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Adding Electrical Stimulation During Standard Rehabilitation After Stroke To Improve Motor Function. A Systematic Review and Meta-Analysis
Adding Electrical Stimulation During Standard Rehabilitation After Stroke To Improve Motor Function. A Systematic Review and Meta-Analysis
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Review
a, b a
Sharareh Sharififar *, Jonathan J. Shuster , Mark D. Bishop
a Department of Physical Therapy, College of Public Health and Health Professions, University of Florida, Gainesville, Florida, USA
bDepartment of Health Outcomes and Policy, Biostatistics Epidemiology and Research Design, Clinical and Translational Science Institute, Biostatistician, UF Clinical Research Center, College of
Medicine, University of Florida, Gainesville, Florida, USA
Article history: Background: Clinical studies have shown that sensory input improves motor function when added to active training after
Received 18 September 2017 neurological injuries in the spinal cord.
Accepted 10 June 2018
Objective: We aimed to determine the effect on motor function of extremities of adding an electrical sensory modality
without motor recruitment before or with routine rehabilitation for hemiparesis after stroke by a comprehensive systematic
Keywords: review and meta-analysis.
Sensory
Methods: We searched databases including MEDLINE via PubMed and the Cochrane Central Register of Controlled Trials
Stimulation
from 1978 to the end of November 2017 for reports of randomized controlled trials or controlled studies of patients with a
Stroke
clinical diagnosis of stroke who underwent 1) transcutaneous electrical nerve stimulation (TENS) or peripheral
Function
electromyography-triggered sensory stimulation over a peripheral nerve and associated muscles or 2) acupuncture to areas
that produced sensory effects, without motor recruitment, along with routine rehabilitation. Outcome measures were motor
impairment, activity, and participation outcomes defined by the International Classification of Functioning, Disability and
Health.
Results: The search yielded 11 studies with data that could be included in a meta-analysis. Electrical sensory inputs, when
paired with routine therapy, improved peak torque dorsiflexion (mean difference [MD] 2.44 Nm, 95% confidence interval
[CI] 0.26–4.63). On subgroup analysis, the combined therapy yielded a significant difference in terms of sensory stimulation
without motor recruitment only on the Timed Up and Go test in the chronic phase of stroke (MD 3.51 sec, 95% CI 3.05–
3.98). The spasticity score was reduced but not significantly (MD 0.83 points, 95% CI -1.77 0.10).
Conclusion: Electrical sensory input can contribute to routine rehabilitation to improve early post-stroke lower-extremity
impairment and late motor function, with no change in spasticity. Prolonged periods of sensory stimulation such as TENS
combined with activity can have beneficial effects on impairment and function after stroke.
1. Introduction few months after brain insult reduces the individual’s potential to participate
in therapy [2,3]. The initial damage to the neuronal pathways followed by
Hemiparesis is one of the prominent impairments caused by stroke that functional reorganization halt the motor recovery; however, many stimuli
affects activities of daily living and quality of life [1]. Clinically, the failure to have shown potential therapeu-tic benefit to improve functional recovery after
recover motor deficits rapidly within a stroke. Tradition-ally, in stroke research, potential therapeutic strategies
targeting motor recovery emphasize motor stimulation associated with
massed motor practice for the recovery of motor skills [4].
* Corresponding author.
E-mail addresses: shararehsharififar@gmail.com (S. Sharififar), shusterj@ufl.edu Afferent motor stimulation leads to neurological improve-ments, but the
(J.J. Shuster), bish@phhp.ufl.edu (M.D. Bishop). recovery of function varies. The effects of increased
https://doi.org/10.1016/j.rehab.2018.06.005
1877-0657/ C 2018 Elsevier Masson SAS. All rights reserved.
340 S. Sharififar et al. / Annals of Physical and Rehabilitation Medicine 61 (2018) 339–344
sensory input on motor outcomes have been relatively neglected in the Trials, Cochrane Database of Systematic Reviews, Web of Science,
rehabilitation literature as compared with those of other interventions, even SPORTDiscus, and Cumulative Index to Nursing and Allied Health Literature
though a number of studies suggested clinical benefits. In 1915, Franz et al. (CINAHL), Google, and WorldCat from 1978 to the end of November 2017.
were the first to report success in recovering upper extremity motor function We also hand-searched the reference lists of published reviews and narrative
by using simple rehabilitative techniques such as massage and vibration. [5] review articles. In addition, abstracts published in relevant conference
In particular, cutaneous and proprioceptive afferent information facilitates the proceedings were polled.
improvement of motor performance and promotes effective motor learning
because it increases the cortico-motor excitability in areas representing the The search terms included ‘‘cerebrovascular accident’’ OR ‘‘stroke’’ OR
stimulated body parts [6– 10]. Subsequent research has shown that electrical ‘‘hemiplegia’’ OR ‘‘hemiparesis’’ OR ‘‘hemiparetic,’’ AND ‘‘vibration,’’
sensory input alters the sensory and motor cortical maps [3,11–13] and ‘‘pressure’’ OR ‘‘haptics,’’ ‘‘kinesthetic*,’’ ‘‘stretch,’’ ‘‘weight,’’ ‘‘joint
clinical studies have shown that sensory input improved motor function when angle,’’ OR ‘‘tactile,’’ ‘‘touch,’’ OR ‘‘texture,’’ OR ‘‘transcutaneous
added to active training after neurological injuries in the spinal cord [14]. electrical nerve stimulation,’’ ‘‘TENS,’’ ‘‘neuro-muscular training,’’ AND
‘‘motor,’’ ‘‘movement,’’ OR ‘‘motion,’’ OR ‘‘mobility,’’ OR ‘‘function,’’
OR ‘‘performance’’. Although each database used differing syntax, this set of
search terms was the basis for the searches in each of those databases.
A recent systematic review and a meta-analysis of the effects of
augmenting rehabilitation with sensory stimulation were publis-hed in the We included reports of randomized controlled trials or controlled trials
past 10 years [15,16]. The review by Laufer et al. did not lead to a meta- with parallel or crossover designs. In studies with more than 2 arms, the
analysis because of too few studies that met inclusion criteria and the meta- values related to e-stim or placebo interventions combined with the routine
analysis by Veerbeek et al. did not separate sensory stimulations that lead to therapy were recorded.
motor recruitment from pure sensory-level stimulation. All reports of sensory modalities investigated such as vibration, pressure,
haptics, stretch, weight, proprioception, tactile, touch, texture, thermal, and
In the current analysis we expanded on these studies. In particular, we transcutaneous electrical nerve stimulation (TENS) as adjunct therapy to
used a newer method for the meta-analysis. The random-effects method is routine rehabilitation to improve post-stroke motor function were included.
commonly used, but it forces the distribution of effect sizes to be independent However, the primarily sensory modality of interest was e-stim. Different e-
of the study design, for no relation between a study’s effect size and the size stim inter-ventions such as repetitive electrical nerve stimulation, acupunc-
of study. This is a strong assumption, which is not necessarily true for all ture or muscle stimulation have common sensory nerve axon stimulation at
studies, so the estimate of the between-studies variance will have poor specific peripheral sites. The comparison groups included active treatment
precision, limiting investigators’ and clinicians’ ability to apply the (active or passive exercise, e-stim over different sites), placebo (sham, sub-
commonly used random-effects method appropriately. Because of major sensory threshold stimulus intensity), and no treatment.
issues with this method [17,18], we used the approach proposed by Shuster et
al. to overcome the fundamental limitations of the empirical weighting
method. In this approach, ‘‘studies-at-random’’ assumes that studies are The outcome measures were any measurable activity-based motor
drawn from a population of studies that are independent and implies that the function. To increase the generalizability of the results to the population of
weight given to each study’s effect size is a random variable [19]. interest, we included studies of participants with all durations of stroke-
related sequelae (acute, sub-acute, and chronic) and severity of stroke-induced
hemiparesis. The Interna-tional Classification of Functioning, Disability and
Thus, this current study extended the previous work by: Health (ICF) allowed us to document functioning and disability outcomes
reported by the included studies across the levels of function (the body, the
potentially broadening the available literature that could be reviewed; person, the society).
using a method suitable for pooling a small number of studies with a small
number of participants; 2.2. Assessment of quality of studies
examining the effects of electrical sensory stimulation without motor
recruitment across levels of function. Two independent raters (SSh and MDB) assessed the methodo-logical
quality of the included articles by using the standardized validated PEDro
The primary questions driving this current analysis were as follows: scale for the quality of controlled clinical trials [20], an 11-item scale [21]
previously used in systematic reviews [22], with total scores ranging from 0
to 10. Agreement in quality assessment on PEDro rating between evaluators
Is there evidence for the efficacy of augmenting rehabilitation with sensory was measured by the Kappa statistic, with 95% confidence intervals (CIs). A
input using electrical stimulation (e-stim) to improve motor function in a kappa of 1 ndicates perfect agreement, and a kappa of 0 indicates agree-ment
person after stroke? equivalent to chance.
What are the specific effects of adding an electrical sensory modality
before or along with routine rehabilitation on motor impairment, activity,
and participation outcomes after stroke? 2.3. Data analysis
The initial screening step involved examining the article title and major
key words, then abstracts and full texts.
2. Methods One author (SSh) extracted the relevant data from each article and
recorded them on standardized Microsoft Excel spreadsheets. To ensure
2.1. Identification and selection of studies accurate copying of the data, a second reviewer (MDB) independently
checked the information in the forms with the related articles. The data
We extracted key words associated from relevant articles and used recorded were the study design, participant characteristics, type of
Medical Subject Heading (MeSH terms) and Major Headings to search for intervention and co-interven-tion, region of the body to which the stimulus
human studies in any language in the databases MEDLINE via PubMed, was applied, and the mean pre-and post-intervention values for each measure.
Cochrane Central Register of Controlled
S. Sharififar et al. / Annals of Physical and Rehabilitation Medicine 61 (2018) 339–344
The meta-analysis involved use of SAS v9.4 (SAS Institute, Inc. Cary, The mean (SD) PEDro quality score for the 11 selected reports was
NC). We used a studies at random approach, which estimated the patient-level 7.18/10 (1.32, range 5–9). The Kappa score was 0.36 (95% CI 0.05–0.67) (P
effect size by assigning the weight of each point estimate based on the total < 0.00).
sample size [23]. We chose this method given limitations to the common used Characteristics of the included studies are in Table 1. The meta-analysis
random-effects model. included 11 studies that investigated the effects of electrical sensory input
without motor recruitment across levels of function. These studies included
The mean effect sizes of the outcome measures were calculated by using 440 participants with stroke (the ratio of males to females 2:1). The mean
the information provided in the articles. When the number of trials was > 5, (SD) age of participants was 61.28 years (6.9, range 49–72), with mean (SD)
the difference in means (MD; post-intervention mean values minus pre- post-stroke period 34.99 months (32.84). Each study had a small sample size:
intervention mean values) in the experimental and comparison groups was < 50 individuals in each group (range 14–67 total partici-pants). The single
considered the effect size of each of the trials [23]. When the number of controlled trial examined the effectiveness of e-stim using sock or glove
studies was small (< 5), we used a conservative t-approximation method electrodes with an intensity that was sufficient for sensory level but
[19,23]. Both periods of crossover trials were included in the analyses [24]. insufficient to produce a tetanic muscle contraction [25]. The remaining
Secondary analyses stratified data by chronicity, comparing participants < 6 studies used randomized controlled trial designs, repeated measures, or
months post-stroke with those > 6 months post-stroke for all outcomes with crossover designs. Most of the studies usually validated and justified their
sufficient data. Two-sided P < 0.05 was considered statistically significant. measu-rements and outcomes and described the intervention effectively. In
most studies, the description of the baseline characteristics was clear, and the
groups did not differ significantly in terms of certain characteristics.
However, the studies failed to screen for specific deficits such as type,
location, chronicity, and severity of stroke. The associated dysfunction in the
studies’ inclusion criteria resulted in non-tailored treatments and the treatment
3. Results of only one of the many deficits manifested in the population under the study.
The results of the systematic search are summarized in Fig. 1. Among the
676 articles identified, 189 were considered for potential inclusion; reports of
11 were finally included.
*
Fig. 1. Flow of studies in the review. Papers may have been excluded for failing to meet more than one inclusion criteria. rTMS, repetitive transcranial magnetic stimulation.
342 S. Sharififar et al. / Annals of Physical and Rehabilitation Medicine 61 (2018) 339–344
Table 1
Summary of included studies.
Table 1 (Continued )
Yavuzer, Oken RCT n = 30 Exp = ES of the paretic lower extremity Impairment = modified-Ashworth,
et al., 2007 [32] Mean (SD) age (yr) = 63.1 (1.7) 10 mA below palpable contraction, duty cycle gait kinematics
Sex = 14F 10 s on/10 s off 240 ms pulse width 240 ms pulse Activity = lower extremity motor
Mean (SD) chronicity (mo) = 3.4 width asymmetric biphasic rectangular at recovery, walking velocity (m/s)
(0.4) 35 Hz Participation = FIM
30 min(*)/day 5/wk 4 wk
Con = placebo
Both = Conventional stroke rehabilitation
program 2 to 5 hr (*)/day 5/wk 4 wk
CT: controlled trial; BL: baseline; Con: control group; ES: electrical stimulation; Exp: experiment group; F: female; FIM: functional independence measure; FRE: functional
resistance exercise; NA: not applicable; max: maximum; mo: months; ROM: range of motion; OT: occupational therapy; PT: physiotherapy; wk: week; yr: year; TENS:
transcutaneous electrical nerve stimulation.
a Standard stroke rehabilitation interventions such as neuromuscular re-education, RCT, randomized controlled trial; ROM, strengthening, neuromuscular facilitation, functional training, and use of
physical modalities and adaptive equipment as indicated.
b
Amount of the inhibition of the H reflex during vibration, excitability of soleus stretch reflex in terms of latency, onset angles and magnitude.
c
FRE included (1) loading exercise on the affected leg; (2) stepping-up exercise with the affected leg; (3) stepping-down exercise with the unaffected leg; (4) heel lifts from a dorsiflexed position in
standing and 2 functional training; (5) standing up from a chair, walking a short distance, and returning to the chair; and 6) walking with rhythmic
auditory cues generated by a metronome.
d
The physiotherapist provided standardized progression by using higher wooden blocks when subjects could perform the weight-bearing exercises 20 times without compensatory movement and
by increasing the number of repetitions completed within 10 min. Walking was progressed by increasing its speed.
Table 2
Summary effect sizes of combined sensory and motor inputs.
Activity Timed Up and Go test (sec) 4/171 7.87* 7.08 to 22.82 0.19
Timed Up and Go test (sec), chronic 3/133 3.51 3.05 to 3.98 0.00
Walking ability (m/s) 7/266 0.04 0.02 to 0.11 0.14
Walking ability (m/s), chronic 5/184 0.03 0.05 to 0.11 0.28
Body impairment Ashworth/modified Ashworth/CSS 8/487 0.83 1.77 to 0.10 0.07
Ashworth/modified Ashworth/CSS, chronic 6/182 0.17 0.85 to 0.51 0.53
4. Discussion
Our findings from this systematic review and meta-analysis show that
electrical sensory stimulation without muscle contrac-tion can help improve
post-stroke lower-extremity muscle function and functional mobility before or
with routine rehabili-tation for hemiparesis after stroke. An insufficient
number of studies reported common outcome measures. We used the t-
approximation method to calculate the effect sizes for 5 of 13 of the reported
outcomes, which were pooled from more than 3 studies per outcome measure.
The variability in methodology, in addition to the low power to find real
effects in many of the trials, may have contributed to these limited findings.
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