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Research Report

Functional Electrical Stimulation to the Dorsiflexors and Quadriceps in Children with Cerebral Palsy

van der Linden, Mariëtta L. PhD; Hazlewood, M Elizabeth MCSP; Hillman, Susan J. MSc, CEng; Robb, James E. MD, FRCS

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doi: 10.1097/PEP.0b013e31815f39c9
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INTRODUCTION

Functional electrical stimulation (FES) is the electrical stimulation of muscles that have impaired motor control to produce a contraction to obtain functionally useful movement.1 FES as a treatment option in children with cerebral palsy (CP) was first proposed by Gracanin2 and has several possible benefits. It may be used to achieve a direct “orthotic” effect during gait, for example, by triggering the ankle dorsiflexors to lift the foot in swing, or to trigger the quadriceps to extend the knee in stance. Possible long-term “therapeutic” effects of FES include a reduction in the tendency for muscle atrophy and improved motor control by improving the effectiveness of neural pathways.3

Previous case reports on the effects of surface FES to the lower limb in children with CP have shown promising results,4–7 but only a few studies have included more than two children.8–10 Using a case experimental design, Postans and Granat8 applied different FES strategies in children, six with diplegia and two with hemiplegia to investigate the direct orthotic effect of FES. Three children in their study showed clinically significant improvements, achieving the predefined target of a 5° increase in dorsiflexion in midswing and at initial contact when FES was switched on. In another study by Durham et al,9 FES was applied for 3 months to the dorsiflexors of 10 children with hemiplegia. No therapeutic effect was found, but the authors concluded that FES resulted in an improved foot-contact pattern on the affected side when the FES was switched on, hence an orthotic effect, although no statistical significance was reported. Finally, in the study of Comeaux et al,10 14 children received a daily therapy session consisting of gait and pregait activities for 14 weeks. In addition to this therapy, electrical stimulation using a remote switch was applied to the gastrocnemius (treatment 1) and the gastrocnemius and tibialis anterior (treatment 2) three times a week for 4 weeks. They reported a significant orthotic effect of both treatments on ankle dorsiflexion at initial contact measured on the video screen using a manual goniometer.

To the authors' knowledge, however, no randomized controlled trials have investigated both the orthotic and therapeutic effects of surface FES in children with CP. The aim of this exploratory trial was to provide effect sizes and data on the orthotic and therapeutic effects of FES required for a future appropriately powered randomized controlled trial. The null hypothesis was that there is no orthotic effect; hence no difference was expected in gait parameters between FES “on” and FES “off” and no therapeutic effect, hence no difference was expected between the control and experimental group. A second aim of this study was to investigate the feasibility of using FES equipment at home and school for children with CP.

METHODS

Participants

Physiotherapists and consultants in Edinburgh, Scotland and surrounding areas were asked to identify children with CP aged between 4 and 15 years who had either toe or forefoot contact or increased knee flexion during stance. Candidates for FES applied to the dorsiflexors (DF group) were those children who had decreased dorsiflexion in swing of more than two standard deviations compared with children developing typically and who made initial contact by the toe or forefoot. Candidates for FES to the quadriceps (Quads group) were those children who had increased knee flexion at initial contact and during stance of more than two standard deviations compared with a group of children assessed at our gait laboratory who were developing typically.11 Exclusion criteria were significant shortening of the muscles or joint limitation, ie, >10° of plantarflexion from neutral when the knee was extended, <40° of straight leg raise, or a hip flexion contracture of >15°. Children with significant athetosis, dystonic or dyskinetic CP, with cardiac conditions, uncontrolled epilepsy, or severe learning difficulties were also excluded.

Twenty-four invitations were issued for participation in the study, and 18 children with CP were recruited initially. However, after the baseline assessment three children did not fit the inclusion criteria. One girl in the control group failed to attend the third assessment. Fourteen children were matched as closely as possible on type of CP, function using the Functional Assessment Questionnaire12 and age. Of each of the resulting seven pairs, one child was randomly allocated to the treatment group while the other child of the pair was allocated to the control group. Randomization was performed by drawing identical tokens from a bag. Details of the 14 children who completed the study are shown in Table 1. The Local Research Ethics Committee approved the study and parents gave written, informed consent before their child's participation.

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TABLE 1:
Subject Characteristics of the Children in the Treatment Group and Control Group

Study Protocol

All children were invited to the gait analysis laboratory three times, at baseline, after the 2-week period of cyclic electrical stimulation (cyclic ES) for the treatment group and after the 8-week period of FES for the treatment group. During the first session, 3D gait analysis was performed of the child's usual walking pattern to determine whether the child fit the inclusion criteria and which muscle group was to be targeted.

At the second and third visit to the gait laboratory, all children in both the treatment and control groups were fitted with FES. Once the electrode position, footswitch position, and stimulation parameters were optimized, gait analysis was performed both with the stimulator switched on and off. The FES parameters for the treatment group at the third assessment were the same as those used at home.

The first and third session also included a physical examination of the range of motion of the joints targeted by FES. The joint and muscle ranges were assessed by passive manipulation, inhibiting spasticity by applying a slow stretch and appropriate positioning of the child and the examiners hands. The ranges were measured with a manual goniometer. The same observers performed all assessments. The researcher who measured range of motion and performed the data analysis was blind to group allocation.

Cyclic Electrical Stimulation

Weakness in children with CP13 may result in an inability to trigger the muscles effectively in the initial stages of FES. It was therefore hypothesized that 2 weeks of cyclic ES, sometimes called neuromuscular electrical stimulation, with the aim of improving the strength of the target muscles14 and to familiarize the child with the sensation of the electrical stimulation would make the application of FES more effective. For this reason, after the first baseline assessment, the children in the treatment group received 2 weeks of cyclic ES for an hour a day, 6 days a week to either the ankle dorsiflexors or the knee extensors. The stimulator used was the Neurotrac2™ (Verity Medical, Chilbolton, Hampshire, UK), which has an asymmetrical rectangular biphasic waveform.

An experienced pediatric physiotherapist made an initial home visit and instructed the child's parents on the use of the stimulator and electrode placement and also provided detailed written instructions. Follow-up home visits were made weekly during treatment to monitor and adjust the electrode positioning. The parents also had a contact phone number available (all hours) if any problems occurred. While receiving the cyclic ES the children were allowed to move around as normal but asked to avoid “rough and tumble” or water play. In the first week, stimulation comprised of 30 minutes at 40 Hz (duty cycle of 6 seconds on, 14 seconds off), followed by 30 minutes at 10 Hz (duty cycle: 6 seconds on, 10 seconds off) to avoid muscle fatigue. In the second week, stimulation comprised of 60 minutes at 40 Hz (duty cycle: 6 seconds on, 14 seconds off). Pulse duration was 100 microseconds for the dorsiflexors and 150 microseconds for the quadriceps for the first 30 minutes of the first week and during the full 60 minutes during the second week. One hundred microseconds was found to be sufficient to elicit an adequate contraction of the dorsiflexors, with least discomfort in the small muscles of these children. The quadriceps required a greater pulse duration to trigger a contraction. For the second 30 minutes in the first week this was 75 microseconds for both muscles to reduce the level of contraction thereby avoiding fatigue, while maintaining a low level of stimulation to continue the familiarization process. The ramp from zero to full stimulation lasted 0.8 seconds for both weeks. During the 2 weeks of cyclic ES, the parents gradually increased the intensity of stimulation under the guidance of the physiotherapist until a good contraction of the target muscles was achieved and tolerated by the child. “Good” was considered a visible contraction of the muscle, and resulted in appropriate movement of the target joint.

For both cyclic ES and FES, the motor points as defined by Scott15 were used as an initial guide for the attachment of the gel electrodes (PALS, Platinum Blue, Nidd Valley Medical, Knaresborough). The square 4 × 4 cm2 electrodes were found to be most comfortable for all children and lasted for 2 to 4 weeks. For the DF group, the electrode positions were adjusted until straight sagittal plane dorsiflexion was achieved, hence avoiding excessive inversion and eversion. This was generally achieved with the proximal electrode over the motor point of the tibialis anterior and the distal electrode often placed over the extensor digitorum. For the Quads group, the proximal electrode was sited over the anterolateral side of the thigh and the distal electrode over the motor point of vastus medialis. Electrode positions were adjusted by moving the electrodes until a maximum contraction of the selected muscle with the least discomfort was obtained, without excessive overflow to other muscle groups or any unwanted movement of the limb. The stimulation was also adjusted so that the muscles were not contracting at the limit of range to avoid potential damage.

Functional Electrical Stimulation

The single-channel Odstock Dropped Foot Stimulator (ODFS III, Biomedical Engineering and Medical Physics, Salisbury, UK) was used for FES. This stimulator has an asymmetrical biphasic voltage driven waveform. Output amplitude ranged from 20 to 70 mA and the stimulation frequency was 40 Hz. Output time, extension time, and ramp were adjusted for each subject. The level of intensity of the ODFS III was adjusted by increasing the pulse duration and ranged from approximately 3 to 350 microseconds. The same electrodes and the selection of their position were used as described above for the cyclic ES.

Footswitches were used inside the child's shoe to trigger the dorsiflexors immediately as the foot was raised from the ground. The settings were adjusted for each child so that dorsiflexors remained stimulated throughout swing to aid clearance and prepositioning of the foot before stance, and continuing briefly into loading to avoid foot-slap. The quadriceps muscles were triggered at initial foot contact and through loading. If necessary, the stimulation extended into midstance to maintain the knee extension, taking care to avoid delaying the initiation of knee flexion. Attempts were made to trigger the quadriceps in terminal swing, but this proved impossible because of the short swing time of these children.

Footswitches supplied by the stimulator manufacturer were used initially. These were later replaced by in-house manufactured footswitch strips (Fig. 1), which could be cut to an appropriate length for each child. In the first 2 weeks of the 8-week treatment, the pulse duration which, in these units, increases the intensity of the stimulation, and the duration of the daily use of FES, were gradually increased by the parents under the guidance of the physiotherapist to achieve a comfortable and effective level of stimulation. As with the cyclic ES, the families were visited weekly by the same physiotherapist. The children wore the units all day but removed them for sports activities. The physiotherapist also visited the child's school to inform and instruct teachers or auxiliaries, and parents were asked to keep a diary of stimulator use.

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Fig. 1.:
Custom made footswitch. The length and position of which was adjusted to the child's foot contact pattern.

Gait Analysis

Three-dimensional gait analysis was undertaken using a 50 Hz six-camera Vicon 370 motion analysis system (Oxford Metrics, Oxford, UK) and one Kistler force plate (Kistler Instrumente AG, Winterthur, Switzerland).

For those children who were candidates for FES to the quadriceps, gait analysis was performed with the children wearing their normal shoes and orthoses. Barefoot gait was assessed for the DF group.

Markers were placed on the lower limbs and pelvis according to the Vicon Clinical Manager (VCM) manual. Six to 10 trials were captured for each condition (FES off and FES on).

Ankle and knee angles and walking speed were calculated using the VCM software. In addition, the foot–floor angle at initial contact was derived from the foot orientation. A negative angle foot–floor indicates initial contact by the toe/forefoot, zero indicates flat foot initial contact, and a positive angle indicates initial contact by the heel.

The Gillette Gait Index (GGI) formerly known as the Normalcy Index16 is a measure of the amount of gait deviation compared with the gait of an average person without impairments. The GGI was computed from a selection of gait parameters derived from 3D gait analysis. The higher the score, the higher the deviation from the average person without impairments.

Physical Examination

An experienced physiotherapist performed passive range of dorsiflexion of the ankle both with the knee flexed and extended, and a second experienced professional made a measurement of the range using a manual goniometer. Intra-assessor coefficient of repeatability17 was 9.3° and 10.0° for dorsiflexion with the knee flexed and extended, respectively, for measurements 1 week apart.

Questionnaires

The parents of the children in both groups completed the Functional Assessment Questionnaire.12 The scores on this questionnaire range from 1 to 10, with 10 indicating the highest functional level. After the final visit to the gait analysis laboratory, the parents of the children in the treatment group were also given a questionnaire regarding their experience with FES.

Data Analysis

Two effects of FES during gait were investigated. First, the direct orthotic effect was determined by comparing the effects when the FES was switched off to those when FES was switched on during the same assessment. This “orthotic effect” was assessed for the children in both the treatment and control group. Second, the long-term “therapeutic effect” was investigated by comparing the differences in range of motion and gait parameters between the last and first assessment between the treatment and control group.

Statistical Analysis

The orthotic effect was investigated using paired Student t tests. The therapeutic effect was investigated by comparing values from the first and third assessment between the control and treatment group using repeated measures ANCOVA with the values at baseline as a covariate. For all statistical tests the level of significance was set at p < 0.05.

No separate statistical analysis was performed on the results of the children who received FES to the quadriceps because of the small number of children in this group (n = 4).

RESULTS

Compliance and Practical Issues of FES in the Treatment Group

One of the two children in the treatment group who received FES to the quadriceps completed the 2-week cyclic ES but only used FES for 1 week at home as he did not want to wear it to school. Although he came back for the third assessment, this child was excluded from the analysis for a therapeutic effect.

For one child the problem of excessive triggering of the peroneal muscles resulting in excessive eversion was not successfully resolved until after 6 weeks when the electrodes were reduced to very thin strips. The original footswitches broke easily and had to be replaced with more robust, pressure-sensitive strip footswitches (Fig. 1) manufactured in-house for all children. The families were provided with a spare switch and therefore minimal time was lost because of this problem. The in-house switches proved suitable for active children and made triggering more effective when they were running or toe walking, as the switch worked over the entire length of the sole.

Orthotic Effect of FES to the Dorsiflexors

Table 2 shows the ankle and knee kinematics at the two sessions with and without FES for the 10 children who received FES to the dorsiflexors. Both peak dorsiflexion in swing and foot–floor angle were significantly improved (p < 0.01) with FES in both sessions. Individual improvements for both dorsiflexion and foot–floor angles were as much as 8.8°. Nine of 10 children walked slower when the FES was switched on during both the first and second session. This resulted in a small but significant decrease in average walking speed of 0.07 m/sec (p < 0.01) in the first session and of 0.03 m/sec (p < 0.05) in the second session. FES to the dorsiflexors did not significantly affect the knee kinematics.

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TABLE 2:
Orthotic Effect of Applying FES to the Dorsiflexors (n = 10)

Orthotic Effect of FES to the Quadriceps

Table 3 shows the average knee kinematics of the four children in the Quads group. At the second visit to the gait analysis lab, two of the four children showed a decrease in knee flexion during stance of 6.1° and 6.2° when FES was switched on, while during the third visit the same children showed improvements of 8.6° and 4.6°. The differences between FES off and on conditions in the other two children were 2° or less. FES on the quadriceps had little or no effect (<1.5°) on the foot–floor angle and knee extension at initial contact.

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TABLE 3:
Orthotic Effect of Applying FES on the Quadriceps (n = 4)

Analyzing the orthotic effect of FES in the dorsiflexors and quadriceps groups together, a statistically significant (p < 0.01) effect was found for the GGI, which is a measure of the deviation of “overall” gait pattern from normal. FES resulted in improvements of 8 and 11 points during the first and second FES session, respectively.

Therapeutic Effect

Table 4 summarizes the long-term treatment effect of using 2 weeks of cyclic ES and 8 weeks of FES. The Functional Assessment Questionnaire, the deviation of the gait pattern from normal (GGI), foot–floor angle, dorsiflexion angle in swing, and passive dorsiflexion with the knee flexed showed a trend toward improvement or less deterioration in the treatment group compared with the control group with effect sizes between 0.3 and 0.9. However, none of the changes between first and third assessment were significantly different between the control and the treatment group.

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TABLE 4:
Therapeutic Effect of Applying Cyclic ES for 2 Weeks and FES for 8 Weeks

Parental Questionnaire

The parents of one child did not return the questionnaire on their opinion of using the FES stimulator but were interested in continuing to use the stimulator. Regarding the ease of use of the stimulator, the parents of one 13-year-old replied “very easy,” three found it not difficult, one found it difficult, and one very difficult. The main problems quoted were the leads becoming disconnected and removing and attaching the electrodes.

No skin problems were encountered with the square PALS electrodes. All children except one used the stimulator 4 to 6 days or more a week and for 6 or more hours a day. Three children used the stimulator only in the home and school. The other children wore it all day, except during physical education and swimming. One child quite liked using the stimulator, three did not mind, one just tolerated, and one disliked it. The 11-year-old child who disliked it did not use the FES stimulator after the first week as he felt embarrassed about the leads and electrodes and was also participating in many sports activities which meant removing and attaching the electrodes and leads several times a day.

On the question as to whether the parents thought using FES was a practical treatment for a child that age, two (ages 11 and 5 years) replied “no,” one (age 7 years) “yes” but only in the home and school (normal activities), and three (ages 5, 10, and 13 years) replied “yes.” All parents except one found using the stimulator quite demanding of their time. Finally, of the parents of the children who used the FES stimulator for most of the 8 weeks, all except one thought they had seen an improvement in the child's walking or motor skills.

DISCUSSION

FES to the dorsiflexors resulted in a statistically significant orthotic effect on peak dorsiflexion in swing and the foot–floor angle at initial contact, giving individual improvements up to 8.8° for both foot–floor angle and peak dorsiflexion in swing. Winter18 showed that a change in joint angle of as little 2° could significantly alter foot clearance. In the current study, the statistically significant changes in the ankle kinematics with FES ranged from 2.3° to 3.8° and could thus be regarded as clinically significant.

When FES to the dorsiflexors was switched on, nine of the 10 children walked slightly slower. Many children with CP have difficulty controlling forward progression. The small but significant decrease in speed when the FES was on may reflect a more controlled gait pattern because of the improved foot contact.

Individual improvements as a result of FES to the quadriceps ranged from 4.6° to 8.6°, hence higher than found for the dorsiflexors. However, an effect of FES to the quadriceps was only found for two of the four children. The other two did not tolerate a level of stimulation to the quadriceps high enough to result in a visible contraction. None of these four children tolerated a particularly long pulse duration (probably less than 200 microseconds, the dial on these units does not allow us to be exact). However, the two children who did achieve an effective contraction were slender, the other two were not. Children with large amounts of adipose tissue are therefore not likely to be good candidates for FES.

A statistically significant orthotic effect of FES was also found for the GGI. FES resulted in improvements of 8 and 11 points during the first and second FES session, respectively. However, it should be noted that Romei at al.19 suggested that changes in the GGI of 12 or less are not clinically significant.

Because of the limited number of subjects in each group, this exploratory trial only allowed an analysis of effect sizes of the therapeutic effect of using cyclic ES for 2 weeks and FES for 8 weeks. The treatment group (n = 7) showed a trend toward an improvement in passive dorsiflexion compared with the control group (7.2° vs 0.4°). The standardized effect size of the difference between the two groups was 0.7 which means a group size of 33 would be required to detect a significant difference in passive dorsiflexion at p < 0.05 and a power of 80%.20 To detect a significant improvement in dorsiflexion in swing and the GGI (effect size of 0.9) at p < 0.05 with a power of 80%, 20 children in each group would be required. A low effect size of 0.3 was found for the foot–floor angle. It is possible that this lack of therapeutic effect may be because electrical stimulation requires no voluntary control and is therefore unlikely to result in motor learning.

During the initial 1 to 4 weeks of FES all children in the treatment group tolerated the stimulation to a level of visible contraction and movement of the limb. In contrast, Postans and Granat8 found that six of the 21 children initially recruited did not tolerate the stimulation. Two weeks of cyclic ES in this study may have helped the patients' understanding and acceptance of the electrical stimulation in contrast to Postans and Granat's experience.

Results from the parental questionnaire showed that reasons for not using the stimulator were embarrassment, skin problems (unrelated to the use of the stimulator), and not being practical for “non-standard activities,” eg, playing out of doors or organized sports. It proved less of a burden when used by older children, who could take responsibility for the units themselves. Older children are often reluctant to continue to use their ankle foot orthoses, and FES may be a practical alternative. The younger children whose parents and schools were very supportive also managed well. FES may therefore be considered for children as young as 4 years, with sufficient supervision and support. However, as the effect of FES can be very dramatic to see, it should be made clear to the parents and children that FES is purely an assistive device, and is not a cure for impaired motor control in CP.

A common problem in studies involving children with CP is the limited number of suitable subjects who can be recruited and the variability of children with CP resulting in low statistical power.14,21 This, and the fact that we studied the effect of FES on two different muscle groups are the main limitations of this study. However, we feel that our results inform clinicians about the feasibility and practical issues of using FES for children with CP. It also provides an estimation of the sample size required in future randomized controlled trials on the effects of FES in children with CP.

CONCLUSION

This exploratory trial showed that FES applied to the dorsiflexors resulted in significant improvements in the gait of children with CP. The researchers also reported on both the positive and negative experiences of parents and children who used FES every day for 8 weeks. In our opinion, FES for children with CP can be a practical treatment option to improve gait kinematics in a carefully selected group of children, receiving adequate support from therapist, parents, and teaching staff.

Further randomized controlled trials with a group size of at least 20 subjects should be carried out to investigate whether daily use of FES results in a long-term therapeutic effect on joint range of motion, gait kinematics, and functional ability.

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Keywords:

cerebral palsy; child; electric stimulation therapy/methods; gait; human movement system; motor skills; physical therapy/methods; articular range of motion; treatment outcome; walking

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