From the Departments of Physical Medicine and Rehabilitation (J.C., F.B.,
T.B., L.D., T.D.) and Orthopedics (J.C., F.B.), MetroHealth Medical Center,
Cleveland, Ohio, and the Center for Physical Medicine and Rehabilitation
(J.C.) and Rehabilitation Engineering Center (J.C., F.B.), Case Western
Reserve University School of Medicine, Cleveland, Ohio.
Correspondence to John Chae, MD, Center for Physical Medicine and Rehabilitation, Case Western Reserve University, MetroHealth Medical Center, 2500 MetroHealth Dr, Cleveland, OH 44109-1998. E-mail jchae{at}metrohealth.org
Methods—Forty-six stroke survivors admitted to an inpatient
rehabilitation unit were randomly assigned to receive either
neuromuscular stimulation or placebo. Twenty-eight subjects completed
the study. The treatment group received surface neuromuscular
stimulation to produce wrist and finger extension exercises. The
control group received placebo stimulation over the paretic forearm.
All subjects were treated 1 hour per day, for a total of 15 sessions.
Outcomes were assessed in a blinded manner with the upper extremity
component of the Fugl-Meyer Motor Assessment and the self-care
component of the Functional Independence Measure at pretreatment, after
treatment, and at 4 and 12 weeks after treatment.
Results—The treatment subjects and control subjects had
comparable baseline characteristics. Parametric
analyses revealed significantly greater gains in Fugl-Meyer
scores for the treatment group after treatment (13.1 versus 6.5;
P=0.05), at 4 weeks after treatment (17.9 versus 9.7;
P=0.05), and at 12 weeks after treatment (20.6 versus
11.2; P=0.06). Functional Independence Measure scores
were not different between groups at any of the time periods
(P>0.10).
Conclusions—Data suggest that neuromuscular stimulation enhances
the upper extremity motor recovery of acute stroke survivors. However,
the sample size in this study was too small to detect any significant
effect of neuromuscular stimulation on self-care function.
Both basic and clinical studies suggest that poststroke motor recovery
or motor relearning of the paretic limb may be maximized by the active
repetitive use of the affected limb.17 18 19 20 21 22
However, many acute stroke survivors exhibit a significant degree of
hemiparesis, which limits the application of this strategy in the acute
stroke rehabilitation environment. Furthermore, with significant
reduction in acute inpatient rehabilitation length of stay and
outpatient services, many rehabilitation service providers are forced
to focus principally on compensatory strategies to maximize function in
the shortest amount of time rather than the restoration of motor
control.23
One technique that may facilitate motor restoration of stroke survivors
is neuromuscular stimulation–induced repetitive movement exercises.
Numerous studies have suggested that neuromuscular stimulation reduces
spasticity24 25 26 and enhances the muscle strength
of the hemiparetic limb.26 27 28 29 30 31 32 33 34 A recent
meta-analysis of four randomized trials concluded that
neuromuscular stimulation improves the motor strength of stroke
survivors.35 The authors write "Given the large
burden of disability from cerebrovascular disease and the paucity of
efficacious therapeutic modalities, further research on the use of
electrostimulation would appear to be prudent (p 552)." In view of
the limitations of prior studies, Glanz and associates further
recommend that "Future studies should be double-blinded and
sham-controlled, and ideally should examine more sustained and complex
aspects of neurofunctional recovery after stroke (p 552)." Thus this
study uses a double-blind, placebo-controlled, randomized design to
test the hypotheses that neuromuscular stimulation enhances the upper
extremity motor and functional recovery of acute stroke survivors as
reflected by the Fugl-Meyer Motor Assessment and the Functional
Independence Measure (FIM), respectively. We test an additional
hypothesis that the therapeutic effects of the neuromuscular
stimulation are sustained for up to 3 months beyond the termination of
treatments.
Intervention
Assessments
Motor function was assessed with the upper extremity motor subscore of
the Fugl-Meyer Motor Assessment.36 The items in
the motor subsections were derived from Brunnstrom's stages of
poststroke motor recovery, although the specific stages were not
used.37 Reliability and validity of the
Fugl-Meyer Motor Assessment have been
documented.38 39 The upper extremity–related
disability was assessed with the self-care component of the FIM. The
FIM, which was historically derived from the Barthel
Index,40 is primarily an ordinal scale with some
interval characteristics. The reliability and validity of the FIM have
been previously documented.41 42 43 44
Analysis
The baseline characteristics of the NS and placebo subjects are shown
in Table 3
The study has several limitations. There was a high dropout rate, with
pain from stimulation being the most common cause. Future studies
should use alternative techniques such as percutaneous
stimulation to minimize the discomfort of stimulation and the potential
confounding effect of selective dropout. An intention-to-treat
analysis should be used to further minimize the effect of
dropout. The motor function of control subjects was somewhat lower than
that of the treatment group. The control group also had more cortical
stroke survivors, whereas the treatment group had more subcortical
stroke survivors. Although the differences in these variables were
not statistically significant, the small sample size places the study
at risk for a type II error, allowing for the possibility that the
treatment group was composed of individuals with greater potential for
spontaneous recovery compared with that of control subjects. The small
sample size in this study and the high dropout rate after randomization
further limit the generalization of the results to the broader stroke
population. As will be discussed below, the upper extremity–related
disability measure used in this study may have been inadequate, and
future studies should use measures more specific and sensitive to the
intervention.
Given these limitations, conclusions must be drawn with caution. The
study suggests that active repetitive exercises induced by
neuromuscular stimulation enhance the motor recovery of acute stroke
survivors. Furthermore, the effect appears to be sustained for up to 3
months after completion of treatment. This is consistent with
the evolving basic and clinical data on central motor neuroplasticity
that support the use of active repetitive training of the paretic limb
to maximize motor recovery after stroke. The motor recovery enhancing
effect of amphetamine in a rat model after unilateral ablation of the
motor cortex is blocked if the animals are not allowed to actively and
repetitively use their paretic limb.17 A recent
study in primates suggests that after local damage to the motor cortex,
active repetitive training of the hemiparetic limb shapes subsequent
functional reorganization in the adjacent intact cortex and that the
undamaged motor cortex plays an important role in motor
recovery.18 19 A clinical study of subacute
stroke survivors also emphasizes the importance of frequent active
movement repetition for motor rehabilitation of the centrally paretic
hand and challenges conventional physiotherapeutic strategies that
focus on tone modification and functional compensation instead of early
initiation of active movements.20 Among stroke
survivors who are beyond 6 months from their stroke, "forced"
active repetitive movement of the paretic limb also appears to enhance
motor and functional recovery.21 22
This study failed to demonstrate that neuromuscular stimulation
enhances the upper extremity–related functional recovery of acute
stroke survivors. Previous studies have demonstrated that motor and
functional recovery roughly parallel one
other.5 6 Although the lower extremity motor
status of stroke survivors correlates well with ambulatory function,
the relation between upper extremity Fugl-Meyer and the self-care
component of the FIM is modest at best.46 This is
due to the nature of the FIM. The self-care component of the FIM
measures general disability and is not arm disability specific. Stroke
survivors with severe upper extremity hemiplegia can score high on the
self-care component of the FIM as long as they are able to learn
compensatory single-handed techniques to perform the activity. The
items in the self-care component of the FIM are basic in nature and
patients are not penalized for using a single-handed versus a bimanual
strategy. Future studies should use a functional outcome measure that
is specific to the arm and is more sensitive to the degree of arm
hemiparesis. Tests of arm function47 48 49 that
specifically assess the functional ability of the hemiparetic limb and
more complex bimanual functional tasks may be more appropriate
disability outcome measures for these types of studies.
This study suggests that surface neuromuscular stimulation enhances the
upper-extremity motor recovery of acute stroke survivors and that the
affect is maintained for up to 3 months after completion of treatment.
However, the study failed to demonstrate any significant functional
benefit. To make definitive recommendations, a large, multicenter,
randomized clinical trial with intervention-specific objective measures
of motor and functional impairment should be carried out. Future
studies should also define the dose effect and elucidate the mechanism
of action to further guide the clinical implementation of neuromuscular
stimulation. While the definitive study remains to be carried out, the
evidence from the present study, prior small
studies,25 26 27 28 29 30 31 32 33 34 and the recent
meta-analysis35 suggest that
neuromuscular stimulation may be beneficial for a select group of
stroke survivors in maximizing their motor recovery.
Received November 3, 1997;
revision received March 6, 1998;
accepted March 6, 1998.
© 1998 American Heart Association, Inc.
Original Contributions
Neuromuscular Stimulation for Upper Extremity Motor and Functional Recovery in Acute Hemiplegia
Abstract
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Background and Purpose—The purpose
of this study was to assess the efficacy of neuromuscular stimulation
in enhancing the upper extremity motor and functional recovery of acute
stroke survivors.
Key Words: hemiplegia • motor recovery • rehabilitation
Introduction
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Dedicated stroke
units, which admit patients for acute medical management and subsequent
interdisciplinary rehabilitation, enhance the overall medical,
neurologic, and functional outcome of stroke
survivors.1 2 However, a robust relation between
specific treatments directed at motor impairment and corresponding
reduction in physical disability has not been
established.3 The degree of motor recovery after
stroke varies widely and is directly related to the degree of initial
severity and the interval from stroke to initiation of voluntary
movement.4 5 6 During this period, motor recovery
is believed to be enhanced by various techniques such as the
neurodevelopmental technique,7 sensorimotor
integration,8 proprioceptive neuromuscular
facilitation,9
biofeedback,10 and functional utilization of
evolving synergies.11 However, controlled studies
have failed to demonstrate that any one method is superior to the
others in enhancing motor or functional recovery of stroke
survivors.12 13 14 15 16
Subjects and Methods
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Subjects
Stroke survivors admitted to an acute inpatient rehabilitation
service within 4 weeks of their unilateral stroke were screened for
inclusion. Subjects were 18 years old or older with moderate to severe
upper extremity paresis (Fugl-Meyer score less than 44). Subjects were
excluded if they had a history of potentially fatal cardiac
arrhythmias, demand cardiac pacemaker placement, seizures
within the 2 years before admission, active reflex sympathetic
dystrophy, prior stroke with residual motor weakness, lower motor
neuron lesion of the impaired upper extremity, spinal cord injury,
traumatic brain injury, multiple sclerosis, or Parkinson's disease.
Enrolled subjects were excluded after randomization if they could not
tolerate the stimulation, if they were medically unstable, or if they
were discharged before completing their treatment and were unable to
continue with the treatment at home. When enrolled subjects were
dropped from the study, the next subject who qualified for the study
assumed the assignment of the dropped subject on enrollment. Subjects
who were excluded after randomization were followed up by telephone to
assess their disposition (home versus nursing home) and the degree of
arm paresis.
The study institution's human subjects committee approved the
study protocol, and subjects signed informed consent. The treatment
procedures were in accordance with institutional guidelines. Subjects
were assigned to the treatment or placebo group by a computer-generated
random number table. All subjects received standard physical,
occupational, and speech therapy interventions as per routine of the
inpatient stroke rehabilitation program. In addition, all subjects
received 1 hour per day of electrotherapy with a portable, commercially
available surface neuromuscular stimulation unit (FOCUS, Empi Inc). All
subjects received a total of 15 sessions. The treatment group received
stimulation of the extensor digitorum communis and the extensor carpi
radialis (ECR) through circular 2.5-cm surface electrodes. The brevis
and longus heads of the ECR could not be further differentiated with
surface stimulation. The stimulation current intensity was set to
produce full wrist and finger extension with a duty cycle of 10 seconds
on and 10 seconds off. The stimulus pulse was a symmetric biphasic
waveform with amplitude ranging between 0 to 60 mA, pulse width of 300
µsec, frequency ranging between 25 to 50 Hz, and ramp up and down
time of 2 seconds each. The current amplitude and stimulus frequency
were adjusted to subject comfort. The control subjects also received
surface stimulation, but the electrodes were placed away from all motor
points, producing only cutaneous stimulation just beyond sensory
threshold and without motor activation. All treatments were carried out
under the supervision of a trained occupational therapist. Subjects who
were discharged before completing the treatment continued to receive
the treatment at home under the supervision of a trained family
member.
All subjects were characterized with respect to demographics
(age, sex, and stroke onset to treatment interval), medical
comorbidities (hypertension, coronary artery disease,
congestive heart failure, diabetes mellitus, and prior stroke),
presence of sensory impairments and hemineglect, side of the
hemiparesis, stroke type (hemorrhagic versus nonhemorrhagic), stroke
level (cortical versus subcortical), and vascular distribution
(anterior versus posterior). Blinded evaluations of upper
extremity–related motor function and disability were performed before
treatment, after treatment, and at 4 and 12 weeks after treatment by
trained physical and occupational therapists, respectively. Blinding
was assured by having separate therapists provide the treatment and the
assessment. The assessing therapist was unaware of the treatment
assignments. Subjects were instructed not to discuss the nature of
their treatment with the treating and assessing therapists.
A sample size of 14 subjects per group was calculated by power
analysis with anticipated difference in Fugl-Meyer scores
between groups of 1 standard deviation in Fugl-Meyer scores with ß of
0.2 and one-tailed 
of 0.05. The anticipated difference between
groups was based on results of a pilot study on the effects of
electromyogram-triggered neuromuscular stimulation on the upper
extremity motor recovery of acute stroke
survivors.45 The baseline characteristics of
subjects who successfully completed the treatment protocol and those
who dropped out after randomization were compared to assess for
potential bias caused by dropout. Similarly, the baseline
characteristics of treatment and control subjects were compared to
assess the success of randomization. Continuous and nominal baseline
variables were compared with the independent t and
2 tests, respectively. The gain in Fugl-Meyer
and FIM scores were compared across groups at each test period with the
independent t test.
Results
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
A total of 46 subjects initially enrolled in the study.
Twenty-eight subjects completed the treatment protocol. Among those who
completed the treatment protocol, 14 were assigned to the neuromuscular
stimulation (NS) group and 14 to the control group. Eighteen subjects
were excluded from the study after randomization for the various
reasons shown in Table 1
. Of the 18
subjects who were excluded, follow-up data were available for 17
subjects. All subjects were still alive at an average follow-up period
of 17 months after treatment. Eighty percent (8 of 10) and 100% (7 of
7) of subjects assigned to the treatment and placebo groups,
respectively, were back in the community at follow-up
(2=1.6; P=0.21). Attempts to assess
the degree of motor recovery for each group by telephone interview was
unsuccessful because family and subjects often reported the degree of
paresis to be significantly worse than the previously recorded
baseline Fugl-Meyer scores. The baseline characteristics of subjects
who completed the treatment protocol and those who were excluded from
the study after randomization are shown in Table 2. The groups were comparable with
respect to demographics, medical comorbidities, stroke characteristics,
and baseline upper extremity Fugl-Meyer and self-care FIM scores.
View this table:
[in a new window]
Table 1. Subjects Excluded After Randomization, Treatment
Assignments, and Reasons for Exclusion
View this table:
[in a new window]
Table 2. Baseline Characteristics of Subjects Who Dropped Out
of the Study After Randomization and Those Who Completed the Treatment
Protocol . There were no significant
differences between the groups with respect to demographics, medical
comorbidities, stroke characteristics, and baseline upper extremity
Fugl-Meyer and self-care FIM scores. The gain in the upper extremity
Fugl-Meyer and self-care FIM scores are shown in Table 4. In general, subjects in both groups
experienced motor recovery in the untreated arm muscles (shoulder
abduction-adduction, shoulder external-internal rotation, and elbow
flexion-extension) before recovery in the treated forearm muscles
(wrist and finger extension-flexion). The analyses of the
Fugl-Meyer gain scores with the independent t test revealed
significantly greater motor improvement for the NS group before
treatment (t=-2.1; P=0.05), at 4 weeks after treatment
(t=-2.2; P=0.05), and at 12 weeks after treatment (t=-2.0;
P=0.06). The effect sizes at each follow-up period were
0.73, 0.73, and 0.73, respectively. More conservative estimates of the
effect size with the larger standard deviation of the two treatment
groups for each period were 0.64, 0.64, and 0.62, respectively. The
difference in the FIM gains scores between groups were not
statistically significant at any of the follow-up periods
(P>0.10).
View this table:
[in a new window]
Table 3. Baseline Characteristics of Control and
Neuromuscular Stimulation Groups
View this table:
[in a new window]
Table 4. Gains in the Upper-Extremity Fugl-Meyer and
Self-care FIM Scores After Treatment and at Follow-up Periods
Discussion
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
The major finding of this double-blind, placebo-controlled,
randomized study is that stroke survivors treated with surface
neuromuscular stimulation gained significantly greater upper extremity
motor recovery than did control subjects. However, the gains in the
motor function did not translate into significant improvement in the
performance of basic self-care activities. In contrast to prior
studies, this study documents the effects of neuromuscular stimulation
on the complex aspect of neurofunctional recovery as reflected by the
Fugl-Meyer Motor Assessment and the FIM, and the outcomes are assessed
for up to 3 months after treatment.
Acknowledgments
This study was supported in part by the Rehabilitation Medicine
Scientist Development Program (NIH 1K12 HD01097–01A1) and the Physical
Medicine and Rehabilitation Education and Research Foundation (New
Investigator Award).
Footnotes
Presented in part at the 1997 Annual Assembly of the American Academy of Physical Medicine and Rehabilitation.
References
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
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