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Neurorehabilitation and

Neural Repair
Volume 23 Number 2
February 2009 184-190
© 2009 The American Society of
Motor Training of Upper Extremity With Functional Neurorehabilitation
10.1177/1545968308324548

Electrical Stimulation in Early Stroke Rehabilitation http://nnr.sagepub.com


hosted at
http://online.sagepub.com

Sabine Mangold, PhD, Corina Schuster, MPTSc, Thierry Keller, PhD,


Andrea Zimmermann-Schlatter, MPTSc, and Thierry Ettlin, MD

Background. Functional electrical stimulation (FES) allows active exercises in stroke patients with upper extremity paralysis. Objective.
To investigate the effect of motor training with FES on motor recovery in acute and subacute stroke patients with severe to complete arm
and/or hand paralysis. Methods. For this pilot study, 23 acute and subacute stroke patients were randomly assigned to the intervention
(n = 12) and control group (n = 11). Distributed over 4 weeks, FES training replaced 12 conventional training sessions in the intervention
group. An Extended Barthel Index (EBI) subscore assessed the performance of activities of daily living (ADL). The Chedoke McMaster
Stroke Assessment (CMSA) measured hand and arm function and shoulder pain. The Modified Ashworth Scale (MAS) assessed resis-
tance to passive movement. Unblinded assessments were performed prior to and following the end of the training period. Results. The
EBI subscore and CMSA arm score improved significantly in both groups. The CMSA hand function improved significantly in the FES
group. Resistance to passive movement of finger and wrist flexors increased significantly in the FES group. Shoulder pain did not change
significantly. None of the outcome measures, however, demonstrated significant gain differences between the groups. Conclusions. We
did not find clear evidence for superiority or inferiority of FES. Our findings, and those of similar trials, suggest that the number of ses-
sions should be at least doubled to test for superiority of FES in these highly impaired patients and approximately 50 participants would
have to be assigned to each therapeutic intervention to find significant differences.

Keywords:   Electric stimulation; Stroke; Hemiplegia; Upper extremity; Rehabilitation

I mpaired motor control of the upper extremity is one of the


most frequent consequences of a stroke. As few as 13% of
the participants examined within the first 2 weeks after onset
However, in some studies, FES was applied in addition to
conventional therapy or was compared to a placebo therapy,
reducing the certainty as to whether FES effects can be attributed
have no upper extremity motor impairment,1 and 6 months to either the additional therapeutic time for motor training or the
after the injury, severe motor deficits remain in 30% to 66% application of the particular method. Thus, more studies are
of stroke survivors.2 necessary that provide the same amount of motor training to the
To improve arm function, standard therapeutic interventions intervention and control group. Moreover, in standard rehabilitation
are used, such as Bobath therapy,3 constraint-induced therapy,4 settings, additional time devoted to a therapeutic strategy may not
and a task-specific motor relearning program.5 Therapeutic be financially feasible so integration of FES into the usual clinical
strategies that impose a higher level of practice activity in the treatment schedule is more feasible than an additional application.
paretic muscles should be preferred.6 This is an ambitious In this trial, we applied FES under the realistic rehabilitation
demand for patients who have very little voluntary function conditions of our country by not adding time to the typical course
of the paretic limb. One method that does not require voluntary of therapy. We examined stroke patients with severe to complete
muscle function during motor tasks is functional electrical paralysis of the arm and/or hand in the acute or subacute phase.
stimulation (FES). A variety of therapeutic objectives have The effects of FES on this group of patients have not been
been partially achieved through FES, such as facilitation of sufficiently examined. Accordingly, our purpose was to compare
voluntary movements, improvement of manual dexterity and motor recovery in severely affected stroke patients in early
activities of daily living (ADL),7-11 and reduction of shoulder rehabilitation who were treated with FES or conventional motor
pain12 and spasticity.13 training under normal clinical conditions.

From the Balgrist University Hospital, Spinal Cord Center, Zurich, Switzerland (SM, TK); Reha Rheinfelden, Rheinfelden, Switzerland (CS, AZ-S, TE); and
the Automatic Control Laboratory, Swiss Federal Institute of Technology, Zurich, Switzerland (TK). Address correspondence to Sabine Mangold, PhD, Balgrist
University Hospital, Spinal Cord Center/Research, Forchstrasse 340, 8008 Zurich, Switzerland. E-mail: smangold@balgrist.unizh.ch.

184
Mangold et al / FES in Early Stroke Rehabilitation   185  

Methods programmable FES system, including 4 current-regulated


stimulation channels, was used to generate custom-made
Participants movement sequences. Proximal muscles (eg, anterior deltoid
muscle, m. triceps brachii) as well as distal muscles (finger
Participants were recruited from an inpatient rehabilitation
extensors and finger flexors) were integrated into the stimulation
stroke center. The local ethics committee approved the study
sequence to reach, grasp, and release an object. Therapists
protocol and informed written consent to participate in the
selected the muscles to be stimulated with respect to muscles
study was obtained from all participants. In cases of writing
that met the following criteria: (a) had priority for the individual’s
disability, one witness confirmed the participant’s informed
current rehabilitation process, and (b) helped in the grasp
consent.
process (reach, grasp, and release an object). If necessary,
First-time stroke survivors admitted to the rehabilitation
therapists manually treated spasticity, used a help arm to reduce
center were screened for eligibility. They were included in the
gravity, and provided manual assistance to support the grasp
study if they met the following criteria: were 18 years of age
action and to prevent movements that might cause damage such
or older; had their first stroke from 2 weeks to 18 weeks from
as pathologic scapula movements. Before the FES treatment
entry into the trial; had an infarct or hemorrhage localized
period, stimulation thresholds for each muscle and the set-up
from the cortex to the brainstem; had severe hemiparesis to
were determined in a 1-hour single FES session. If the patients’
complete hemiplegia of the arm and/or hand (maximum values
arm functions changed during the 4-week FES training,
of the Chedoke McMaster Stroke Assessment [CMSA] for the
stimulation programs and supporting measures were adapted.
arm and hand were 3 points); were with or without aphasia, but
Each FES training session consisted of a program including
had the ability to understand the study and to provide informed
repetitive grasping functions. After the system was donned,
consent; and had the ability to sit in a wheelchair or on a chair
stimulation current amplitudes were individually set for each
with no contact to the back rest.
muscle group to achieve sufficient functional contraction force
Participants were excluded in cases with the following: a
without pain or discomfort. The stimulation frequency was 25 Hz.
pace-maker or other stimulation devices; pregnancy; epilepsy;
The pulse width varied between 0 and 250 microseconds to achieve
prosthesis of bones or joints in the local region of the electrical
controlled muscle contraction. Every reach-grasp-release cycle
treatment; skin injuries, rashes, burns, or fresh scars at the sites
consisted of different steps triggered by a push button, eg, stretching
of stimulation; prior stroke or other brain impairments; severe
the arm with the hand opening, hand closing, arm moving back, etc.
impairment of sensitivity and proprioception (according to
Figure 1 shows a typical cycle. The participants were encouraged
clinical estimation); shoulder-hand syndrome on the affected
to make volitional attempts to reach, open the hand, and close the
side; constant, strong pain in the shoulder of the affected side
hand simultaneously with the stimulation. They could either trigger
(CMSA value for painful shoulder, 1-3); or considerable
the stimulation sequence themselves or the therapist performed this
subluxation (>20 mm) of the affected shoulder joint.
task, indicating verbally to the participant when the next step was
initiated. Grasping objects were used such as a small bottle, ball,
Therapies and FES Intervention tube, tin, glass, or handkerchief. The FES session lasted 45 minutes,
Participants included in the 4-week training program were consisting of about 15 to 20 minutes of donning, other preparations
randomly assigned to the intervention (FES and conventional (eg, treating spasticity), and doffing, leaving 25 to 30 minutes for
training) or to the control group (conventional training) using functional training.
a computer-generated randomization list.
In both groups, 3 to 5 occupational therapy sessions for the
Assessments
upper extremity training were scheduled per week, each lasting
45 minutes. The number of therapies was adapted to the patient’s For baseline comparability, the following data were
resilience via a number of accompanying therapies, including assessed for each patient: age, gender, time poststroke, affected
physiotherapy, speech therapy, and neuropsychological training. side, diagnosis (hemorrhagic or nonhemorrhagic stroke), and
In the intervention group, FES made up 3 of the occupational hemineglect. Additionally, the Extended Barthel Index (EBI)
therapy training sessions per week. If the patient had more was selected to determine the level of independence with respect
functional training sessions per week, they were carried out in to ADL and the CMSA to assess motor recovery of the paretic
conventional therapeutic form. upper limb. The EBI contains 16 items (each rated with 0-4
Conventional occupational therapy for upper extremity points) including ADL, mobility, bowel and bladder functions,
training mainly consisted of mobilization and selective move­ communication, and cognitive and social functions.
ments of the shoulder, hand, and arm, and grasping exercises Baseline outcome measures were assessed 8 days and 1 day
supported by the therapist if necessary. To a small degree, before the beginning of the 4-week program. Posttreatment
ADL (eg, mixing cream, pouring water into a glass) and assessments were performed at the end of the 4-week program.
sensory retraining were practiced, as supported by the therapist Follow-up measurements were planned at 6 months after the
or performed bimanually. beginning of the treatment.
FES was carried out with the portable system called Compex An EBI subscore, including 4 items focusing on upper
Motion14 using standard self-adhesive surface electrodes. The extremity function (Table 1), and the arm and hand function
186   Neurorehabilitation and Neural Repair

Figure 1 chosen. Shoulder pain ranges from constantly strong pain in


Typical Grasping Cycle the shoulder and other parts (1 point) to no pain in the shoulder
and no prognostic indicators (7 points). The MAS measures
nonvoluntary resistance against passive movement. It ranges
from no increase in muscle tone (0 points) to rigidity of the
affected parts in flexion or extension (5 points). The following
muscles were assessed with the MAS: finger flexors, finger
extensors, wrist flexors, wrist extensors, pronators, supinators,
elbow flexors, and elbow extensor.
The nursing staff assessed the EBI and the two trained
physiotherapists performed the CMSA and MAS. Participants
and assessors were not blinded. The reliability and validity of
the CMSA,15 EBI,16 and MAS17,18 have been confirmed.

Data Analysis
Note: Six push-button signals trigger this typical grasping cycle to allow
an individual timing. The dashed plateau lines within one step indicate that Data analysis was performed by intention-to-treat. An
the stimulation remains constant until the next step is triggered. The sig- analysis of kurtosis and skewness was done for age, time
nals are the following: (1) anterior deltoid muscle, m. triceps brachii, and poststroke, and number of occupational therapy sessions of
finger extensors are activated (the arm stretches forwards with hand open upper extremity training to select adequate statistical tests for
to reach an object); (2) arm remains stretched and hand closes to grasp an
the evaluation of baseline comparability.
object; (3) hand remains closed and arm muscles relax; (4) arm stretches
to the front while fingers remain closed; (5) arm remains stretched Baseline comparability was evaluated with the following
and hand is opened to release the object; (6) the stimulation of arm mus- statistical tests. Age was tested with the independent t test
cles stops, bringing the arm passively back to the resting position. Once (Levene’s test for equality of variances). Time poststroke and
completed, the cycle can be started anew. number of occupational therapy sessions were evaluated with
the 2-tailed Mann-Whitney U test for nonparametric data,
CMSA score of the paretic arm were selected as primary because they were not normally distributed. This test was also
outcome measures. Each CMSA item score ranges from no used for EBI and CMSA scores (mean baseline values),
or almost no voluntary muscle activity (1 point) to normal because they are ordinal parameters. The number of participants
coordination of movement (7 points). in each group was compared with the χ2 test. The Pearson
As secondary outcome measures, the item “shoulder pain” 2-sided χ2 test was used to evaluate proportional differences
of the CMSA and the Modified Ashworth Scale (MAS) were in both groups regarding gender, diagnosis (hemorrhagic or

Table 1
Extended Barthel Index (Subscore)
Item Item Description Score
Eating and drinking Is unable, or requires a stomach feed tube and is dependent on assistance with device 0
Needs help in cutting and spreading 2
Is independent with adaptive equipment (eg, adapted cutlery handles) 3
Is independent, or requires a stomach feed tube, but can handle device independently 4
Grooming (washing face, Is unable 0
   combing, shaving, Needs help with many, but not all procedures 1
   brushing teeth) Needs minor assistance (eg, opening the toothpaste tube), or is physically independent, but needs supervision 2
Is independent with adaptive equipment (eg, extension of the hairbrush handle) 3
Is independent 4
Dressing and undressing Is unable 0
   (including tying shoes, Needs help with most, but not all articles of clothing, or needs help with all articles of clothing, but assists actively 1
   buttoning up) Needs help with only a few procedures (eg, support for tying shoes, donning orthotic devices), or is physically 2
   independent, but needs supervision
Is independent (perhaps with assistive devices such as sock aids) 4
Bathing self Is unable 0
Needs assistance with many, but not all procedures, (eg, support for transfers, is able to wash the upper part of the 1
   body, but not the lower part)
Needs minor assistance (eg, opening dispensers), or is physically independent, but needs supervision 2
Needs adaptive equipment (eg, bath chair, bath lift), but can use it independently 3
Is independent and needs no adaptive equipment 4
Mangold et al / FES in Early Stroke Rehabilitation   187  

Table 2 3. Baseline comparability was confirmed for all demographic


Patients’ Clinical Characteristics at Baseline data and primary outcome measures except one: The FES
and Statistical Group Differences group had a significantly higher EBI subscore than the control
Group
group (P = .013).
Control FES Differences
Group Group (P Value) Therapy Sessions
n 11 12 .84 Nine patients participated in 11 to 12 FES sessions. Three
Age (years), mean (SD) 62 (16.2) 57.5 (16.7) .74 participants stopped FES after 3 to 7 FES sessions. One
Female participant, n (%) 4 (36) 2 (17) .28 participant could not tolerate the stimulation intensity that was
Time poststroke (weeks), 7.3 (5.8, 8.2) 6.7 (6.4, 7.3) .56
   median (quartiles) necessary for a functional muscle contraction; another stopped
Nonhemorrhagic stroke, n (%) 9 (82) 10 (83) .92 because he developed high finger flexors tonus during the
Right hemiparesis, n (%) 4 (36) 3 (25) .55 session, although not stimulated. In their remaining therapy
Dominant arm affected, n (%)a 7 (64) 4 (40) .28 sessions, these participants received conventional therapy.
Neglect, n (%) 2 (18) 6 (50) .11 In total, the participants in the control group had 8 to 15
EBI, median (quartiles) 25 (21, 32) 32 (26, 35) .14
therapy sessions (median 13) and in the FES group 10 to 20
Abbreviations: FES, functional electrical stimulation; EBI, Extended Barthel (median 13), including FES and conventional therapy sessions.
Index. The number of therapy sessions was not significantly different
a
There were 2 missing values in the FES group. in either group (P = .38).

nonhemorrhagic stroke), affected side, dominant arm affected, Movement Quality


and hemineglect. The Wilcoxon Signed Rank test was applied FES generated distinct finger and arm movements, but the
to examine pre- and posttreatment changes in each group, therapist had to provide manual support when participants
comparing mean baseline values with the values at the end of reached to an object and opened the hand. Hand closure and
the 4-week program. The differences of functional gains retracting the arm were not manually supported. All participants
between both groups were analyzed with the Mann-Whitney U used the help arm to help reduce gravity.
test. All statistical analyses were performed with SPSS 11.5
for Windows (SPSS, Chicago, Illinois). Results were accepted
as statistically significant at P ≤ .05. Primary Outcome Measures
The minimal clinically important difference (MCID) was The FES group showed significant improvements in all
defined as a change of at least 9% of the maximum score primary outcome measures (EBI subscore, CMSA arm and
of the scale.19 With this 9% threshold, the MCID for the hand) from pretreatment to posttreatment (Table 3, Figure 2).
EBI subscore was 1.4 points, for each CMSA item the This was also true for the control group with the exception that
score was 0.6, and for each MAS item the score was 0.45 CMSA hand function only barely reached the level of significance
points. Additionally, effect sizes (Cohen’s d) of the primary (P = .06). Gains from pretreatment to posttreatment were not
outcome measures were determined for each group (within- significantly different between either group (Table 3, Figure 2).
group changes) and for gain differences between both Clinical importance, according to the MCID, was found for
groups. Cohen’s d was calculated using the means (m) and the following primary outcome measures (Table 3). In the
standard deviations (s) of the pretreatment and posttreatment control group, the gains of the median EBI subscore (3 points)
values, which were respectively the gains of both groups. and CMSA arm score (1 point) were clinically important. In
The calculation was performed with the Microsoft Office the FES group the EBI subscore reached this change criterion
Excel 2003 software using the following formula: Cohen’s (1.5 points). Group differences of median EBI subscore gains
d = m1 - m2/spooled, where spooled s the square root of [(s1² + s2²)/2]. (1.5 points higher in the control group) and of the CMSA arm
Based on the measured effect sizes, an alpha level of 0.5, and score gains (1 point higher in the control group) were clinically
a test power of 0.8, the optimal group size was derived from a important.
table.20 Cohen proposed labeling effect sizes of 0.2 as small, 0.5 as
medium, and 0.8 or higher as large.21 According to this
classification, pretreatment and posttreatment effect sizes of
Results the primary outcome measures were small to high (Table 4)
and effect sizes of gain differences between groups were small
Baseline Data
to medium (0.27 to 0.62). Hence, for medium effect sizes, a =
A total of 23 participants were enrolled, 11 in the control 0.05, and test power = 0.8, the optimum sample size would be
and 12 in the FES group. All participants completed the study. 50 participants per group and for small effect sizes the sample
Participants’ baseline characteristics are shown in Tables 2 and size would be 310 participants per group.20
188   Neurorehabilitation and Neural Repair

Table 3
Baseline Values, Gains From Pretreatment to Posttreatment, and Statistical Group Differences of Primary
Outcome Measures and Modified Ashworth Scale of 2 Muscles that Tend to Become Spastic
Control Group (n = 11) FES Group (n = 12)
Group Differences (P Value)
Outcome Baseline Median Gain Median Baseline Median Gain Median
Measures (Quartiles) (Quartiles) (Quartiles) (Quartiles) Baseline Gain

EBI subscore   5 (4, 5.5) 3** (1, 3.3) 6 (6, 7) 1.5** (0.8, 2)    0.013*   0.19
CMSA arm 1 (1, 2) 1* (0, 1) 2 (1, 2)   0* (0, 1) 0.73   0.57
CMSA hand 2 (2, 2) 0 (0, 1) 2.3 (1, 2.6)   0.3* (0, 0.5) 0.50 1.0
MAS finger flexors 1.5 (0.8, 2)      0 (-0.5, 0.8) 1.3 (0.9, 2)   0.5* (0, 1.1) 0.78   0.17
MAS wrist flexors   3 (1.5, 3) 0.5 (0, 1.3)   2 (1, 2.5)   0.5* (0, 1.1) 0.13   0.68

Abbreviations: FES, functional electrical stimulation; EBI, Extended Barthel Index; CMSA, Chedoke McMaster Stroke Assessment; MAS, Modified Ashworth
Scale.
*P < .05; **P < .01.

Figure 2 Secondary Outcome Measures


Box Plot of the Pretreatment and Posttreatment
Values of the EBI Subscore The baseline MAS score was 0 in 22 participants for finger
extensors, wrist extensors, and supinators. Finger flexors,
wrist flexors, and pronators had median baseline values
between 1.25 and 3, and elbow extensors had a median value
of 0 in the FES group and 0.5 in the control group. Nine
participants in each group had a baseline CMSA shoulder pain
score of 6 (without pain but having at least one prognostic
indicator such as very low arm function or abnormal positioning
of the scapula).
With the small sample size, secondary outcome measures
did not show significant changes within each group from
pretreatment to posttreatment, with the exception of a
significant and clinically important increase of the MAS of
finger and wrist flexors in the FES group (Table 3). However,
no secondary outcome measures demonstrated significant or
clinically important gain differences between either group.

Discussion
We investigated changes of upper extremity function in
Abbreviations: EBI, Extended Barthel Index; FES, functional electrical stroke participants with severe paralysis. Control participants
stimulation. received conventional upper extremity motor training.
Distributed over 4 weeks, FES training replaced 12 conventional
therapy sessions in the intervention group. The total number of
Table 4
therapy sessions did not differ significantly.
Effect Sizes (Cohen’s d) of Gains of the Primary Outcome
Primary outcome measures, ie, the EBI subscore and the
Measures From Pretreatment to Posttreatment
CMSA (arm and hand), improved significantly in both groups
Effect Size (Cohen’s d) except for the CMSA hand score in the control group (P =
.06). According to the MCID, only the gains of the EBI
Outcome Control FES
subscore in the control group (3 points) and FES group (1.5
Measures Group Group
points), and the gain of the CMSA arm score in the control
EBI subscore 1.13 0.53 group (1 point) were clinically important. Having 0 to 2 points
CMSA arm 0.78 0.78 per EBI item at baseline, a change of 1.5 points on the EBI
CMSA hand 0.63 0.29
subscore indicates participant fluctuation in 1 or 2 items from
Abbreviations: FES, functional electrical stimulation; EBI, Extended Barthel either being unable to being able to perform some tasks, or
Index; CMSA, Chedoke McMaster Stroke Assessment. needing significant assistance to minor assistance, or requiring
Mangold et al / FES in Early Stroke Rehabilitation   189  

minor assistance to achieving independence with adaptive to 47% after 6 months.28 At baseline, most of our participants
equipment (Table 1). In their baseline CMSA arm score, all were without shoulder pain. There was no significant change in
participants but one had 1 or 2 points. For participants starting shoulder pain within the groups during the 4-week program and
at 1 point, an increase of 1 point indicated the achievement of no significant gain difference between either group. Electrical
the ability to resist passive shoulder abduction and to extend stimulation can be used to treat shoulder pain, but our stimulation
the elbow with facilitation. For those who had these functions protocol was not adjusted to this special objective. Furthermore,
at baseline, a change of 1 point indicated the ability to touch beneficial effects of FES become obvious in participants who
the chin and the contralateral knee. already have developed shoulder pain29 and not in groups
The findings are in accordance with other studies on the including only few participants with shoulder pain.12,30
affected upper extremity, showing significant improvements Our study was performed with a small group of patients and
with only conventional therapy or additional electrical stimulation group imbalances weakened the validity of the intergroup
within several weeks after onset.7,22 The effect sizes are the same comparisons. Hence, the following conclusions have to be
magnitude found in comparable studies, eg, 0.65 for the Barthel appraised in this context. In acute, severely affected stroke
Index23 or 0.73 for the Fugl-Meyer gain scores.24 We found no patients, our stimulation protocol (12 sessions with 30 minutes
significant differences between functional improvements of the of stimulation time) does not induce superior improvements
intervention and the control group. However, there were compared to the same amount of conventional upper extremity
clinically important group differences of median EBI subscore motor training. We assume that within normal rehabilitation
and CMSA arm score, both favoring the control group. In other conditions in our country, it would be necessary for people to
studies of comparable participants, group differences for similar continue FES themselves at home. This would probably require
functional tests were inconsistent. The lack of significant group a simpler stimulation protocol. Based on our findings, further
differences in our study might not only be because of a small studies have to be carried out in at least 50 participants
group size, but also because of the low number of FES sessions. randomized to FES and conventional therapy, and additional
In other studies on acute stroke patients, various frequencies of dose-response studies with our protocol are necessary to identify
stimulation sessions were applied, from 24 to 120 sessions.8,10,24,25 the required minimum number of FES training sessions.
Furthermore, 25% of our participants had only 7 or less
stimulation sessions, reducing the potential effect of FES. The Acknowledgments
donning and doffing of the system reduced the effective time for
exercises in the FES group, suggesting that control participants The authors thank the physicians of the Reha Rheinfelden
had clinically important, though not significantly higher gains of in Switzerland for assessing subjects for eligibility; the
the EBI subscore and CMSA arm score. Baseline differences occupational therapists, physiotherapists, and nursery staff for
might also be responsible for these results. The proportion of thoroughly carrying out the treatment and assessment; and all
participants with hemineglect was higher in the FES group, patients for their participation in the study. This work was
reducing the motor recovery potential.26 The dominant hand supported in part by the National Center of Competence
was more frequently affected in the control group. Because of NCCR: Plasticity and Repair.
higher motor awareness of the dominant hand,27 the dominant
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