Cerebral palsy (CP) is defined as a group of nonprogressive movement and posture disorders caused by a lesion to the developing brain.1 Spasticity is one of the key impairments in children with CP, affecting approximately two-thirds of this population.2
Traditionally, spasticity has been viewed as the main movement disorder in children with spastic CP, and strength training has thus been avoided for fear of exacerbating the already high muscle tone.3 More recent literature has, however, shown that muscle weakness is an integral part of the clinical presentation of spastic CP,4,5 and the contribution of both weakness and spasticity to the clinical presentation of spastic CP is thus a topic of debate in current literature. There is increasing evidence that strengthening programs can address specific missing components and thus form a vital component of the physiotherapy treatment of CP. Not only does improved muscle strength correlate with increased levels of functional skills,6 thus reducing dependence on caregivers and assistive devices, but it also results in improved cardiorespiratory endurance.
Authors of several studies have advocated a multidisciplinary approach to spasticity reduction and specific muscle strengthening in the management of children with CP.5,7–9 In this light, focal reduction in muscle tone by the injection of botulinum toxin is frequently combined with strengthening of the antagonist muscle during therapy.9 Although the effect of the toxin wears off after 3 to 6 months,10,11 the aim of this combined treatment approach is to integrate improved movement patterns on a central basis to achieve functional gains that last longer than the action of the chemical compound.11,12
One modality gaining popularity in addressing both spasticity and weakness in CP is functional electrical stimulation (FES). It is characterized by the stimulation of intact peripheral nerves to activate their associated muscles in a functional manner.13 By applying electrical stimulation to the agonist, muscle strengthening is brought about by increasing motor unit recruitment and by increasing contractile proteins, with resultant muscle hypertrophy.14 In addition, electrical stimulation applied to the antagonist can cause a decrease in tone in the agonist15 through reciprocal inhibition.16,17 Although extensive investigations into the separate effects of FES and botulinum toxin have been conducted, very few studies have combined these 2 modalities. The primary aim of this study was therefore to investigate the effect of this combination therapy on plantar flexor muscle strength and self-selected walking speed in children with CP. Furthermore, as the primary objective of botulinum toxin injection is to reduce tone in the calf musculature (enabling the dorsiflexors to strengthen into their new range of movement), and as FES is also applied to the tibialis anterior, strength of the dorsiflexors was also investigated.
Because one-third of all patients with CP present with hemiplegia,18,19 the target population of this study was limited to children with hemiplegia who exhibited spastic equinus during gait. Children between the ages of 4 and 6 years were considered for inclusion in the study because the gait pattern of this group is consistent.18 Subjects had to present with full passive range of motion (ROM) of the knee and ankle of the affected leg.
The databases of the pediatric departments of the local state hospitals were searched for potential subjects. Furthermore, children were referred by the physiotherapy departments of these hospitals and local schools for children with special needs for assessments for inclusion in the study.
Self-selected walking speed and isometric muscle strength of the ankle plantar flexors and dorsiflexors of the affected leg were assessed in this study.
A Sport Timer stopwatch was used to measure the time that it took each subject to complete the walking test. These values were needed to calculate the subject's self-selected walking speed for each test.
A hand-held dynamometer (Myometer; calibrated and adapted for the use on the lower limb by an independent mechanical engineer) was used to test the isometric strength of the ankle plantar flexors and dorsiflexors. Hand-held dynamometry has been shown to be a reliable and a valid way to objectively measure the strength of lower limb muscles.20,21 It correlates well with isokinetic strength testing and is portable and user friendly.20
Data Collection Procedure
All data were collected by the principal researcher and recorded on a data capture sheet.
The protocol followed was based on the one described by previous researchers,22 which the authors have shown to be reliable and to correlate well with other gait measures. A level 10-m walkway was marked with tape at floor level. Two meters were allocated before the start and 2 m after the finish line to allow for acceleration at the beginning and deceleration at the end of the walk, respectively. The subjects were then asked to walk from the start to the end of the walkway at their own pace and instructed to walk normally past the finish line. This walking test was repeated 3 times, with a 30-second rest period between consecutive walks during which the subject sat down and quietly looked at a children's storybook. Although walking aids (as used by each subject on a day-to-day basis) would have been permitted during testing, none of the subjects made use of any lower limb assistive devices. Orthoses were not to be worn during testing because these could have influenced the active ROM available at the ankle joint.
A stopwatch was used to measure the time taken to cover the distance from the instant at which the subjects crossed the start line to the instant they crossed the finish line. The walking speed (meters/seconds) for each of the 3 walks was then calculated and recorded on the data sheet.
Isometric Muscle Strength Testing.
After the third walk, the subject was given a 5-minute rest period before isometric muscle strength was tested, as the lower limbs need to be warmed up yet rested to allow maximal force production.20 The subjects were asked to lie in the supine position with their legs extended. This position allows maximal stabilization of the ankle and optimal positioning of the dynamometer.5 The researcher placed the hand-held dynamometer over the ventral aspect of the foot, with a foam layer between the force pad and the foot to provide comfort and skin protection. The researcher stabilized the ankle joint and held the dynamometer still while the subject exerted a maximal plantar flexion (PF) force against it. The subject was instructed to gradually increase the force of the contraction and not to contract the muscle explosively. The subject was asked to hold the contraction for 5 seconds because maximum force is usually reached during this period.20,21 Verbal encouragement was provided throughout. The maximum value of force production during these 5 seconds was then recorded on the data sheet.5
Isometric strength measurements for the plantar flexors were taken in neutral and in 10 degrees PF. All measurements were taken 3 times, and the maximum value for each ankle position was recorded. A rest period of 30 seconds was included between measurement repetitions to minimize the effects of muscle fatigue and reciprocal inhibition on the strength readings. Taking measurements in different ankle positions means that results are more representative of muscle strength through full ROM, as opposed to isometric measurements in a single position. Similarly, isometric muscle strength of the ankle dorsiflexors was tested in neutral and 10 degrees of dorsiflexion (DF).
Data Collection Procedure
The principal researcher randomly allocated each subject to 1 of 5 different treatment protocols (Figure 1) by drawing numbers out of a hat. These time intervals between botulinum toxin injection and the start of FES were based on findings from the literature concerning the optimum effects of botulinum toxin,23 and the carryover effects of FES applied to the tibialis anterior and the gastrocnemius muscles on active ankle ROM.24,25 Because no literature was found regarding optimal timing intervals for the introduction of FES after botulinum toxin, the time frame for the multiple-baseline approach used in this study falls into the time period deemed most effective for treatment interventions after botulinum toxin.23,26 Subjects were to continue with activities (including regular physiotherapy treatment) as per usual during the entire study.
Three baseline measurements were taken, spread over a period of 1 week. On the day after the third measurement, an orthopedic surgeon administered botulinum toxin with the subject under general anesthesia at a local hospital. The fourth measurement took place 4 to 5 hours after the injection.
Measurement session 5 took place on the day of the start of the FES program, ie, between 3 and 35 days after the botulinum toxin injection (Figure 1). At this time, the researcher demonstrated the use of the stimulation device to all subjects and their caregivers and gave instructions for home use.
Four weeks after the start of the FES program, data for measurement session 6 were collected. At that point, FES was withdrawn, and the subjects were required to return the stimulation device to the principal researcher. A seventh measurement session took place 2 months later to determine medium-term carryover effects.
FES was applied to the tibialis anterior and the gastrocnemius muscles by means of the Odstock 2 Channel Stimulator (O2CHS II) (O2CHSPI version 3.0, United Kingdom) The O2CHS II is powered by a 9-V battery. It permits the selection of either asymmetrical or symmetrical biphasic output. In this study, the former mode was selected to allow for maximum power output. A single-force sensitive foot-switch, placed in the ipsilateral shoe of the subject, was synchronized to trigger emission of 2 channels. The optimal position for the foot switch in the shoe was determined by the individual's pattern of weight-bearing.
Channel 1 was used to stimulate the tibialis anterior muscle. Emission was set to start when pressure was removed from the weight-bearing part of the foot. The output was set to last until initial contact, and thus adapted to the subject's walking speed (adaptive timing mode). The maximum permissible output (time control) was set at just longer than the normal swing period (between 0.5 and 6 seconds). An added period of stimulation (between 0 and 1.5 seconds) was added after initial contact, preventing foot slap by stimulating eccentric control by the tibialis anterior muscle (extension time). This ensured a more normal gait pattern.27 Final settings for each subject were determined on an individual basis. The rising and falling edge ramp times were also set on an individual basis to avoid a stretch reflex from being elicited.
Channel 2 was used to stimulate the gastrocnemius muscle. The configurations were the same as for channel 1, except that emission was set to start at initial contact. A delay of 0 to 2 seconds between channels 1 and 2 was set to allow for weight transfer during gait.
This algorithm follows the one being used in the Department of Medical Physics and Biomedical Engineering, Salisbury District Hospital, Salisbury, UK.27 These settings were used to determine the most effective electrode positions. Pals Plus self-adhesive electrodes were used. During electrode application, the knee was positioned in full extension to limit skin movement over the underlying bony structures. To maximize conduction, the skin of the application area was washed with warm water before application. The active electrode of channel 1 was placed over the common peroneal nerve, with the top edge of the electrode in line with the top of the fibula head. The inactive electrode was positioned 5 cm inferomedially to the active electrode, over the tibialis anterior motor point. If an ineffective contraction was produced, the positions of the active electrode were adjusted accordingly. The electrodes of channel 2 were placed over the medial and lateral heads of the gastrocnemius muscle. The electrodes needed to be positioned correctly because this allows a lower output current to be used for the same physiological effect and greater comfort during use. Stimulation intensity was then increased to produce the desired movements.
After the botulinum toxin injection and the relevant pre-FES phase, the principal researcher demonstrated the use of the O2CHS II to the subject and the caregiver and gave instructions for home use. The researcher set the device according to the individual's needs. Potential discomfort occurring from the use of the stimulator was discussed with the relevant caregivers. Caregivers were thus only required to apply the electrodes, connect the leads, and switch the device on. A user manual was also provided for their reference. The researcher marked the skin areas where the electrodes were to be placed with a marker to ensure proper positioning with each application. The subject was then required to practice walking at home with the device on for 30 minutes per day 5 times per week for 4 consecutive weeks (total of 20 sessions). Caregivers were instructed to retrace the outlines for the electrode positions with each application to ensure their proper positioning during subsequent use. The researcher called the caregiver on a weekly basis to inquire about any problems with the use of the stimulation device and to encourage compliance with the prescribed protocol. In addition, the researcher was telephonically available at all times to address any queries or problems and to conduct home visits (if necessary) to address problems and encourage compliance with the prescribed program.
Data analysis was conducted by an independent statistician at a local university. Data for each outcome measure for each subject were graphed to illustrate change in values over time. Repeated-measures analyses of variance were also conducted on each dependent variable to determine change over time. Subjects were included in the data analysis if they had been present during the first and last measurement sessions.
The study was approved by the Research Ethics Committee from the Health Science faculty of a local university. In addition, consent was obtained from the Department of Education for testing to be conducted at the participating schools and from the Medical Superintendent of the relevant hospital. Written informed consent for participation was also obtained from the parents or legal guardians of the subjects. Subjects were allowed to withdraw from the study at any time without negatively influencing their future medical care. Anonymity and confidentiality were maintained at all times.
All subjects participating in the main study presented with spastic hemiplegia due to CP and were between the ages 3 and 6 years (Table 1). All subjects cooperated well during baseline testing and the botulinum toxin injection. However, subject 1 developed a skin reaction at the botulinum injection sites shortly after the procedure and could thus not continue with the stimulation protocol until 8 days after the intended start of the program, during which time the subject was treated with antibiotics. The principal researcher subsequently conducted a home visit to again demonstrate the correct positioning of the electrodes to the caregiver and to ensure proper implementation of the stimulation device. The research design was thus adapted (Figure 1).
Subjects 2 and 5 subsequently refused to cooperate with the stimulator being applied to their lower leg. Subject 2 tolerated a submaximal stimulation intensity (intensity setting of 1 instead of a required setting of at least 4) but refused to walk with the electrodes attached to the leg. Subject 5 refused to allow the electrodes to be applied to the leg at all. Administration of the required stimulation during gait was thus impossible for these 2 subjects, even after repeated attempts and extensive reassurance (from both the relevant caregiver and the principal researcher). This included attempts to start the stimulation at very low intensity levels with the aim to later increase it to an acceptable level. Although 5 subjects participated in the main study, the researcher was thus able to compare subjects 2 and 5 (who did not receive the FES intervention) with the remaining 3 subjects (who did receive the FES). For this purpose, subjects 2 and 5 were grouped into a non-FES group, whereas subjects 1, 3, and 4 made up the FES group. Data analysis was thus conducted per subject and for the 2 groups.
Caregivers were telephonically reminded of the data collection dates 3 days before the respective day, which resulted in a 100% attendance rate. Although all caregivers were asked to record the dates and times of FES use at home, only 1 caregiver complied with this instruction. All caregivers attested to use the stimulation device for the entire 20 sessions, as prescribed.
A slight decrease in walking speed was noted after injection in 4 subjects and a slight increase in another, but none of these changes were significant. Between the injection and the commencement of the FES program, subjects 1, 3, and 5 showed slight increases in walking speeds, whereas decreases were recorded for the other 2 subjects (Table 2).
When comparing walking speeds immediately before (session 5) and after session 6, the stimulation program in the FES group, subject 4 showed the largest increase of 0.07 m/s (P = .19), but this was not maintained after intervention (Table 2). Average walking speed of subject 1 did not change during the FES phase, whereas that of subject 3 showed a decrease of 0.18 m/s (Table 2). Both subjects 1 and 3 showed an increase in walking speed during the withdrawal phase (Table 2). Although subject 2 did not receive FES, he showed a significant increase in walking speed of 0.27 m/s (P = .01) between measurement sessions 5 and 6, whereas walking speed of subject 5 remained constant.
Isometric Plantar Flexor Muscle Strength in a Neutral Ankle Position
Between the botulinum toxin injection (session 4) and the commencement of the FES phase (session 5), subjects 1 to 4 showed decreases in isometric muscle strength, whereas subject 5 showed an increase (Table 3). In a pre- and post-FES comparison, the largest strength increase was measured in subject 4 (+2.0 N). Subject 1 showed a significant increase of 1.7 N (P = .01) during this time, whereas subject 3 showed a decrease of 1.5 N (Table 3). Both subjects in the non-FES group also showed muscle strength improvements of 2.0 N at this time, even though they had not received the intervention as prescribed.
Isometric Plantar Flexor Muscle Strength at 10 Degrees PF
After the stimulation phase, the FES group showed a significant increase in isometric plantar flexor strength at 10° of ankle PF (P = .04). The largest increase was observed in subject 4 (+3.6 N; P = .06), compared with 2.7 N (P = .16) and 2.8 N (P = .52) increases for subjects 1 and 3, respectively. Subjects 1 and 3 were able to maintain these improvements for 2 months after the intervention had ended (session 7), but a decrease in plantar flexor muscle strength was measured for this time period in subject 4 (−4.1 N) (Table 4).
Although subjects in the non-FES group also showed an increase in isometric muscle strength over the time period of the intended stimulation phase, this change was smaller than in the FES group subjects (Table 4).
Isometric Dorsiflexor Muscle Strength in a Neutral Ankle Position
Of the subjects receiving the prescribed intervention, subject 3 showed the largest increase (+0.7 N) during the FES program, followed by subject 1 (+0.4 N). Isometric dorsiflexor muscle strength in neutral did not change for subject 4. For the 2 subjects who did not receive the FES intervention, a strength increase of 0.5 N was recorded in subject 2, whereas a decrease was observed in subject 5 (Table 5).
Isometric Dorsiflexor Muscle Strength in 10° of Ankle DF
Only 2 subjects were able to maintain the required 10° of DF for testing. At baseline, subject 1 (FES group) showed an average strength value of 0.01 N, whereas subject 5 (non-FES group) showed an average isometric muscle strength of 0.83 N. There was no significant change for this measure at any time for any subject.
The results of this study have shown a trend toward increased isometric plantar flexor muscle strength after FES, although subjects did not demonstrate changes in self-selected walking speeds.
Overall, FES after botulinum toxin injection had a negligible effect on gait speed for all the subjects participating in this study. The effect that botulinum toxin had on walking speed, however, differed among subjects. Measurement 5 for subjects 1 and 2 took place very soon after the botulinum toxin injection (11 and 7 days, respectively), and it could thus be assumed that the toxin had not reached its full potency at the start of the FES program. It is thus conceivable that the self-selected walking speed would not have decreased at this time. Subject 5, on the other hand, experienced a 35-day interval between the injection and the start of the FES program and also demonstrated a decrease in self-selected walking speed after botulinum toxin injection. The botulinum toxin could by this stage be expected to have resulted in maximal spasticity reduction (exposing underlying muscle weakness)26 with a resulting decrease in self-selected walking speed at this point.
When comparing walking speeds immediately before and after the stimulation program, some subjects showed increases in walking speed, whereas others showed a decrease or no change. However, the baseline speed measurements of most subjects fell within the range of speeds measured in children who are developing typically,28 and the small effect size for this outcome measure is thus understandable.
Although subject 4 had shown an increase in walking speed during the FES program, he was unable to maintain these improvements during the withdrawal phase. One possible explanation is the length of the prescribed treatment program. Subjects were supposed to use the stimulator for a total of 20 sessions over 4 weeks. This was a significantly shorter time interval compared with the length of exposure in a previous study,29,30 which was focused on adolescents with CP. Although the primary aim of FES in this study was as a facilitator of gait as opposed to a pure strengthening modality, muscle strengthening does take place and has also previously been shown to reduce an improvement in terms of function.16 In contrast, another study showed an increase in mean walking speed maintained for 4 weeks after combining FES treatment to the tibialis anterior and gastrocnemius muscles with botulinum toxin in children during an intensive 3-day treatment program.31 Although it is possible that the intervention of this study did not reach sufficient intensity levels to significantly improve walking speed, it has to be remembered that the walking speeds of the study subjects were comparable to those of children developing typically. FES was thus not expected to make a significant change in this variable.
An interesting finding of this study is that the subject who showed the largest increase in terms of plantar flexor muscle strength both with the ankle in a neutral and in a plantar flexed position during the FES period (subject 4), also showed the largest increase in self-selected walking speed. The results from this study thus correlate with previous findings,6 which have shown that improvements in muscle strength may positively influence functional abilities in CP. Although the researchers in this study targeted the knee flexors and extensors, available evidence seems to suggest that strengthening the lower limb may have a positive influence on self-selected walking speed in CP.
Effect of FES After Botulinum Toxin on Isometric Plantar Flexor Muscle Strength
Although FES is not primarily intended to increase muscle strength, the repeated use of muscles that were previously weak or inactive during a functional task should result in improved muscle strength on a cellular level and in improved neural drive. In a pre- and postintervention comparison, the largest strength increase with the ankle in a neutral position was measured in subject 4. These results suggest that an interval of 1 month between botulinum toxin and FES is optimal for strength gains to occur, although some improvements can be seen with shorter intervals as well. All these improvements were maintained during the withdrawal phase. Although the results from another study in children with CP32 combining botulinum toxin with electrical stimulation to the triceps surae complex reported no significant difference in terms of physical rating scores, ankle position at initial contact of gait, or spasticity as measured on the Modified Ashworth Scale, subjects exercised 3 times per week for 10 weeks. Training intensity thus might not have been sufficient to effect significant functional changes. No other studies investigating the influence of botulinum toxin on plantar flexor muscle strength could be found.
Effect of FES After Botulinum Toxin on Isometric Dorsiflexor Muscle Strength
Some subjects showed strength improvements immediately after FES. These strength gains were, however, not maintained at 2 months after FES. Although the changes for this outcome measure did not reach statistical significance, this study does suggest that FES can improve isometric dorsiflexor strength readings with the ankle in a neutral position, but that a longer intervention period may be needed for the gains to last beyond the intervention phase.
Timing of FES After Botulinum Toxin Injection
It is interesting to note that a functional improvement (increased walking speed) was recorded in the same subject (subject 4) whose plantar flexor muscle strength also improved. These results support the statement made by previous researchers4 that strength improvements in the triceps surae muscle group could be assumed to result in improved work output ratios around the ankle, resulting in lower levels of energy expenditure during gait. After the 2-month withdrawal phase, subject 4 in this study presented with a significantly reduced amount of plantar flexor muscle strength in 10° of PF. Walking speed had also decreased during this interval, whereas neutral plantar flexor strength had remained fairly stable. This finding supports the positive correlation between impairment and function discussed earlier because the loss of gastrocnemius muscle strength in this instance coincided with a certain reduction in functional capabilities. Although the intervention as administered to 1 subject thus seems to have had favorable outcomes, longer exposure to the intervention may be necessary to effect longer lasting improvements such as found by other researchers.33
Impairment- and function-oriented outcome measures did not correlate in the results of other subjects. The results of this study thus seem to suggest that a period of approximately 1 month between botulinum toxin and the commencement of FES to the lower leg may result in impairment and functional changes. After such a time interval, the chemodenervating effect of botulinum toxin would have resulted in maximal spasticity reduction. However, these results merely represent trends at this point and need to be confirmed by future studies.
Limitations and Recommendations
Although the single-subject research design has previously been shown to be appropriate for the use in the CP population,34,35 it has limitations.
There was potential for measurement bias because the researcher was not blinded to the intervention protocols.
Multiple Baseline Research Design.
Experimental research in the form of a single-subject design with a multiple-baseline approach across subjects was deemed appropriate for this study because this combination therapy is not only new in our developing country, but a novel treatment approach. Previous researchers36 have supported the application of single-subject research in the CP population because this study design places the focus on recognizable individual change that is relevant on a clinical level. A better understanding of the potential effects at impairment and functional levels is necessary before undertaking a larger more expensive randomized, controlled experimental design.
Understanding and cooperation can be a problem in the treatment of young children with FES. It is suggested that subjects eligible for FES treatment after a botulinum toxin injection be tested by applying stimulation to the lower leg before the botulinum toxin is administered. If the subject tolerates the device, this combined form of treatment is appropriate.
FES Intervention Protocol.
More research needs to be conducted into different FES protocols (eg, proximal versus distal muscle stimulation) and stimulation dosage and parameters, and their effect on specific outcomes to provide clinicians with feasible guidelines for implementing FES in clinical practice. In addition, neuromuscular electrical stimulation may be applied in a controlled environment such as a school or during physiotherapy sessions to adequately strengthen weak muscles before introducing FES as a home program and to familiarize the child with electrical stimulation.
The effect of FES on isometric plantar flexor and dorsiflexor muscle strength and self-selected walking speed had varying outcomes. The results of this study have shown that FES can increase isometric plantar flexor muscle strength. However, despite improvements in muscle strength, subjects in this study did not demonstrate changes in self-selected walking speeds. Furthermore, a 32-day interval between the botulinum toxin injection and the start of the stimulation program seems to have the greatest effect on most of the described variables.
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