEX and 18
R-CONTROL were on antihypertensive medications, including
5 in each group on ␤-blockers. Dosage of ␤-blockers was
2208
Stroke
October 2005
TABLE 1. Clinical and Demographic Features of Patients
Randomized to Treadmill and Control Groups
Characteristic
Treadmill Exercise
Group, n⫽32 (%)
Control Group,
n⫽29 (%)
Age, y (mean⫾SD)
63⫾10
64⫾8
Gender, male:female
22:10
21:8
Race, black:white
20:12
15:14
Brain lesion side, right:left
18:14
13:16
Latency since stroke, mo
(mean⫾SD)
35⫾29
39⫾59
Coronary artery disease
7 (22)
4 (17)
Hypertension
20 (63)
25 (86)
Diabetes mellitus
13 (41)
11 (38)
Former smokers
17 (53)
13 (45)
Current smokers
5 (16)
4 (14)
15 (47)
11 (38)
Ankle–foot orthoses
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Figure 1. Mean percent change in 6-min walk distance in
T-AEX (solid line) and R-CONTROL (dotted line) groups. There
was a significant group-by-time interaction in 6-min walk distance by repeated-measures ANOVA (†P⬍0.02) with progressive
gains across the 6-month intervention period (*P⬍0.05). Values
are mean⫾standard error.
Assistive device
None
11 (34)
6 (21)
Single-point cane
13 (40)
14 (48)
Quad cane
4 (13)
7 (24)
Walker
4 (13)
2 (7)
SD indicates standard deviation.
unchanged throughout, except for discontinuation in one
R-CONTROL.
Treadmill testing and training were well tolerated with no
adverse events. Compliance was high with 84% attendance
for T-AEX and 77% in R-CONTROL. In T-AEX, all training
parameters showed progression, with initial mean aerobic
intensity of 47⫾15% HRR, increasing to 58⫾14% HRR by 6
months (P⫽0.02). Training duration increased from baseline
12⫾6 minutes to 41⫾10 minutes by 6 months (P⬍0.0001).
Training velocity increased from baseline 0.48⫾0.3 to
0.75⫾0.3 m/s by 6 months (P⫽0.012), a mean 56% increase.
There was no change in body mass in either group.
Cardiovascular Fitness and Economy of Gait
Repeated-measures ANOVA revealed a significant groupby-time interaction for VO2 peak, indicating T-AEX was
more effective in improving cardiovascular fitness levels
(P⬍0.005, Figure 1). There was a 17% increase in VO2 peak
(L/min) with T-AEX (P⬍0.001), which remained significant
after adjusting for body mass (VO2 mL/kg/min, P⫽0.001;
Table 2). Fitness gains were progressive and evenly distributed across 6-months (Figure 2). R-CONTROL group
showed no change in VO2 peak. There was no significant
group-by-time interaction for economy of gait. However,
when the interaction term was dropped, within-groups analysis revealed both groups improved (Table 2).
Ambulatory Performance Capacity
There was a significant group-by-time interaction for
6-minute walk (P⬍0.01; Table 2), with T-AEX achieving
nearly triple the gains of R-CONTROL in percentage terms
(Figure 2). T-AEX increased 6-minute walk distance by 30%
with most improvement (77%) occurring by 3 months (Figure
2). There was no group-by-time interaction for 30-ft timed
walk, and within-groups analysis revealed improved 30-ft
timed-walk velocities in both groups (Table 2).
TABLE 2. Effects of 6 Months T-AEX and R-CONTROL on Cardiovascular Fitness, Timed-Walk Performance,
and Functional Mobility
Treadmill Group
Variables
Control Group
Posttreatment
P, Group-by-Time
Interaction
1.25⫾0.36
1.28⫾0.36
0.004
14.7⫾1
14.9⫾1
0.018
Baseline
Posttreatment
Baseline
Peak VO2, L/min
1.22⫾0.47
1.43⫾0.57†
Peak VO2, mL/kg/min
14.9⫾0.9
17.3⫾1†
Economy of gait, VO2 (mL/kg/min)
10.7⫾0.6
9.9⫾0.6*
10⫾0.5
9.2⫾0.5*
0.730
6-min walk, ft
761⫾73
922⫾79†
848⫾109
868⫾100
0.018
30-ft walk usual pace, m/s
0.63⫾0.06
0.74⫾0.06*
0.67⫾0.07
0.76⫾0.08*
0.707
30-ft walk fast pace, m/s
0.82⫾0.08
0.95⫾0.09*
0.9⫾0.10
1⫾0.11*
0.970
45⫾7
70⫾7†
50⫾7
56⫾8
0.031
11.3⫾0.4
12⫾0.3
11.7⫾0.4
11.8⫾0.4
0.115
WIQ distance subscale, patients
Rivermead Mobility Index, patients
*P⬍0.01 significance for time main effect after dropping group-by-time interaction.
†P⬍0.001 for significant improvement within T-AEX group.
Macko et al
Treadmill Exercise After Stroke
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Determinants of the Response to T-AEX
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Figure 2. Between-group comparison of peak aerobic capacity
across 6 months. There was a significant time by group interaction in VO2 peak (mL/kg/min) by repeated-measures ANOVA
(†P⬍0.005). VO2 peak was significantly different from baseline at
both the 3-month and 6-month time points within the T-AEX
group (*P⬍0.05). Values are mean⫾standard error.
Functional Mobility
Group-by-time analysis revealed only T-AEX improved
WIQ– distance with 4-fold progressive improvement compared with R-CONTROL (Table 2, Figure 3). There were no
differences between groups in WIQ speed or stair-climbing
scores. Group-by-time analysis revealed no statistically significant improvements in RMI scores with T-AEX compared
with R-CONTROL (P⫽0.12).
Figure 3. Between-group comparison of WIQ distance scores
across 6 months of training shows a significant and progressive
improvement (*P⬍0.05) in the T-AEX group only. Values are
mean⫾standard error.
There were no clinical or demographic factors that predicted
a lack of T-AEX treatment response for any of the measured
outcomes. Regression analyses showed no associations between increase in VO2 peak or 6-min walk and age at entry,
latency since stroke, initial VO2 peak, or gait deficit severity
(P⫽not significant [NS]). However, progression in selected
treadmill training, parameters across 6 months were associated with key functional and fitness outcomes. Conversely,
increase in treadmill training duration predicted improvements in 6-minute walk (r⫽0.41, P⬍0.05) but not change in
VO2 peak (r⫽0.19, P⫽0.34). In contrast, increase in treadmill
training velocity predicted gains in VO2 peak (r⫽0.43,
P⬍0.05) but not change in 6-min walks (r⫽0.17, P⫽0.46).
Median split analyses according to degree of treadmill velocity progression within the T-AEX group revealed that subjects in the upper half of trainers experienced the greatest
gains in VO2 peak (25%, n⫽11, P⬍0.01), whereas those in
the bottom half of velocity progression did not reach a
significant within-group fitness gain (9%, n⫽12 P⫽NS;
Figure 4).
Discussion
We demonstrate for the first time in a randomized trial that
T-AEX improves cardiovascular fitness and ambulatory function in chronic stroke. Although both R-CONTROL and
T-AEX improved economy of gait and walking velocity over
short distances, T-AEX was requisite to improve main
outcomes of cardiovascular fitness, sustainable (6-min) ambulatory performance capacity, and the functional mobility
measures. These findings demonstrate the physiological and
functional benefits of task-oriented training administered
according to a progressive aerobic exercise formula. The data
Figure 4. Median split analysis of VO2 peak change according
to progression in training velocity across the 6 months. The
group in the upper half of velocity progression increased VO2
peak by 25% (*P⬍0.01), whereas the training group in the bottom half of velocity progression increased their peak VO2 by only
9% (P⫽NS). Values are mean⫾standard error.
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October 2005
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further suggest that training prescriptions emphasizing velocity progression rather than longer duration will optimize
gains in aerobic fitness compared with locomotor function,
respectively.
The natural history of mobility recovery after stroke
reveals a plateau within 3 to 6 months. Prospective studies
report 95% of patients show no further recovery in ambulatory function beyond 11 weeks with conventional care.4
Current practice patterns for outpatient stroke rehabilitation
typically include approximately 9 physical therapy sessions,
ending within 28 to 140 days poststroke. Yet functional
mobility declines in 43% within the year inpatient rehabilitation ends, with early therapy cessation predicting worsening.3 Randomized studies show delayed generic physiotherapy aimed at gait restoration increases 10-meter walk velocity
9% in patients with chronic stroke, whereas delayed entry
controls become 12% slower, suggesting inactivity propagates mobility declines.24 Our participants had already completed all conventional physical therapy and were a mean 3
years poststroke, well beyond the expected therapeutic window for mobility recovery. However, the results show
T-AEX improves fitness, reduces energy costs of hemiparetic
gait, and increases ambulatory function even at this late stage.
All of these outcomes may combine to improve activity of
daily living function. We identify no clinical factors that
predict lack of treatment response, including latency since
stroke to at least 10 years. Hence, such exercise models have
potential to generalize functional and cardiovascular health
benefits across a broad spectrum of the chronic stroke
population.
Cardiovascular fitness levels after stroke are only 50% of
age-matched normals, energy demands of hemiparetic gait
are elevated 1.5- to 2-fold, and patients with stroke often
cannot maintain their preferred walking pace as a result of
exercise intolerance.5,6,25 Randomized studies in patients with
chronic stroke show that although 3 months aerobic exercise
increases VO2 peak 8%, fitness levels decline 10% in delayed
entry controls,26 revealing the expected relationship between
inactivity and progressive deconditioning. Conventional rehabilitation does not systematically provide an adequate
exercise stimulus. Cardiac monitoring reveals ⬍3 min per
physical therapy session reaches low aerobic intensity.23
Notably, our R-CONTROL group maintained fitness levels
across 6 months and improved 30-ft floor walking and gait
economy, which may enable activity of daily living tasks to
be performed at a lower percent of peak exercise capacity.11
These gains may have resulted from the relatively active
nature of the R-CONTROL rehabilitation program.
Post hoc analyses suggest specific characteristics of a
T-AEX regimen may influence the nature of exercisemediated adaptations. We found that the degree of progression in training session duration predicted improvements in
6-minute walk but not VO2 peak. This suggests “mass
training,” indexed by greater repetition in longer training
sessions, governs gains in locomotor control, consistent with
animal studies in which task-repetitive sensorimotor stimuli
are crucial to mediating neuroplasticity.9 Conversely, progression in T-AEX training velocity predicted fitness gains
but not change in ambulatory function. Thus, cardiovascular
adaptations after stroke may be contingent on advancing
training velocity rather than HRR, the standard for defining
exercise intensity in non-neurologic populations.18 In addition, the trajectory of fitness gains showed no plateau,
suggesting that training beyond 6 months may produce
further benefits. The features of exercise needed to optimize
gains in aerobic fitness versus locomotor function require
confirmation in prospective studies using differing progression strategies.
The small sample size and various design issues, including
strict entry criterion, limit interpretation of this study. Only
medically eligible subjects with mild–moderate gait deficits
were enrolled, which may have selected a healthier and more
mobile cohort not entirely representative of the general stroke
population. The absence of blinding with respect toVO2 peak
testing represents another potentially confounding limitation.
Although it was impractical to completely blind testers to
subject treatment assignment during treadmill aerobic testing
as a result of personnel constraints, every effort was made to
standardize protocols to minimize bias. Although a strength
of our study is its randomized design, R-CONTROLs also
improved, indicating even stretching plus low-intensity walking is beneficial. We had no usual care control group, which
in chronic stroke typically includes no supervised exercise.
Hence, no inferences can be made regarding effectiveness of
T-AEX compared with conventional care. Finally, considering the relatively high study exclusion and dropout rates
across 6 months, we do not know what proportion of community-dwelling patients with stroke could participate in or
maintain longitudinal aerobic training.
Summary
In conclusion, T-AEX is superior to a reference control
program and requisite to improving cardiovascular fitness
and functional mobility. Specific features of the exercise
prescription unique to neurologic patients may determine the
nature of adaptations in motor function versus cardiovascular
fitness. Further studies are needed to determine whether
task-oriented exercise can improve long-term functional independence and cardiovascular health in chronic stroke.
Acknowledgments
The authors thank the participants in this study, the nurses, and
exercise physiologists in the GRECC and Pepper Centers who
assisted with the research testing and exercise training. The study
was supported in part by The Baltimore Veterans Administration
Geriatrics Research, Education, and Clinical Center, a Veterans
Affairs Medical Service Career Development Award (RFM), R29
AG14487 (RFM), T32AG00219 (APG), and P60AG12583 (Claude
D. Pepper Older Americans Independence Center; RFM).
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Richard F. Macko, Frederick M. Ivey, Larry W. Forrester, Daniel Hanley, John D. Sorkin,
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Stroke. 2005;36:2206-2211; originally published online September 8, 2005;
doi: 10.1161/01.STR.0000181076.91805.89
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