INTRODUCTION

Physical therapy is the predominant therapy for reduction of spasticity in children with cerebral palsy (CP). Physical therapy is practiced in many different ways. However, the pure reduction of spasticity does not always improve function, 1 which should be the ultimate goal of all therapy. One evident limitation that may not always be addressed is the lack of muscular strength in the spastic muscle. This hampers function even if spasticity per se has been reduced. 1–4

Neuromuscular electrical stimulation (NMES) is transcutaneous application of electrical current to innervated, superficial muscle to stimulate muscle fibers, augment muscle contractions, increase range of motion (ROM), and enhance sensory awareness. 5–7 The broad term NMES involves the external control of innervated yet paretic or paralytic muscles by electrical stimulation (ES) of the corresponding intact peripheral nerves. In general, NMES has been applied so that the motor threshold is exceeded (high intensity) for a short period (15–60 minutes). 5

When the specific goals of therapy entail functional and purposeful movements, the specialized term functional ES (FES) is applied. FES therefore is a subset within the more broadly defined term NMES. 5

Threshold ES (TES) differs from NMES by being administered at the subsensory or sensory level (low intensity) for a longer period (overnight for eight to 12 hours). TES was first used in children by Pape et al, 8 who developed a program for treatment of disuse muscle atrophy in newborn infants who were ventilator dependent. Later, they used a similar protocol for children with CP.

In 1993, Carmick 6 reported on the clinical use of NMES in children with CP. She used ES as an add-on therapy so that it first gave a tapping sensation and sensory input without causing a fused contraction. When this sensation was tolerated by the child, the setting was increased to give fused muscle contractions. She analyzed the functional differences that occurred after the application of NMES to the lower extremities of three boys, aged 1.6, 6.7, and 10 years. The youngest child displayed an immediate improvement in his ability to walk and run symmetrically. The two older boys demonstrated a significant increase in locomotor efficiency. One boy’s Physiological Cost Index improved fourfold, whereas that of the other boy improved twofold. 6

The effect of electrically stimulating the anterior tibialis muscles of children with hemiplegic CP was studied by Hazlewood et al. 9 Ten children received NMES, applied daily for an hour for 35 days by their parents at home. Ten children acted as controls. During the stimulation, the intensity was set to cause dorsiflexion and the children had no scheduled exercises. The children were assessed prior to the treatment, and the outcome was assessed between six and 12 weeks later (mean = nine weeks). There was a significant increase in the passive range of dorsiflexion of the children receiving ES. There was also a significant increase in the power of the anterior tibialis muscle in the stimulated group. The power was estimated using the Medical Research Council grades of muscle power. 9

Comeaux et al 10 used gait analysis in 14 children with CP to study NMES given for 15 minutes to the gastrocnemius or gastrocnemius and tibialis anterior muscles of children during scheduled gait and/or functional activity. The children received no other physical therapy during this study. Each period was four weeks, including pre- and posttreatment periods. Stimulation treatments, gastrocnemius only or gastrocnemius and tibialis anterior, improved heelstrike dorsiflexion.

TES was used by Pape et al, 8 who applied subsensory TES overnight for six months to six patients with mild CP and noted a statistically significant improvement of function. At follow-up, after the children had been without TES for six months, there was a uniform decrease in scores. In a randomized study of children with CP who had undergone selective posterior lumbosacral rhizotomy more than a year earlier, Steinbok et al, 11 using low-intensity overnight TES, demonstrated improvement in the Gross Motor Function Measure score. A contradictory result was obtained by Dali et al, 12 who, in a randomized, double-blind, placebo-controlled study of 57 children with CP (age range, five to 18 years), failed to show any significant effects using TES for 12 months.

In a randomized, crossover study over 24 months Sommerfelt et al 13 evaluated the effect of TES applied to the antagonists of the spastic leg muscles in 12 children (age range, five to 12 years) with spastic diplegia and were unable to show any significant effect of TES on motor or ambulatory function.

In athletes, NMES has been shown to increase muscular strength, 14,15 and therefore it could be speculated that stimulation of this kind as an adjunct to physical therapy in children with CP would enhance the options for new active movements. 1,4,6,7,16

The aim of our open clinical trial was to administer sensory-level ES to the tibialis anterior muscle during physical therapy sessions as an add-on therapy to facilitate voluntary movement to find out whether ankle dorsiflexion thereby could be improved.

METHODS

Patients

The Department of Child Neurology at the Helsinki University Central Hospital is the secondary and the tertiary referral unit for a population of 1.4 million people living in the catchment area of this hospital. All the children with CP for whom treatment other than physical therapy is considered are referred to this unit. The clinical criteria for inclusion in this study were as follows: age three to 11 years, failure to make substantial progress using standard physical therapy, limited active dorsiflexion (defined as being less than the passive range or absence of selective active ankle dorsiflexion), no botulinum toxin treatment for the past six months, and the ability to cooperate during physical therapy sessions.

The first 17 children who fulfilled these criteria and were seen during a six-month period (November 1, 1998, to April 30, 1999) were recruited for this study. Informed consent was obtained from their parents. Their mean age was six years and five months (range, 3.8 to 8.9 years) at the start of therapy. There were nine girls and eight boys, and 11 of the children had hemiplegic CP. Two of the children with spastic diplegia used walking aids (tripod canes, ordinary canes). Six of the children wore hinged ankle orthoses, three wore dynamic ankle-foot orthoses, and the other eight individuals wore foot orthoses.

Ethical approval for the experiment was granted by the Ethics Committee at the Hospital for Children and Adolescents, Helsinki University Central in Helsinki.

Treatment

An ENS 931 EMPI (Enrauf Nonius, the Netherlands) unit was used as the neuromuscular electrical stimulator. The stimulator was tested and accepted by the electricity checkpoint at the Helsinki University Central Hospital. This equipment produces symmetrical biphasic waveforms. The battery-powered stimulator has two channels that allow two different muscles to be stimulated at the same time. The small size of the portable device allows the child to move freely. Self-adhering electrodes (EMPI, 5 × 5 cm) were placed on clean skin. The so-called active electrode was placed on the probable motor point of the tibialis anterior muscle, and the other electrode was placed on the same muscle distal to the active electrode.

Initially, the ES was introduced with a hand-held vibrator, called the “tickler,” applied to the therapist’s arm or a parent’s arm. The child was given time to feel, adjust to, and accept the sensation. ES was described as being like the tickler, and children were told that they would feel a tickling sensation but no pain. At the beginning of the therapy, stimulation was given at a frequency of 10–20 Hz, which produced a tickling sensation and sensory input but no muscle contraction. The goal of ES was to increase sensory awareness and muscle response. The current required to achieve this varied from child to child (variation of four to 20 mA). The pulse duration was fixed at 300 microseconds (set by the device). On-off times were set at one second on followed by one second off. If the sensation started to vanish, the intensity was increased.

The basic therapy for these children was physical therapy based on neurodevelopmental training techniques. This was not modified during the ES program, and the duration and frequency of physical therapy had been set according to the individual needs (Table 1). The mean frequencyof physical therapy was 1.8 times a week. During the study period of one calendar month, the children in this study additionally received ES during their physical therapy sessions. The stimulation time varied from 20 to 60 minutes (mean = 32 minutes). During the experimental period of one month, the children in this study received ES between four and 15 times (mean = eight times) according to the variations of the individual programs. The use of aids or orthoses before the stimulation period can be seen in Table 2.

TABLE 1: Main Characteristics of the Study Group of 17 Children TABLE 2: The Use of Aids or Orthoses Before and Nine Months After the Stimulation Period

Asessment

All 17 children were assessed before and after the ES period, and the assessments were repeated one, two, and nine months later. All assessments were carried out by the same persons (H.M. and R.J.).

The Goal Attainment Scale (GAS) was set for each individual leg in the following way: 0 = no change; 1 = significant increase of active selective ankle dorsiflexion; (>5°) with the knee flexed or extended; 2 = 1 + additional active functions; −1 = significant decline (>5°) of active dorsiflexion; −2 = −1 and additional deterioration of function.

With the child lying in the supine position with the hip and knee flexed (90°), active and passive dorsiflexion and plantar flexion of the ankle were measured using a standard goniometer. 17 Keeping the child in the same position but with extended hip and knee, these measurements were repeated. The mid-position (90°) of the ankle was used as baseline with the goniometer set at zero.

The differentiation of active inversion, eversion, toe flexion, and toe extension were assessed with the child sitting with freely hanging feet. This position enabled the children to see their feet, which helped them to perform the selective movement. Muscle function was tested using a scale modified after Daniels and Worthingham 18: 0 = no visible activation on request; 1 = visible contraction without active movement; 2 = visible active movement less than available passive ROM; 3 = visible active movement equal to available passive ROM.

Standing on one foot without support (seconds) was measured barefoot to eliminate variation caused by different types of orthoses. The number of hops on one bare foot was counted. Hopping on both feet was examined in the children with spastic diplegia and only the affected foot in children with hemiplegia.

In the statistical analysis, nonparametric analysis of variance was used primarily to assess the significance of the changes, and Tukey-Kramer statistic was used as the post hoc test. The alpha level was set to 0.05. The analyses were calculated by the number of feet treated (23 stimulated feet) because there were children with either diplegia or hemiplegia.

RESULTS

All the children tolerated the procedure well, enjoying the tickling electrical stimulator during the physical therapy sessions. All but one found the tickling feeling pleasant. However, the child who did not find it pleasant tolerated the stimulation better toward the end of the stimulation period.

Results Immediately After the Stimulation Period

The GAS showed progress (score 1 or 2) in 15 of 17 children (21 of 23 feet). In all, 12 children (14 feet) scored GAS 2 and five children (seven feet) scored GAS 1. The two scores of 0 were for two children with spastic diplegia, in which only one foot changed (Table 3).

The mean ROM of active dorsiflexion of the ankle increased significantly with the knee flexed (p = 0.0002) and with the knee extended (p < 0.0001). Passive dorsiflexion increased (p = 0.0133) and passive dorsiflexion with the knee extended increased, but the difference did not reach statistical significance (p = 0.0682). Active inversion also improved significantly (p = 0.0093), as did eversion (p = 0.032). There was a significant difference in active toe flexion (p = 0.0027) and active toe extension (p = 0.0022).

Standing on one foot (p = 0.0014) and hopping on one foot also improved but not to a statistically significant degree (p = 0.0645). This analysis was confined to those 15 children who did not use any walking aids and showed that seven children were able to hop at least once on one foot prior to the treatment, whereas 11 were able to do so immediately after the treatment period (Table 4).

TABLE 4: Effects of ES on Sensory Level in 17 Children with CP

Results Two Months After the Stimulation Period

The GAS showed a slight further improvement two months later compared with baseline as 16 of 17 children (22 of 23 feet) scored 1 or 2. Of these, 13 children (15 feet) scored 2 and four children (seven feet) scored 1. One child with spastic hemiplegia had returned to baseline level (Table 3).

Compared with the baseline level, the improvement in the ROM of active dorsiflexion of the ankle with the knee flexed and with the knee extended remained significant (p < 0.0001 for both). There was improvement in passive dorsiflexion of the ankle with the knee flexed (p = 0.0184), but passive dorsiflexion of the ankle with the knee extended remained unchanged (p = 0.1264).

Active inversion (p < 0.0001) and active eversion of the foot improved significantly (p < 0.0001). Correspondingly, the improvement of active toe flexion (p < 0.0001) and extension remained significantly improved (p < 0.0001) compared with the situation before treatment.

Standing on one foot remained improved (p = 0.0088), whereas hopping on one foot now had improved significantly (p = 0.0025).

No statistically significant differences (Table 4) were found when the results were analyzed using the Tukey-Kramer multiple comparisons test to analyze the function two months after the cessation of stimulation compared with the results obtained immediately after the stimulation period.

Results Nine Months (± Two Months) After the Stimulation

Compared with baseline, the improvement in the GAS score remained as 16 of 17 children (21 of 23 feet) scored 1 or 2. Within this group, eight children (10 feet) scored 2, and eight children (11 feet) scored 1. One child with spastic diplegia lost the skills that she had had at two months and returned to her baseline functional level (Table 3).

Compared with baseline recordings, the significant improvement in the ROM of active dorsiflexion of the ankle remained both with the knee flexed (p < 0.0001) and the knee extended (p < 0.0001). Passive dorsiflexion with the knee flexed remained significant (p = 0.0362) but not with the knee extended (p = 0.2671).

The improvement in active inversion and active eversion remained significant (p < 0.0001), as did active toe flexion and extension (p < 0.0001). Interestingly, the improvement in standing on one foot still remained statistically significant (p = 0.0126). The same was true for hopping on one foot (p = 0.0126).

Comparing the differences in function nine months after the cessation of stimulation with the differences in function just after the cessation of the treatment period, statistically there was improvement only in toe extension (p = 0.0048). Comparing the results obtained two months after cessation of treatment with those obtained immediately after cessation, there were no statistically significant differences.

DISCUSSION

The history of ES is long, dating back to at least 1775. 5 However, in children, different ES techniques have been used more extensively during the past few decades and especially in children with CP. ES treatment in general has been applied either during a physical therapy session 6,7,19 or by parents at home during free activity 9,10 or overnight. 8,11 The potential advantage of ES is that it can enhance sensory input, thereby increasing the child’s awareness of muscle function. The positive effect of ES may be mediated through activation of the muscle fibers or through activation of cutaneous and muscle afferent pathways that modulate excitability levels of interneurons and α motor neurons. 4,5,20 In a number of studies using TES, the stimulation was used at the sensory or subsensory level and was applied overnight during sleep. 8,12,13,17 The reported results have been very contradictory, perhaps reflecting subtle but important differences in the protocols. 21

Generally, NMES is administered so that muscle contraction is elicited. The main underlying muscle impairment in equinus gait in children with CP usually is the spasticity of the triceps surae muscle. Therefore, the weak antagonist muscles, the ankle dorsiflexors, usually have been the target of neuromuscular ES in children with spastic hemiplegia or diplegia.

A different approach is represented in Carmick’s case report in which NMES was used for strengthening the spastic gastrocnemius in a child with spastic diplegia and showed a positive result. 19 Similarly, Comeaux et al 10 demonstrated an improvement in both ROM and gait patterns after NMES applied to the gastrocnemius or gastrocnemius/tibialis anterior. In both studies, the favorable results were attributed to reciprocal inhibition. Stimulating the tibialis anterior inhibits the gastrocnemius and stimulating of the gastrocnemius inhibits the tibialis anterior so that coactivation of the two muscles is diminished. In addition, NMES provides proprioceptive input and acts as a type of biofeedback. 5,20

Several authors have pointed out that the terminology in the field of neuromuscular ES has not been used consistently, and this has caused problems in interpreting and comparing results of different studies. Our study differs from all previous ones by using ES at the sensory level only. It differs from Carmick’s report 19 by not reaching muscle contraction. In comparison with the TES used by Pape et al, 8 it should be noted that the stimulation level is similar, but the duration was short (30 to 60 minutes). A reason for using a short treatment was derived from reported experiences with NMES, 5,6,10,19 which have shown that even 10 minutes of stimulation can cause muscle fatigue. This is especially important because the muscles usually are weak in children with CP and become tired very rapidly during active practicing. Another reason for choosing this protocol was that this duration appeared to be well tolerated by the children and their families. Because this treatment was planned as an add-on therapy, it was considered advantageous to apply the stimulation simultaneously with the physical therapy. This design contributed markedly to the variability of the treatment intensity. We also found that the intensity of physical therapy tended to be higher in spastic diplegia than in hemiplegia. The evident drawback of this design is the relatively low or individually very variable frequency of stimulation sessions, but the aim of the study was not to change the children’s basic physical therapy program. The on/off time usually used in NMES 6,7,9,10 has been reported to vary from four to 15 seconds/12 to 20 seconds. In our study, we chose the shorter on/off ratio (both 1 second) because the children felt that it was comfortable and easy to identify.

The overall aim of this study was to find out whether a low-intensity add-on treatment of this type would yield any measurable effects, and therefore we confined our assessments to ROM and the GAS. Usually only passive ROM has been assessed, but because active ROM is functionally more important, we also measured active ROM. Probably the most important observation was that all children gained new active muscular movements (inversion/eversion and toe flexion/extension). The fact that the new skills did not vanish during the follow-up suggests that motor learning occurred. 2,19 From a functional point of view, it is important that the original supporting dynamic orthoses of eight children could be replaced by less supporting ones, such as foot orthoses during the follow-up period of nine months. Some of parents of the children with hemiplegia reported that their children did not need any support when cycling. When the results were analyzed and the children were split into two groups, younger or older than seven years of age, it was found that age analyzed in this way did not influence the outcome.

Based on previous studies, 1,4,6–8,15 we assume that the favorable effects shown by sensory-level ES can be explained as follows: Giving ES at the sensory level helps the children to localize stimulated muscles during exercise. This in turn increases the activity of the children during the therapy sessions and when practicing by him- or herself, the muscles are not overfatigued. This interpretation is, however, clearly speculative. The lack of a control group means that no adjustment for maturation-induced possible spontaneous development could be made. Because physical therapy and sensory-level ES were used simultaneously, no definite conclusions regarding the effect of the two components separately can be drawn. Recently, McDonough et al 22 presented data from a study of 60 children (ages five to 16 years) with CP who were randomized into three groups to receive NMES (15 minutes 5 days per week), TES (overnight 5 days per week), and physical therapy. The duration was four months, and strengthening of the quadriceps was the goal of the therapy. Assessment by Gross Motor Function Measure and Lifestyle assessment questionnaire showed that TES and NMES were significantly superior to physical therapy. This observation supports the claim that TES or NMES have specific effects, which are not directly comparable with those of physical therapy. 21,22

CONCLUSIONS

These preliminary data show that there may be a place for sensory-level ES as an adjunct to physical therapy in children with CP because the children in our study not only attained the set goals but also acquired new muscular activities. The definite place of ES therapy in children with CP can be judged only after controlled trials combining several regimens of therapy also addressing function have been carried out.