Electrical stimulation has been applied for children with cerebral palsy (CP) to increase strength1 and range of motion,2 reduce spasticity,3 and improve the performance of activities.4–6 However, forms of electrical stimulation vary. For example, neuromuscular electrical stimulation activates muscles in isolation when aimed at reducing impairments such as weakness1 or spasticity,7,8 whereas threshold electrical stimulation affects muscles at subcontraction levels (often during sleep) when aimed at increasing circulation.8–11 In contrast, functional electrical stimulation (FES) causes muscles to contract during the performance of an activity such as sitting, standing up from a chair, walking, or reaching for and manipulating objects.12,13 We were interested in this latter form, that is, examining the effect of FES used to improve activity in CP.
Given that the various forms of electrical stimulation are delivered differently and have different aims, separately examining the effect of different forms of electrical stimulation at the level of either impairment or activity limitations is important. Three previous systematic reviews examined the effect of electrical stimulation in CP.13–15 However, 2 of the reviews failed to separate the different forms of electrical stimulation and included low levels of evidence such as case studies.13,14 Only 1 review examined the independent effect of FES on activity15 and showed a beneficial effect. However, 3 of the 4 studies included in the meta-analysis of that review were randomized trials.
The research questions for our systematic review were, in children with CP: (1) is FES effective (ie, better than no-FES intervention)? (2) is FES more effective than activity training alone? (3) is the effect of FES maintained after the cessation of intervention?
To make recommendations based on the highest level of evidence, this review included only randomized controlled trials of children with CP (<18 years old) using FES to contract muscles during the performance of everyday activities with the aim of improving those activities.
Identification and Selection of Studies
The first review phase was to determine whether studies met the inclusion criteria. Searches were conducted of MEDLINE (1966 to February 2013), CINAHL (1982 to February 2013), EMBASE (1974 to February 2013), Cochrane (to February 2013), Web of Science (1945 to February 2013), and PEDro (1966 to February 2013) databases, without language restrictions using words related to CP and randomized controlled trials and words related to electrical stimulation such as electrical stimulation, biofeedback, and neuromuscular (see the Appendix available as Supplemental Digital Content at http://links.lww.com/PPT/A62). Titles and abstracts were displayed and screened by 1 reviewer to identify relevant studies. Full paper copies of relevant studies were retrieved and their reference lists were screened. The methods of the retrieved papers were reviewed independently by 2 reviewers using predetermined criteria of including only randomized controlled trials in which participants with spastic CP younger than 18 years received FES versus either no-intervention or placebo FES intervention (Question 1) or activity training that was consistent with the experimental group (Question 2). Functional electrical stimulation was defined as involving electrical stimulation during practice of an activity (Table 1). Disagreement or ambiguous issues were resolved by consensus after discussion.
Assessment of Characteristics of Studies
The quality of included studies was determined by extracting PEDro scores from the Physiotherapy Evidence Database (http://www.pedro.fhs.usyd.edu.au/). Two independent trained raters carry out the rating of trials in this database. When a trial was not included on the database, 2 reviewers who had completed the PEDro Scale training tutorial on the Physiotherapy Evidence Database assessed it independently.
Studies involving participants of either gender, regardless of the level of initial disability, were included. Age and Gross Motor Function Classification System (GMFCS) level were recorded so that the similarity of participants between studies could be examined.
The experimental group had to receive FES, that is, electrical stimulation while performing an activity such as walking. The control group had to receive either no intervention or placebo FES intervention (Question 1) or activity training that was consistent with the experimental group (Question 2). Participants could be receiving usual therapy as long as both groups received usual therapy. Activity trained using FES, duration and frequency of the intervention, and stimulation parameters were recorded so that the similarity of intervention between studies could be examined.
Measures of activity that best reflected the activity trained were used in the analysis. When continuous data (eg, walking speed) were not available, ordinal data (eg, Gross Motor Function Measurement) were used.
Information about the method (ie, design, participants, intervention, measures) and outcome data (ie, the number of participants and mean [SD] of outcomes) were extracted by 1 reviewer and checked by the other reviewer. When necessary, authors were contacted to provide additional information. If possible, data were pooled and the mean between-group differences (95% confidence interval) were calculated. If this was not possible, we calculated the mean difference (% difference) for each study and presented the between-group analysis reported by the author.
Flow of Studies Through the Review
The search strategy identified 341 studies. After screening titles and abstracts, 45 full papers were retrieved. After being assessed against the inclusion criteria, 5 randomized controlled trials6,16–19 were included in the review. See the Figure for flow of studies through the review.
Characteristics of Included Studies
Of the 5 included studies, 3 investigated FES versus no FES intervention or placebo and 2 investigated FES versus activity training alone. The quality of included studies is presented in Table 2 and a summary of the studies is presented in Table 3. Additional information was obtained from the authors of 2 studies.16,17
The mean PEDro score of the studies was 3.4 (range, 2-5) (Table 2). All studies were randomized (100%), and reported point estimate and variability (100%); the majority analyzed the between-group difference (60%). The majority of studies did not carry out concealed allocation (100%), blind participants (100%), assessors (60%), or therapists (100%), carry out an intention-to-treat analysis (100%), have similar groups at baseline (80%), or report less than 15% loss to follow-up (80%).
Four studies included children and adolescents ranging from 4 to 15 years and classified as Level I/II (independent walkers) on the GMFCS.20 One study included infants with a mean age of 1 year, classified as Level II/III (sit with support or using hands to maintain balance) on the GMFCS. The type of CP included diplegia (n = 102), hemiplegia (n = 11), and monoplegia (n = 2).
The experimental group received FES while performing either walking (4 studies) or sitting (1 study). The frequency and duration of intervention varied, with the total duration ranging from 180 to 2880 minutes. In 4 studies, low-frequency (∼30 Hz), high-intensity electrical stimulation (>20 mA) was applied and in 1 study high frequency (∼100 Hz), low intensity (<20 mA) stimulation was used. The control group received no intervention or placebo FES intervention (Question 1, 3 studies) or activity training that was consistent with the experimental group (Question 2, 2 studies).
Activity was measured using direct measures of performance in all studies with continuous data (walking speed in 3 studies) or ordinal data (Gross Motor Function Measure in 2 studies).
Effect of FES
Outcomes could not be pooled into a meta-analysis for several reasons. First, data for the outcome of interest were incomplete, which was not always rectified as a result of contact with the authors. Second, a large difference in baseline scores existed between the groups suggesting that between-group differences could be misrepresented if postintervention scores were used in a meta-analysis. Although this problem could be overcome if the pre-/postchange scores were used, they were not available for 3 of the studies. Therefore, the results of the between-group analyses are examined individually (Tables 4 and 5).
Effect of FES Versus No FES intervention
A statistically significant between-group difference in activity in favor of FES was reported for all 3 studies, immediately after the intervention period. This difference represented a 30% to 32% greater increase in activity compared with no FES intervention. A follow-up measurement was reported for 1 study, but no data were reported.
Effect of FES Versus Activity Training
Both studies reported a statistically nonsignificant between-group difference in activity compared with activity training, immediately after the intervention period. One study included a follow-up measurement, but no data were reported.
This systematic review is the first to examine the effect of FES on activity in children with CP using only randomized trials. However, evidence was limited with only 5 trials being included. This limited evidence suggests that FES is effective, that is, it is better than no FES intervention, but that it is no more effective than activity training, that is, practicing the activity without FES will be just as effective. Furthermore, no evidence was found on whether any benefits are maintained beyond the intervention period because even though a follow-up measurement was reported for 2 studies, the authors failed to provide data.
Even though the review was restricted to the highest standard of evidence, randomized trials, firm conclusions cannot be made. This is primarily because of the absence of group data (means and SD) in the papers, preventing a meta-analysis. This poor reporting is disappointing given that 3 of the 5 trials were published within the last 5 years. Therefore, we may be fairly confident that FES is effective given that all 3 trials reported statistically significant between-group differences in favor of FES, but with no meta-analysis providing an effect size, it is not possible to judge the clinical significance of the benefit.
The suggestion that FES is no more effective than practice of the activity without electrical stimulation implies that there is no convincing effect of implementing electrical stimulation in clinical practice. However, the machine to apply the electrical stimulation is easy to carry because it is a small, lightweight, battery-powered unit, is low-cost and commercially available, and has no adverse effects. Given that FES might be more effective than no FES intervention, it might be useful for those children who find exercise programs difficult due to cognitive disability since the stimulation may draw attention to the muscle to be contracted. No authors reported that they used published guidelines to inform their choice of duration and stimulation parameters. The available information suggests that frequencies of around 30 Hz elicit a smooth contraction, balancing muscle fatigue with an effective contraction,21 which is in line with the studies included in this review. Most of the studies reported the intensity as a “visible contraction,” which may not have been strong enough to move the limb. It is interesting to speculate on whether stronger muscle contractions may have increased the effectiveness of the intervention.22 Notably, participants in 2 studies in this review received FES as a home-based program carried out by their parents, suggesting that it is a feasible treatment option for practice at home.
Little clinical heterogeneity was present across the trials. Most trials included participants who were children with CP between the ages of 4 and 16 years with a mild disability. The electrical stimulation was mostly applied at low frequency and intensity. Activity was measured using direct observation of performance producing continuous or ordinal data. Probably the most heterogeneous aspect of the trials was the duration of intervention, which ranged from 180 to 2880 minutes.
This review has both strengths and limitations. The strengths are the comprehensive search strategy, lack of bias in selecting studies by blinding reviewers to journals, authors and outcomes, and the inclusion of only randomized trials. However, high-quality evidence is still not available because insufficient data were reported in these trials to allow a meta-analysis to be performed. Furthermore, an average score of 3.7/10 on the PEDro scale for quality meant that many of the important components of good randomized trials, such as concealed allocation and blinded assessment, were missing. Furthermore, the results of this review are potentially affected by small trial bias, with an average number of 22 participants per trial (range, 9-32) and no estimate of effect size for clinical significance. In addition, the baseline measurements of participants were not the same, which meant that even when postintervention group data were reported, they could not be used.
Limited evidence about the effect of FES for children with CP is available. The published evidence suggests that FES is more effective than no FES intervention but has a similar effect to activity training alone. Rather than being used routinely in clinical practice, it might be useful for those children who find exercise programs difficult due to their level of disability of poor concentration. Future studies investigating the effect of FES for children with CP and more severe disability may be useful to guide clinical practice.
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adolescent; cerebral palsy; child; electrical stimulation; exercise therapy; meta-analysis; physical therapy/techniques; rehabilitation; systematic review; randomized controlled trials
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