effects of intensive physical rehabilitation on neuromuscular

EFFECTS OF INTENSIVE PHYSICAL REHABILITATION
ON NEUROMUSCULAR ADAPTATIONS IN ADULTS WITH
POSTSTROKE HEMIPARESIS
LARS L. ANDERSEN,1 PETER ZEEMAN,2 JØRGEN R. JØRGENSEN,2 DANIEL T. BECH-PEDERSEN,2
JANNE SØRENSEN,2 MICHAEL KJÆR,3 AND JESPER L. ANDERSEN3
1
National Research Center for the Working Environment, Copenhagen, Denmark; 2Center for Rehabilitation of Brain Injury,
University of Copenhagen, Copenhagen S, Denmark; and 3Institute of Sports Medicine, Bispebjerg Hospital, Copenhagen NV,
Denmark
ABSTRACT
Andersen, LL, Zeeman, P, Jørgensen, JR, Bech-Pedersen, DT,
Sørensen, J, Kjær, M, and Andersen, JL. Effects of intensive
physical rehabilitation on neuromuscular adaptations in adults
with poststroke hemiparesis. J Strength Cond Res 25(X): 000–
000, 2011—Hemiparesis—disability and muscle weakness of 1
side of the body—is a common consequence of stroke. Highintensity strength training may be beneficial to regain function,
but strength coaches in the field of rehabilitation need
evidence-based guidelines. The purpose of this study was to
evaluate the effect of intensive physical rehabilitation on
neuromuscular and functional adaptations in outpatients
suffering from hemiparesis after stroke. A within-subject
repeated-measures design with the paretic leg as the
experimental leg and the nonparetic leg as the control leg
was used. Eleven outpatients with hemiparesis after stroke
participated in 12 weeks of intensive physical rehabilitation
comprising unilateral high-intensity strength training with nearmaximal loads (4–12 repetition maximum) and body weight
supported treadmill training. At baseline and 12-week followup, the patients went through testing consisting of isokinetic
muscle strength, neuromuscular activation measured with
electromyography (EMG), electrically evoked muscle twitch
contractile properties, and gait performance (10-m Walk Test
and 6-min Walk Test). After the 12-week conditioning program,
knee extensor and flexor strength increased during all contraction
modes and velocities in the paretic leg. Significant increases
were observed for agonist EMG amplitude at slow concentric
and slow eccentric contraction. Twitch torque increased,
whereas twitch time-to-peak tension remained unchanged. By
contrast, no significant changes were observed in the nonparetic
Address correspondence to Lars L. Andersen, [email protected].
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control leg. Gait performance increased 52–68%. In conclusion,
intensive physical rehabilitation after stroke leads to clinically
relevant neuromuscular improvements, leading to increased
voluntary strength during a wide range of contraction modes
and velocities, and improved gait velocity. Strength training
coaches working in the field of rehabilitation can use this
knowledge to safely and efficiently add high-intensity strength
training to existing rehabilitation paradigms.
KEY WORDS electromyography, stroke, physical therapy,
isokinetic, twitch, resistance training
INTRODUCTION
S
troke is the most frequent type of acquired brain
injury and remains a leading cause of death and
disability worldwide (40). In the United States
alone, 780,000 people experience a new or recurrent stroke annually (47). The majority of adults suffering
from stroke now survive, leaving a challenge for the medical
system to provide efficient rehabilitation (37,63). Neurological and functional recovery occurs gradually for up to
20 weeks after the lesion and thereafter plateaus (34). A half
year after the lesion has occurred, half of all adults surviving
from stroke still display disabilities in essential activities of
daily living (33). In the long term, more than a third of all the
survivors of stroke are left dependent on other people for
performing the activities of daily living (61).
Hemiparesis is common after stroke, affecting half of the
survivors chronically (47). Poststroke weakness can be
marked with losses of muscle strength of .50% (3,12,51).
Contrastingly, a certain minimal threshold of muscle strength
is required to perform activities of daily living (15,52) and to
prevent falls in the frail elderly (16). Importantly, voluntary
muscle strength of the knee extensors has been shown to be
closely related to gait ability in patients with stroke (13,58).
Thus, loss of muscle strength after stroke is considered
a major determinant of disability (11,17,41). Consequently,
a cornerstone in rehabilitation should be to regain muscle
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Rehabilitation of Stroke
strength (46). Although some studies found no convincing
effect of strength training on functional outcome (27,36,39),
the majority of studies have documented positive effects of
4–12 weeks of strength training weeks on poststroke
weakness (9,14,21,24,45,50,55,58,59). However, there is
limited knowledge of the underlying neural and muscular
adaptation mechanisms of strength gains in response to
strength training in adults suffering from stroke (46).
While neuromuscular activation can be estimated using
surface electromyography (EMG) during maximal voluntary
muscle contraction (1), intrinsic muscle contractile properties
can be assessed by electrically evoked twitch contractions of the
resting muscle (29). Weakness after stroke has been associated
with decreased neuromuscular activation of agonist muscles of
the paretic limb (20,26,28). In contrast, conflicting results exist
with regard to muscular changes. Although muscular atrophy
after long-term hemiparesis has been reported (35,49), a more
recent study found no evidence for this (18). However, 1 study
reported lower electrically stimulated twitch torque of the
paretic leg compared with the contralateral leg (56), indicating
decreased intrinsic contractile strength capacity. Thus, more
research is warranted in this area.
Maximal voluntary muscle contraction strength is expressed
by a combination of both neural and muscular factors and can
be measured during various contraction modes and velocities
using isokinetic dynamometry (60). In various clinical settings,
isokinetic dynamometry combined with EMG has provided
more useful functional information on muscle strength capacity
compared with measurements of static muscle strength alone
(7,19). In patients with stroke, isokinetic dynamometry has
revealed deficits of muscle strength and neuromuscular
activation that are more pronounced during fast concentric
compared with static muscle contraction (19,38). Functionally,
concentric and eccentric muscle strength is more important
than static muscle strength, because most activities of daily living
occur during situations of dynamic muscle work. Collectively,
isokinetic dynamometry combined with EMG and percutaneous electrical muscle stimulation can be used to assess
adaptations in neural, muscular, and functional parameters in
response to physical training (6) and deconditioning (53).
The purpose of this study was to investigate the effect of
intensive physical rehabilitation with strength training and
body weight supported treadmill training (BWSTT) on
neuromuscular adaptations in outpatients suffering from
hemiparesis after stroke. We hypothesized that intensive
physical rehabilitation would increase neuromuscular activation (EMG amplitude) and enhance muscle contractile
properties (twitch torque) of the paretic limb compared with
the nonpateric limb, leading to increased voluntary muscle
strength during isokinetic and static contraction.
METHODS
Experimental Approach to the Problem
control leg was used. Outpatients with hemiparesis after
stroke participated in 12 weeks of intensive physical
rehabilitation comprising high-intensity strength training
with near-maximal loads and BWSTT. Strength training
was performed unilaterally with the paretic leg only (PAR).
The contralateral nonparetic leg was used as a control leg that
was tested but not resistance trained (CON). At baseline and
12-week follow-up, the patients went through testing
consisting of isokinetic muscle strength, neuromuscular
activation measured with EMG, electrically evoked muscle
twitch contractile properties, and gait performance (10-m
Walk Test and 6-min Walk Test).
Subjects
All the subjects had stroke in the chronic stage, that is, at least
6 months postinjury (Table 1). There was no upper limit for
the postinjury duration. Three of the 11 subjects had a right
hemisphere lesion. All brain lesions had been confirmed by
means of computed tomography or magnetic resonance
imaging. Inclusion criteria were chronicity (i.e., time since
injury) of .6 months, a moderate to severe hemiparesis
based on a clinical assessment by a physiotherapist on
volitional function of the upper and lower limbs, an age of at
least 16 years, moderate to severely impaired gait function
defined as covering less than two-thirds to one-half of
‘‘normal’’ gait distance for healthy age-, weight-, height-, and
sex-matched individuals (22) and that the subject was
mentally prepared to participate in the intervention. The
subjects were medically stable and generally independent
with regard to most basic activities of daily living. Alcohol or
substance abuse, psychiatric diseases, and any progressive
diseases were the exclusion criteria.
Before the intervention, the amount of training per week
with a physiotherapist varied considerably among subjects.
However, 82% had received rehabilitation training between
2 and 7 hwk21, and only 1 subject had not received
rehabilitation at all. This study received approval from the
local Ethics Committee (KF-01-240/04), and all the subjects
provided written informed consent before participation.
Procedures
For clarity, this section is subdivided into a description of the
12-week training intervention and then the physiological
measurements performed at baseline and follow-up.
TABLE 1. Demographics (mean 6 SE).
Age (y)
Weight (kg)
Height (m)
Time since injury (y)
Gender (men/women)
Side of lesion (right/left)
51 6 3.9
85 6 2.7
1.78 6 0.02
0.97 6 0.17
9/2
3/8
A within-subject repeated measures design with the paretic
leg as the experimental leg and the nonparetic leg as the
2
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Intervention
The physical training intervention took place at the gait
rehabilitation facility of the Center for Rehabilitation of Brain
Injury in Copenhagen, Denmark. The facility had been
especially equipped for the project that comprised 12 weeks
of training, 5 times 1.5 hwk21. The intervention comprised
4 key elements: (a) high-intensity strength training; (b)
BWSTT; (c) aerobic exercise; and (d) functional training.
The chief objective was to improve walking speed,
ambulatory safety, and maximum walking distance and to
enhance the maximal muscle strength. High-intensity
strength training was performed 3 dwk21, and aerobic
exercise and functional training were performed 2 times
a week. Each training session always began with BWSTT. All
the training was performed at the highest possible level of
voluntary intensity.
The strength training program consisted of the exercises:
semiseated leg press, hamstring curl, knee extension, and seated
leg press using TechnogymÒ Isotonic Line with Power
Control, offering visual feedback with regard to range of
motion and power output for each repetition and set. General
principles of strength training were applied (25). During the
initial week, the relative exercise loading was 12 repetition
maximum (RM), followed by 10RM loads during the second
week and heavier loads of 8RM during weeks 3–6, and then
increasing the number of repetitions again toward 12RM
during week 8 and gradually increasing the load and
decreasing the number of repetitions toward 4–8RM during
the final weeks. The progression schedule is summarized in
Table 2. All the subjects followed this progression schedule,
but some individual adjustments were necessary; for the
hamstring curl exercise, some of the subjects were not able to
lift the minimum weight concentrically during the initial
TABLE 2. Progression schedule for the 4 resistance
exercises (semiseated leg press, hamstring curl,
knee extension, and seated leg press) performed 3
times per week for 12 weeks.*
Week
1
2
3
4
5
6
7
8
9
10
11
12
RM
Sets per exercise
12, 12, 12
10, 10, 10
8, 8, 8
Functional training
8, 8, 8, 8
8, 8, 8, 8
12, 10, 10, 8
10, 8, 8, 8, 6
8, 6, 6, 6, 4
Functional training
10, 8, 8, 6
8, 6, 6, 4
3
3
3
*RM = repetitions maximum load.
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training sessions and thus had to start by isometric holds or
eccentric lowering. Range of joint motion was gradually
increased through the intervention as strength and flexibility
improved. Three to 5 sets of each exercise were performed
with rest periods of 90 seconds between sets. The subjects
were instructed to exert full intentional acceleration of each
repetition regardless of external load and actual movement
velocity. Strength training was performed unilaterally to
ensure the highest possible training intensity for the paretic leg.
Body weight supported treadmill training was performed
for up to 25 minutes at the beginning of each training session,
typically consisting of 3 gait periods of 6–8 minutes each,
interspersed by a short rest period. A continuous high pace
was used during the first period. To promote contralateral
armswing and balance, this period was performed without
holding on to the bar of the treadmill. Therapists offered
discreet manual guiding when necessary. Interval training was
used during second gait period, consisting of 1-minute
intervals at the highest speed possible alternating with
1-minute intervals at slightly lower speed. This period was
preferably performed without bar support and also offered
discreet manual guiding if necessary. The third gait period was
individually adapted to more specific requirements such as
weight bearing, knee control, cadence, etc., the goal often
being to challenge the cardiorespiratory system by increasing
the treadmill gradient up to 10%. Body weight support varied
from 10 to 25 kg and was determined by assessing the amount
of support that would enhance optimum gait quality.
Treadmill speed, intervals, gradient, and dosage were
evaluated on a daily basis and increased whenever possible.
Aerobic activities besides BWSTT were performed twice
a week and consisted of stationary bipedal and unipedal
cycling (TechnoGymÒ Bikerace HC600), unipedal armcycling (TechnoGymÒ XT PRO Top600), and body weight
supported stair climbing (TechnoGymÒ Steprace HC300). It
was strived to gradually maximize the heart rate and increase
the power output in each activity.
Functional training (weeks 4 and 10, Table 2) was
individually adjusted, the goal being to ensure optimum
carryover from functional improvements to activities of daily
living. Functional training comprised training of specific
details of the gait pattern, gait training in a nonclinical setting,
stair climbing, etc.
Dynamometry
4
4
4
5
5
4
4
A KinCom dynamometer was used for the testing of
isokinetic and static maximal voluntary muscle strength of
the knee extensors (quadriceps) and knee flexors (hamstrings)
(Kinetics Communicator, Chattecx Corp., Chattanooga, TN,
USA). Unilateral measurements of PAR and CON were
performed separately. Verbal encouragement and visual
feedback on a computer screen were provided during all
the contractions. After warm-up and preconditioning, 4
maximal attempts interspersed by rest periods of 60 seconds
were performed during slow and fast concentric contraction
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Rehabilitation of Stroke
(30 and 240°s21, respectively), slow eccentric contraction
(30°s21) for the quadriceps and hamstrings separately (5).
Initial testing showed that for the hamstrings, the fast
concentric contraction at 240°s21 was unfeasible and was
therefore disregarded for the remaining subjects. Further, 4
maximal voluntary static muscle contractions were performed at a knee joint angle of 70° for the quadriceps and
hamstring separately. All torque and position signals were
sampled synchronously at 1,000 Hz using a 16-bit A/Dconverter (dt-9804, Data translation, Marlboro, MA, USA)
and stored on a stationary computer for further analysis.
During off-line analysis, the dynamometer force and lever arm
position signal was digitally lowpass filtered at 15- and 8-Hz
cut-off frequencies, respectively. Subsequently, the torque
signal was corrected for the effect of gravity on the lower leg
and foot (2). The average torque exerted in the 60–80° range
of knee joint motion for each type of contraction was used for
the further statistical analyses. The rationale for choosing this
knee joint angle interval was that the highest torque occurred
in this particular range of motion.
Noorizadeh et al. have previously shown that isokinetic
strength measures are highly reliable in patients with stroke
(intraclass correlation coefficient = 0.85–0.98) (42).
Electromyography
Neuromuscular activation was assessed by simultaneous
recording of EMG from the quadriceps and hamstring
muscles during the dynamometer test described above. After
shaving and cleaning the skin with ethanol, bipolar surface
EMG electrodes (Medicotest M-00-S, Medicotest, Ølstykke,
Denmark) were placed on the medial portion of the 3
superficial heads of the quadriceps femoris (i.e., vastus
lateralis, vastus medialis, rectus femoris) and hamstring
muscles (i.e., biceps femoris and semitendinosus). If impedance was .10 kV, the procedure was repeated. Care was
taken to place EMG electrodes at identical positions on both
legs, and the exact electrode positions were registered and
used during the subsequent posttraining test. The EMG
electrodes were connected directly to small preamplifiers
located 10 cm from the recording site. The signals were led
through shielded wires to custom-built differential instrumentation amplifiers, with a bandwidth of 10–10,000 Hz and
a common mode rejection ratio .100 dB and sampled at
1,000 Hz (5). During the process of off-line analysis, all raw
EMG signals were digitally high-pass filtered at a cut-off
frequency of 10 Hz using a fourth-order zero phase lag
Butterworth filter (60). The EMG signal was then passed
through a symmetric moving root mean square filter with
a time constant of 20 milliseconds and averaged in the 60–80°
knee joint angle interval for the isokinetic contractions and
averaged over the peak 500 milliseconds of the static
contractions at 70°. Quadriceps EMG amplitude was
determined as the average of vastus lateralis, vastus medialis,
and rectus femoris. Correspondingly, hamstring EMG
amplitude was determined as the average of biceps femoris
and semitendinosus. All the analyses of torque and EMG
were performed using custommade macros developed in
Matlab 7.5 (MathWorks, Natick, MA, USA) and Visual Basic
for Applications (Microsoft Corp., Microsoft Danmark ApS,
Hellerup, Denmark).
Figure 1. Normalized knee extensor torque and quadriceps electromyography (EMG) amplitude at pretraining and posttraining. *, **p , 0.05 and 0.01,
respectively, pretraining to posttraining.
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Electrically Evoked Muscle Twitch Contractile Properties
Electrically evoked muscle contractile properties of the
resting quadriceps of PAR and CON were determined
according to a procedure previously described in healthy
subjects (6). Briefly, surface stimulation electrodes (Bioflex,
model PE3590) were placed over the distal and proximal
muscle belly of the largest head of the quadriceps femoris,
that is, vastus lateralis. Care was taken to place the
stimulation electrodes at identical positions on both legs,
and the exact positions were registered and used during the
subsequent posttraining test. Twitch contractions were
evoked on the resting muscle using electrical stimulation
consisting of single square wave pulses of a 0.1-millisecond
duration delivered by a direct current stimulator (Digitimer
Electronics, model DS7) while at the same time measuring
knee extensor torque. Stepwise increments in current were
delivered, separated by rest periods of 30 seconds, until no
further increase in torque was seen (30), and subsequently 3
maximal twitch contractions were obtained. Twitch peak
torque and time to peak tension of the maximal twitches
were used for further statistical analyses.
Gait Performance
Gait speed was evaluated using a 10-m Walk Test. The
subjects were instructed to walk the distance as fast as
possible, starting from static. Gait endurance was evaluated
with a 6-min Walk Test on a 50-m track. The subjects were
instructed to walk as far as possible in 6 minutes, and
subsequently the distance was measured. The subjects used
their habitual assistive devices during the test. When possible,
the subjects were requested to walk without support from an
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elbow crutch or cane. This test was performed on a separate
day by the physiotherapists of this study.
Statistical Analyses
Friedman’s 2-way analysis of variance by ranks for related
samples was performed in SAS version 9 to locate differences
from pretraining to posttraining for torque and EMG of the
quadriceps and hamstring muscles and to locate the differences across contraction modes and velocities. Spearman’s
correlation coefficient was determined between the baseline
variables and between the training-induced change in torque
and EMG. In addition to absolute values, the torque and
EMG amplitude of PAR was expressed as a percentage of
CON to compare the relative deficit between muscles,
contraction modes, and velocities. A value of p # 0.05 was
chosen as statistically significant, and results are reported as
mean 6 SE unless otherwise stated.
RESULTS
After the 12-week intervention period, changes in muscle
strength and EMG activity were observed solely in PAR.
Normalized values of torque and EMG amplitude for PAR are
given in Figures 1 and 2 (i.e., expressed as a percentage of
CON), and absolute values for PAR and CON are provided in
Table 3.
Baseline Observations
At baseline, torque and quadriceps EMG during knee
extension and torque and hamstring EMG during knee
flexion were significantly lower in PAR compared with
those in CON during all contraction modes and velocities
Figure 2. Normalized knee flexor torque and hamstrings electromyography (EMG) amplitude at pretraining and posttraining. *, **p , 0.05 and 0.01, respectively,
pretraining to posttraining.
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Rehabilitation of Stroke
TABLE 3. Isokinetic and static muscle strength for the knee extensors (quadriceps) and knee flexors (hamstrings) and
electrically evoked twitch peak torque and TPT at preintervention and postintervention for the PAR and CON.
Maximal voluntary contraction
Quadriceps
Velocity (°s21)
PAR
Pre
Post
CON
Pre
Post
230
0
30
240
230
0
30
240
230
0
30
240
230
0
30
240
Torque (Nm)
112 6
125 6
74 6
17 6
147 6
157 6
108 6
21 6
164 6
191 6
131 6
82 6
159 6
193 6
144 6
67 6
12
17
11
5
14†
20§
12§
5
16
21
16
12
18
24
16
13
Hamstrings
EMG (mV)
100 6
112 6
81 6
71 6
137 6
132 6
134 6
85 6
173 6
203 6
175 6
281 6
193 6
220 6
211 6
270 6
Twitch contraction
12
14
11
14
22‡
22
22†
15
24
29
35
41
31
28
34
57
Torque (Nm)
EMG (mV)
Quadriceps
Torque (Nm)
TPT (ms)
12 6 5
21 6 6
462
21 6 8
18 6 3
13 6 6
21 6 2.3
86 6 3.0
24 6 6§
30 6 8§
15 6 4‡
45 6 12§
27 6 8
34 6 7§
31 6 2.4†
89 6 2.0
77 6 10
79 6 9
56 6 6
148 6 35
145 6 32
132 6 24
24 6 3.1
85 6 2.5
73 6 12
80 6 12
59 6 9
152 6 28
145 6 24
163 6 20
28 6 3.1
87 6 2.8
*TPT = time to peak tension; PAR = paretic; CON = nonparetic control leg; EMG = electromyography.
†p , 0.05 pretraining to posttraining.
‡p , 0.01 pretraining to posttraining.
§p , 0.001, pretraining to posttraining.
(p , 0.001) (Table 3). Normalized torque and EMG were
significantly lower during knee flexion compared with knee
extension during all contraction modes (compare Figures 1
and 2) (p , 0.0001).
When comparing across velocities, normalized torque and
quadriceps EMG were markedly lower during fast concentric
knee extension compared with slow eccentric, static, and slow
concentric contraction (p , 0.0001) (both at pretraining and
posttraining, Figures 1A and B).
Participation and Training Load
Thirty strength training sessions were planned during the
12-week intervention period. The actual number of strength
training sessions was 29 6 1.0. The training load was
increased in a linear fashion and was more than doubled
during the 12 weeks, which confirmed the high level of
participation. From the initial to the final week of training, the
unilateral load for PAR increased from 39 6 4.4 to 86 6 11 kg
for seated leg press, from 17 6 2.5 to 36 6 4.4 kg for knee
extension, from 47 6 3.9 to 98 6 7.1 kg for semiseated leg
press, and from 15 6 1.9 to 28 6 3.0 for hamstring curls.
Although not measured, the actual muscle load was probably
increased even more than the nominal training load because
the range of joint motion was increased as strength and
flexibility improved. The average progression in training load
for 2 of the exercises is given in Figure 3.
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Intervention, Knee Extension (Quadriceps)
In PAR, normalized knee extensor torque increased significantly in response to the intervention during all the
contraction modes and velocities (Figure 1A); slow eccentric
from 72 6 6.2 to 99 6 9.2% (p , 0.05), static from 67 6 8.3 to
84 6 9.2% (p , 0.01), slow concentric from 62 6 9.2 to 78 6
7.8% (p , 0.01), and fast concentric from 19 6 4.3 to 33 6
7.1% (p , 0.05). Absolute knee extensor torque increased
during slow eccentric, static, and slow concentric contraction
(p , 0.01–0.001) (Table 3).
Significant increases in normalized quadriceps EMG
amplitude were seen during slow eccentric contraction
(from 61 6 7.0 to 83 6 11%, p , 0.05) and slow concentric
contraction (from 59 6 9.0 to 69 6 8.8%, p , 0.01) (Figure 1B).
Increased quadriceps EMG amplitude was significantly
correlated to increased knee extensor torque during
slow eccentric (r = 0.75, p , 0.01) and slow concentric
contraction (r = 0.84, p , 0.01). Absolute quadriceps EMG
amplitude increased during slow eccentric and slow
concentric contraction (p , 0.05–0.001) (Table 3).
Intervention, Knee Flexion (Hamstrings)
In PAR, normalized knee flexor torque increased significantly
during all the contraction modes and velocities (Figure 2A);
slow eccentric torque from 14 6 5.9 to 50 6 21% (p , 0.01),
static from 31 6 9.4 to 44 6 13% (p , 0.01), and slow
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(p , 0.05) and increased significantly with training from 92 6
4.9 to 115 6 6.4% (p , 0.001). The posttraining value of
115 6 6.4% was significantly higher in PAR compared with
that in CON (p , 0.05). Twitch time to peak tension was not
significantly different between PAR and CON and remained
unchanged from pretraining to posttraining (101 6 3.6 vs.
103 6 2.0%). Absolute values are provided in Table 3.
Gait Performance
From pretraining to posttraining, gait speed (10 meter walk
test) increased 52% from 0.89 6 0.14 to 1.35 6 0.12 ms21, and
gait endurance (6 minute walk test) increased 68% from
250 6 30 to 420 6 43 m (corresponding to an average gait
speed of 0.69 6 0.08 to 1.17 6 0.12 ms21) (p , 0.001).
Relative to ‘‘normal’’ gait distance covered during a 6-MWT in
healthy age-, weight-, height-, and sex-matched individuals
(22), this corresponded to 42 6 4.0% at pretraining and
70 6 4.5% at posttraining.
DISCUSSION
Figure 3. Unilateral training load for the paretic leg during 2 of the 4
resistance training exercises (leg press and hamstring curls) over the
12-week intervention period.
concentric from 6.3 6 3.4 to 34 6 15% (p , 0.05). Absolute
knee flexor torque increased during slow eccentric, static, and
slow concentric contraction (p , 0.05–0.01) (Table 3).
Significant increases in normalized hamstring EMG
amplitude were seen only during the slow dynamic
contractions (Figure 2B); slow eccentric from 16 6 7.0 to
43 6 13% (p , 0.05), and slow concentric from 11 6 5.5 to
32 6 8.5% (p , 0.01). Absolute hamstring EMG amplitude
increased during slow eccentric and slow concentric
contractions (p , 0.01) (Table 3).
Electrically Evoked Muscle Contractile Properties
At baseline, twitch peak torque of the resting quadriceps
was significantly lower in PAR compared with that in CON
The main findings of this study are that intensive physical
rehabilitation with unilateral strength training of the paretic
limb combined with BWSTT improves the neuromuscular
activation of agonist muscles and enhances twitch torque,
leading to increased strength during maximal voluntary
eccentric, concentric and static contraction. Together, these
findings show that persons with hemiparesis after stroke can
get clinically relevant improvements of neural and muscular
function in response to intensive physical rehabilitation.
Several interesting observations were made at baseline
before the intervention. The baseline correlations of this study
validate that the reduced neuromuscular activation is primarily
responsible for muscle weakness (20,26,28). However, with the
technique of percutaneous electrical stimulation of the resting
quadriceps, we further showed that muscle twitch torque is
impaired in the paretic leg compared with that in the
nonparetic control leg. The twitch torque deficit of 8% during
electrical stimulation was relatively small compared with the
neural deficit of 40% during maximal voluntary static
contraction. Nevertheless, this result shows that the intrinsic
contractile strength of the muscle is negatively affected after
long-term hemiparesis, which is in agreement with the
findings of a previous study (56). These findings are in line
with the observations that long-term hemiparesis can lead to
muscular atrophy of the paretic limb (35,49).
Another interesting finding at baseline was the severe
weakening of the hamstrings. For instance, muscle strength
during slow concentric knee flexion of the paretic leg was only
6% of the nonparetic control leg. This may partly explain the
common observation of awkward gait pattern in persons with
hemiparesis, that is, the knee is barely flexed and the leg is
swung in a circumductory fashion from the hip with the pelvis
tilted upward and the hip abducted. Thus, special attention
should be paid to increased hamstring activation during
rehabilitation. Although not specifically investigated in this
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Rehabilitation of Stroke
study, it should also be noted that hip and plantar flexor
strength are considered important for normal gait as well (62).
In line with previous observations (19,38), muscle strength
and EMG were more heavily impaired during rapid
compared with slow muscle contraction, which may explain
the inert movement pattern of this patient group. Although
fast concentric knee extensor strength (quadriceps) was only
19% of the nonparetic control leg, fast concentric knee flexor
strength (hamstrings) was minimal (;0%). At baseline, the
highest level of neuromuscular activation of the hamstrings
was achieved during static contraction, which can be
a starting point for the practical strength training, that is,
static holds and then slowly lowering the weight eccentrically. This method was implemented during the initial
training sessions in those subjects who could not lift the
minimal weight concentrically during the knee flexion
exercise. Clark et al. showed a higher preservation of
eccentric compared with concentric knee extensor torque
after stroke and suggested the implementation of eccentric
contractions during rehabilitation (19). This study extends
these findings by showing a severe weakening of eccentric
knee flexor torque (i.e., hamstrings), despite preserved eccentric knee extensor torque (i.e., quadriceps). Thus, although
concentric and eccentric contractions may be feasible during
rehabilitation of the quadriceps, static contractions followed by
eccentric contraction may be more appropriate during
rehabilitation of severely weakened hamstrings.
This study highlights that persons with hemiparesis are
able to complete an intensive physical training intervention
and make progression in training loads comparable with that
previously observed in healthy individuals (6,8). Thus,
training load increased in a linear fashion throughout the
intervention and did not plateau within 12 weeks, indicating
further potential for improvement.
In response to the 12-week training intervention, both EMG
amplitude and intrinsic contractile strength (i.e., twitch torque)
of the paretic leg were enhanced, leading to increased voluntary
muscle strength. Although general increases in torque and
EMG were observed, the most consistent gains—in terms of
both torque and EMG—were found during slow concentric and
eccentric contraction. This was consistent for both knee
extension and flexion. This resulted in an altered shape of the
torque-velocity and EMG-velocity curves, that is, the most
pronounced gains occurred during slow concentric and slow
eccentric contractions. These findings reflect the velocity
specificity of neural adaptations (10), that is, strength training
was performed with heavy loads and consequently relatively
slow external movement speeds of approximately 60–120°s21,
which may have facilitated gains in the neural drive relatively
more during slow contractions than during static and fast
contraction. In line with the present findings, a previous study
reported increased EMG amplitude of the quadriceps after
isokinetic strength training (21). However, the generalizability
of that study may be limited because of learning effects owing
to the identical conditions of training and testing (48).
8
the
As in this study, training-induced changes in EMG
amplitude are commonly used to estimate the changes in
neuromuscular activation. However, it should be noted that
the EMG signal may be affected by confounding factors, for
example, changes in muscle architecture and subcutaneous
fatty tissue with training, skin conductance, EMG electrode
placement, etc. Despite the inherent variance associated with
EMG measurements, the amplitude of the EMG signal is
roughly related to muscle force (32), expressing a combination
of recruitment, rate coding, and synchronization of motor
units (23). In this study, correlation analyses confirmed
a strong relation between training-induced changes in torque
and EMG during slow concentric and slow eccentric
contraction (r = 0.75–0.84). Similarly, in healthy young men
and in women with chronic neck muscle pain, a moderate to
strong association exists between increased EMG amplitude
and gains in slow eccentric and slow concentric muscle
strength in response to strength training (4,5). Together, these
findings support that the changes in EMG amplitude represent
a fair estimate of the changes in neuromuscular activation.
Although improvements of neuromuscular activation
were significant only at the slow concentric and eccentric
contractions in this study, strength gains were observed
throughout the whole range of contraction modes and
velocities, indicating that adaptations in intrinsic contractile
strength positively influenced voluntary strength gains as
well. As a novel finding, we showed that electrically evoked
twitch torque of the paretic muscle relatively to the homologous nonparetic control muscle was enhanced 23% by
strength training. After the intervention period, twitch peak
torque of the paretic leg even exceeded that of the
nonparetic control leg. This finding indicates gross muscular
hypertrophy and adaptations at the muscle cellular level, as
also seen in healthy subjects doing lower-body strength
training of similar type, volume, intensity, and duration (6,8).
This finding may also reflect training-induced adaptations
of sarcoplasmic reticulum Ca2+ kinetics (44). Time to peak
tension remained unchanged, indicating unaltered relative
proportion of type I and II muscle fibers (31). Future studies
should evaluate the impact of high-intensity strength
training on muscle cellular adaptations in this population.
The intervention led to improved gait performance, as
evidenced by a 52 and 68% increase in gait speed and gait
endurance, respectively. Although some studies found no
additional effect of strength training on gait performance
(27,36,39), others have reported between 6 and 30% increase
in gait speed (50,54,55) and 12–23% increase in gait
endurance (43,54). In this study, both gait speed and gait
endurance were positively affected by the rehabilitation
program. A systematic review concluded that gait-oriented
training is effective in improving gait performance after
stroke (57). The marked improvement in gait performance in
this study may be caused by a combination of gait-oriented
functional training, BWSTT, other aerobic activities, and
unilateral strength training.
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the
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In conclusion, this study demonstrated that intensive
physical rehabilitation comprising unilateral strength training
and BWSTTof persons with hemiparesis after stroke can lead
to clinically relevant improvements of neuromuscular
activation of agonist muscles and enhancement of intrinsic
contractile strength, leading to increased voluntary strength
during a wide range of contraction modes and velocities. The
overall efficacy of the rehabilitation program was further
reflected in improved gait speed and gait endurance.
Together, these results show a promising potential toward
achieving functional independence in activities of daily living
in this population.
PRACTICAL APPLICATIONS
Our study shows that high-intensity strength training can be
implemented successfully in rehabilitation programs for
patients with hemiparesis after stroke. Using heavy loads of
4–12RM 3 times a week in a periodized and progressive
manner—quite similar to that used in healthy individuals—patients with stroke can partially regain muscle strength
and gait function in 12 weeks. Particular attention should be
paid to regaining hamstring strength because our study
showed severe weakening of this muscle group at baseline.
Strength training coaches working in the field of rehabilitation can use this knowledge to safely and efficiently add
high-intensity strength training to existing rehabilitation
paradigms.
ACKNOWLEDGMENTS
Rehabilitation at the Center for Rehabilitation of Brain
Injury was financed by the municipality of Copenhagen.
Physiological testing was financed by grants from the Danish
National Research Foundation (J. nr. 504–14).
REFERENCES
1. Aagaard, P. Training-induced changes in neural function. Exerc Sport
Sci Rev 31: 61–67, 2003.
2. Aagaard, P, Simonsen, EB, Trolle, M, Bangsbo, J, and Klausen, K.
Isokinetic hamstring/quadriceps strength ratio: Influence from joint
angular velocity, gravity correction and contraction mode. Acta
Physiol Scand 154: 421–427, 1995.
3. Adams, RW, Gandevia, SC, and Skuse, NF. The distribution of
muscle weakness in upper motoneuron lesions affecting the lower
limb. Brain 113: 1459–1476, 1990.
4. Andersen, LL, Andersen, CH, Zebis, MK, Nielsen, PK, Sogaard, K,
and Sjogaard, G. Effect of physical training on function of
chronically painful muscles: A randomized controlled trial. J Appl
Physiol 105: 1796–1801, 2008.
5. Andersen, LL, Andersen, JL, Magnusson, SP, and Aagaard, P.
Neuromuscular adaptations to detraining following resistance
training in previously untrained subjects. Eur J Appl Physiol 93:
511–518, 2005.
6. Andersen, LL, Andersen, JL, Magnusson, SP, Suetta, C, Madsen, JL,
Christensen, LR, and Aagaard, P. Changes in the human muscle
force-velocity relationship in response to resistance training and
subsequent detraining. J Appl Physiol 99: 87–94, 2005.
7. Andersen, LL, Nielsen, PK, Sogaard, K, Andersen, CH, Skotte, J, and
Sjogaard, G. Torque-EMG-velocity relationship in female workers
with chronic neck muscle pain. J Biomech 41: 2029–2035, 2008.
| www.nsca-jscr.org
8. Andersen, LL, Tufekovic, G, Zebis, MK, Crameri, RM, Verlaan, G,
Kjaer, M, Suetta, C, Magnusson, P, and Aagaard, P. The effect of
resistance training combined with timed ingestion of protein on
muscle fiber size and muscle strength. Metabolism 54: 151–156, 2005.
9. Badics, E, Wittmann, A, Rupp, M, Stabauer, B, and Zifko, UA.
Systematic muscle building exercises in the rehabilitation of stroke
patients. NeuroRehabilitation 17: 211–214, 2002.
10. Behm, DG and Sale, DG. Velocity specificity of resistance training.
Sports Med 15: 374–388, 1993.
11. Bohannon, RW. Knee extension strength and body weight determine sit-to-stand independence after stroke. Physiother Theory
Pract 23: 291–297, 2007.
12. Bohannon, RW and Andrews, AW. Relationships between impairments in strength of limb muscle actions following stroke. Percept
Mot Skills 87: 1327–1330, 1998.
13. Bohannon, RW and Walsh, S. Nature, reliability, and predictive value
of muscle performance measures in patients with hemiparesis
following stroke. Arch Phys Med Rehabil 73: 721–725, 1992.
14. Bourbonnais, D, Bilodeau, S, Lepage, Y, Beaudoin, N, Gravel, D, and
Forget, R. Effect of force-feedback treatments in patients with
chronic motor deficits after a stroke. Am J Phys Med Rehabil 81:
890–897, 2002.
15. Buchner, DM, Beresford, SA, Larson, EB, LaCroix, AZ, and
Wagner, EH. Effects of physical activity on health status in older adults.
II. Intervention studies. Annu Rev Public Health 13: 469–488, 1992.
16. Butler, M, Norton, R, Lee-Joe, T, and Coggan, C. Preventing falls and
fall-related injuries among older people living in institutions: Current
practice and future opportunities. N Z Med J 111: 359–361, 1998.
17. Canning, CG, Ada, L, Adams, R, and O’Dwyer, NJ. Loss of strength
contributes more to physical disability after stroke than loss of
dexterity. Clin Rehabil 18: 300–308, 2004.
18. Carin-Levy, G, Greig, C, Young, A, Lewis, S, Hannan, J, and Mead, G.
Longitudinal changes in muscle strength and mass after acute stroke.
Cerebrovasc Dis 21: 201–207, 2006.
19. Clark, DJ, Condliffe, EG, and Patten, C. Activation impairment alters
muscle torque-velocity in the knee extensors of persons with poststroke hemiparesis. Clin Neurophysiol 117: 2328–2337, 2006.
20. Davies, JM, Mayston, MJ, and Newham, DJ. Electrical and
mechanical output of the knee muscles during isometric and
isokinetic activity in stroke and healthy adults. Disabil Rehabil 18:
83–90, 1996.
21. Engardt, M, Knutsson, E, Jonsson, M, and Sternhag, M. Dynamic
muscle strength training in stroke patients: Effects on knee extension
torque, electromyographic activity, and motor function. Arch Phys
Med Rehabil 76: 419–425, 1995.
22. Enright, PL and Sherrill, DL. Reference equations for the sixminute walk in healthy adults. Am J Respir Crit Care Med 158:
1384–1387, 1998.
23. Farina, D, Merletti, R, and Enoka, RM. The extraction of neural
strategies from the surface EMG. J Appl Physiol 96: 1486–1495, 2004.
24. Flansbjer, UB, Miller, M, Downham, D, and Lexell, J. Progressive
resistance training after stroke: Effects on muscle strength, muscle
tone, gait performance and perceived participation. J Rehabil Med
40: 42–48, 2008.
25. Fleck, SJ and Kraemer, WJ. Designing Resistance Training Programs.
Champaign, IL: Human Kinetics, 2004.
26. Frontera, WR, Grimby, L, and Larsson, L. Firing rate of the lower
motoneuron and contractile properties of its muscle fibers after
upper motoneuron lesion in man. Muscle Nerve 20: 938–947, 1997.
27. Glasser, L. Effects of isokinetic training on the rate of
movement during ambulation in hemiparetic patients. Phys Ther 66:
673–676, 1986.
28. Gowland, C, deBruin, H, Basmajian, JV, Plews, N, and Burcea, I.
Agonist and antagonist activity during voluntary upper-limb
movement in patients with stroke. Phys Ther 72: 624–633, 1992.
VOLUME 0 | NUMBER 0 | MONTH 2011 |
9
Copyright © National Strength and Conditioning Association Unauthorized reproduction of this article is prohibited.
Rehabilitation of Stroke
29. Harridge, SD. Plasticity of human skeletal muscle: Gene expression
to in vivo function. Exp Physiol 92: 783–797, 2007.
30. Harridge, SD, Bottinelli, R, Canepari, M, Pellegrino, MA, Reggiani, C,
Esbjornsson, M, and Saltin, B. Whole-muscle and single-fibre
contractile properties and myosin heavy chain isoforms in humans.
Pflugers Arch 432: 913–920, 1996.
31. Harridge, SD, Bottinelli, R, Canepari, M, Pellegrino, MA, Reggiani, C,
Esbjornsson, M, and Saltin, B. Whole-muscle and single-fibre
contractile properties and myosin heavy chain isoforms in humans.
Pflugers Arch 432: 913–920, 1996.
32. Jensen, C, Vasseljen, O, and Westgaard, RH. The influence of
electrode position on bipolar surface electromyogram recordings of
the upper trapezius muscle. Eur J Appl Physiol Occup Physiol 67:
266–273, 1993.
33. Jorgensen, HS, Nakayama, H, Raaschou, HO, Vive-Larsen, J, Stoier, M,
and Olsen, TS. Outcome and time course of recovery in stroke. Part I:
Outcome. The Copenhagen Stroke Study. Arch Phys Med Rehabil 76:
399–405, 1995.
34. Jorgensen, HS, Nakayama, H, Raaschou, HO, Vive-Larsen, J, Stoier, M,
and Olsen, TS. Outcome and time course of recovery in stroke. Part II:
Time course of recovery. The Copenhagen Stroke Study. Arch Phys
Med Rehabil 76: 406–412, 1995.
35. Jorgensen, L and Jacobsen, BK. Changes in muscle mass, fat mass,
and bone mineral content in the legs after stroke: A 1 year
prospective study. Bone 28: 655–659, 2001.
36. Kim, CM, Eng, JJ, MacIntyre, DL, and Dawson, AS. Effects of
isokinetic strength training on walking in persons with stroke: A
double-blind controlled pilot study. J Stroke Cerebrovasc Dis 10:
265–273, 2001.
37. Lopez-Yunez, AM. The management of stroke patients by
neurologists: Common questions and new observations. Semin Neurol
22: 53–61, 2002.
38. Lum, PS, Patten, C, Kothari, D, and Yap, R. Effects of velocity on
maximal torque production in poststroke hemiparesis. Muscle Nerve
30: 732–742, 2004.
39. Moreland, JD, Goldsmith, CH, Huijbregts, MP, Anderson, RE,
Prentice, DM, Brunton, KB, O’Brien, MA, and Torresin, WD.
Progressive resistance strengthening exercises after stroke: A singleblind randomized controlled trial. Arch Phys Med Rehabil 84:
1433–1440, 2003.
40. Murray, CJ and Lopez, AD. Mortality by cause for eight regions
of the world: Global Burden of Disease Study. Lancet 349:
1269–1276, 1997.
41. Nadeau, S, Arsenault, AB, Gravel, D, and Bourbonnais, D. Analysis
of the clinical factors determining natural and maximal gait speeds in
adults with a stroke. Am J Phys Med Rehabil 78: 123–130, 1999.
42. Noorizadeh, DS, Talebian, S, Olyaei, G, and Montazeri, A. Reliability
of isokinetic normalized peak torque assessments for knee muscles in
post-stroke hemiparesis. Gait Posture 27: 715–718, 2008.
43. Olney, SJ, Nymark, J, Brouwer, B, Culham, E, Day, A, Heard, J,
Henderson, M, and Parvataneni, K. A randomized controlled trial of
supervised versus unsupervised exercise programs for ambulatory
stroke survivors. Stroke 37: 476–481, 2006.
44. Ortenblad, N, Lunde, PK, Levin, K, Andersen, JL, and Pedersen, PK.
Enhanced sarcoplasmic reticulum Ca(2+) release following intermittent sprint training. Am J Physiol Regul Integr Comp Physiol 279:
R152–R160, 2000.
45. Ouellette, MM, LeBrasseur, NK, Bean, JF, Phillips, E, Stein, J,
Frontera, WR, and Fielding, RA. High-intensity resistance training
improves muscle strength, self-reported function, and disability in
long-term stroke survivors. Stroke 35: 1404–1409, 2004.
10
the
46. Patten, C, Lexell, J, and Brown, HE. Weakness and strength training
in persons with poststroke hemiplegia: Rationale, method, and
efficacy. J Rehabil Res Dev 41: 293–312, 2004.
47. Rosamond, W, Flegal, K, Furie, K, Go, A, Greenlund, K, Haase, N,
Hailpern, SM, Ho, M, Howard, V, Kissela, B, Kittner, S, Lloyd-Jones, D,
McDermott, M, Meigs, J, Moy, C, Nichol, G, O’Donnell, C, Roger, V,
Sorlie, P, Steinberger, J, Thom, T, Wilson, M, and Hong, Y. Heart
disease and stroke statistics—2008 update: A report from the American
Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 117: e25–e146, 2008.
48. Rutherford, OM and Jones, DA. The role of learning and
coordination in strength training. Eur J Appl Physiol Occup Physiol 55:
100–105, 1986.
49. Ryan, AS, Dobrovolny, CL, Smith, GV, Silver, KH, and Macko, RF.
Hemiparetic muscle atrophy and increased intramuscular fat in
stroke patients. Arch Phys Med Rehabil 83: 1703–1707, 2002.
50. Sharp, SA and Brouwer, BJ. Isokinetic strength training of the
hemiparetic knee: Effects on function and spasticity. Arch Phys Med
Rehabil 78: 1231–1236, 1997.
51. Sinkjaer, T and Magnussen, I. Passive, intrinsic and reflex-mediated
stiffness in the ankle extensors of hemiparetic patients. Brain 117:
355–363, 1994.
52. Skelton, DA and Beyer, N. Exercise and injury prevention in older
people. Scand J Med Sci Sports 13: 77–85, 2003.
53. Suetta, C, Aagaard, P, Magnusson, SP, Andersen, LL, Sipila, S,
Rosted, A, Jakobsen, AK, Duus, B, and Kjaer, M. Muscle size,
neuromuscular activation, and rapid force characteristics in elderly
men and women: Effects of unilateral long-term disuse due to hiposteoarthritis. J Appl Physiol 102: 942–948, 2007.
54. Sullivan, KJ, Brown, DA, Klassen, T, Mulroy, S, Ge, T, Azen, SP, and
Winstein, CJ. Effects of task-specific locomotor and strength training
in adults who were ambulatory after stroke: Results of the STEPS
randomized clinical trial. Phys Ther 87: 1580–1602, 2007.
55. Teixeira-Salmela, LF, Olney, SJ, Nadeau, S, and Brouwer, B. Muscle
strengthening and physical conditioning to reduce impairment and
disability in chronic stroke survivors. Arch Phys Med Rehabil 80:
1211–1218, 1999.
56. Tsuji, I and Nakamura, R. Prolonged tension lag time of knee
extensor muscle on twitch contraction in patients with spastic
hemiparesis. Tohoku J Exp Med 156: 33–37, 1988.
57. van de Port, I, Wood-Dauphinee, S, Lindeman, E, and Kwakkel, G.
Effects of exercise training programs on walking competency
after stroke: A systematic review. Am J Phys Med Rehabil 86:
935–951, 2007.
58. Weiss, A, Suzuki, T, Bean, J, and Fielding, RA. High intensity
strength training improves strength and functional performance after
stroke. Am J Phys Med Rehabil 79: 369–376, 2000.
59. Winstein, CJ, Rose, DK, Tan, SM, Lewthwaite, R, Chui, HC, and
Azen, SP. A randomized controlled comparison of upperextremity rehabilitation strategies in acute stroke: A pilot study
of immediate and long-term outcomes. Arch Phys Med Rehabil 85:
620–628, 2004.
60. Winter, DA. Biomechanics and Motor Control of Human Movement.
New York, NY: John Wiley & Sons, 1990. pp. 11–50.
61. Wolfe, CD. The impact of stroke. Br Med Bull 56: 275–286, 2000.
62. Yang, YR, Wang, RY, Lin, KH, Chu, MY, and Chan, RC. Taskoriented progressive resistance strength training improves muscle
strength and functional performance in individuals with stroke. Clin
Rehabil 20: 860–870, 2006.
63. Zorowitz, RD, Gross, E, and Polinski, DM. The stroke survivor.
Disabil Rehabil 24: 666–679, 2002.
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