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Review

Neuromuscular electrical stimulation for children with cerebral palsy: a review

Philip A Wright,1 Sally Durham,2 David J Ewins,2,3 Ian D Swain1,4
of Clinical Sciences and Medical Engineering, Salisbury District Hospital, Salisbury, Wiltshire, UK 2Douglas Bader Rehabilitation Centre, Queen Marys Hospital, Roehampton, London, UK 3Centre for Biomedical Engineering, University of Surrey, Guildford, Surrey, UK 4 School of Design, Engineering and Computing, University of Bournemouth, Bournemouth, Dorset, UK Correspondence to Dr Philip Wright, Department of Clinical Sciences and Medical Engineering, Salisbury District Hospital, Salisbury, Wiltshire SP2 8BJ, UK; philip.wright@salisbury.nhs.uk Accepted 7 September 2011
1Department

ABSTRACT The aim of this review paper is to consider the application of neuromuscular electrical stimulation (NMES) to improve gait or upper limb function in children with cerebral palsy (CP). Although most NMES research has been directed at adults with neurological conditions, there is a growing body of evidence supporting its use in children with CP. In line with a recent meta-analysis, the use of electrical stimulation to minimise impairment and activity limitations during gait is cautiously advocated. A detailed commentary on one of the most common lower limb NMES applications, tibialis anterior stimulation (either with or without gastrocnemius stimulation) is given. Although there is a lack of randomised controlled trials and a predominance of mainly small studies, this review further concludes that the balance of available evidence is in favour of upper limb exercise NMES offering benets such as increased muscle strength, range of motion and function in children with CP. The use of dynamic splinting with NMES has been shown to be more effective than either treatment on its own in improving function and posture. There is at present little published work to support the application of botulinum toxin type A to temporarily reduce muscle tone as an adjunct intervention to NMES in this population, although the presence of parallel applications to manage similar symptoms in other muscular disorders is noted.

INTRODUCTION
Electrical stimulation is not a new technique. It dates back to the Ancient Greeks who used rubbed amber and torpedo sh to produce a number of physiological responses, primarily to cause muscular contractions. Its development followed advances in physics by Volta and Faraday during the 18th and 19th centuries which led to more reliable, controllable sources of electricity, as well as advances in neurophysiology as a result of the work of Galvani and Duchenne. Following this, various researchers showed that denervated muscles only responded to stimulation by connecting and disconnecting a direct current source and not to alternating current. However, in upper motor neuron conditions, such as cerebral palsy (CP), it was found that muscle contraction may result from stimulation of an intact motor neuron by an alternating current. There are a number of different types of electrical stimulation ranging from low-level stimulation, such as that used for pain relief, transcutaneous electrical nerve stimulation (commonly known as TENS) and threshold electrical stimulation where there is no activation of the muscle, to neuromuscular electrical stimulation (NMES) where there is an actual muscle contraction. This last type of
364

electrical stimulation, NMES, is the subject of this review and can either be used cyclically as an exercise, or linked to a functional goal where it is usually known as functional electrical stimulation (FES). NMES has been used to treat a wide range of clinical conditions. Readers can consult the web sites of the International Functional Electrical Stimulation Society (www.ifess.org) and the International Neuromodulation Society (www.neuromodulation.com) for additional information. The vast majority of NMES research has been directed at adults with disabilities resulting from a wide range of neurological conditions affecting the upper motor neuron system, including stroke, multiple sclerosis, spinal cord injury and head injury. Nevertheless, there is a growing body of evidence supporting the application of NMES for children with CP.14 The aim of this review is to present a succinct clinically oriented evaluation of the current evidence base underpinning the use of NMES treatment regimes to improve gait or upper limb function in children with CP. In addition, specic consideration is given to the use of NMES alongside the use of adjunct orthotic interventions and local injection of botulinum toxin type A (BTX-A). While four lower limb reviews have been published to date in MEDLINE-cited journals on the use of NMES for CP, only Kerr et al1 and Merrill3 have also reviewed concurrently the important topic of upper limb applications of NMES. The present review is timely because a number of studies relevant to the scope of this paper were not analysed in the reviews by Kerr et al1 525 or Merrill.3 6 9 11 14 1618 23 2628 Moreover, the nature of this review as being a succinct clinically oriented analysis differs from Merrills review, which was a preface to an extended discussion of potential future technological developments.

METHODS
A search for English language articles was conducted on MEDLINE using the terms electrical stimulation and CP. This literature was complemented with appropriate cross-referenced articles. Given editorial constraints, only articles that the authors considered to be of major interest or relevance were included.

NMES for gait improvement

We can consider the application of NMES to the lower limb of children with CP under four headers: NMES applied for exercise. NMES applied during gait cycle. Combined use of NMES and BTX-A. Developments in percutaneous and implanted electrical stimulation.

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Review
Much of the literature on the application of NMES both as exercise and during the gait cycle has been reviewed extensively.1 4 Kerr et al1 concluded that many studies recorded improvements in strength and function, but these often had limited statistical power. In addition, they suggested there was a need for further work with more rigorous study designs and follow-up, larger sample sizes and homogeneous patient groups. The meta-analyses conducted by Cauraugh et al4 demonstrated that electrical stimulation produced medium effect sizes on gait outcomes. They considered that their ndings corroborated earlier work by Kerr et al1 and Hazlewood et al. 26 A subsequent review of FES for gait assistance also noted that further research on stimulation protocols was needed to provide clinically relevant results. 2 There has, however, been relevant work published in this area which was not included in these reviews or which given the purpose of this paper merits further amplication. All the papers reviewed are summarised in table 1. statistically signicant improvements in peak dorsiexion in swing and in footoor angle at initial contact through stimulation of the dorsiexors in swing. Furthermore, clinically signicant improvements in dorsiexion during swing and at initial contact were seen in three of ve children while stimulation was being applied to the dorsiexor muscles in individually tailored programmes of NMES during walking.7 Nevertheless, equivocal results were observed in the remaining three children in this study who received stimulation for both ankle dorsiexion during swing and knee extension (during swing or stance as appropriate).7 Another study described an immediate effect of applying percutaneous intramuscular NMES in eight children with CP.8 The authors reported a trend towards improved ankle kinematics while stimulation was applied to tibialis anterior during swing. However, they observed statistically signicant outcomes when calf stimulation during stance was added. This was presumed to be due to improved coordination of muscle activation and sensory feedback provided by stimulation to the muscles around the joint at the appropriate time during the gait cycle. These small studies have concentrated on the immediate changes seen on applying stimulation functionally. Longer-term changes such as improvements in the asymmetries of temporal spatial data following stimulation of the anterior tibial muscles during swing in children with hemiplegic CP have also been investigated. 23 Plastic changes occurring in response to a repeated stimulus are suggested as the mechanism for this motor learning. Other investigators report positive effects on swing phase kinematics following stimulation of the calf muscles (gure 1). The rationale for targeting the calf muscles for a duration slightly longer than the stance phase is based on the premise that stimulation has the potential to: interrupt the constant state of activity in the spastic gastrocnemius; allow reciprocal inhibition of tibialis anterior; generate a stretch reex to the tibialis anterior; and strengthen the weak calf muscle. 27 Further, assuming a potential for motor relearning, these changes may be maintained after the intervention period. Case studies by Carmick reported improvements in selective control, range of active dorsiexion and foot position at initial contact during and following prolonged periods (312 months) of stimulation of the calf during stance combined with gait training. 31 32 In addition, increased dorsiexion at initial contact was observed following both calf stimulation during stance, and calf stimulation with anterior tibial muscle stimulation during swing, in a group of 14 children. 27 De nitive studies still need to be undertaken in this area, but the review by Seifart et al2 would suggest that stimulation of the gastrocnemius with or without tibialis anterior may effect greater gait improvements than stimulating the tibialis anterior alone.

NMES applied for exercise

Improvements in hamstring spasticity and lower limb function, 5 and quadricepshamstring co-contraction,19 have been recorded through an extended period of quadriceps exercise stimulation. Khalili and Hajihassanie18 also found improvements in hamstring spasticity (and passive knee extension) when stimulation of the quadriceps was added to a passive stretching regime, however, they considered the change for the experimental group as a whole not to be clinically relevant. They concluded that the marginal size of the effect may be due to the short duration (30 min, three times per week for 4 weeks) and relatively low-intensity regimen investigated, and that larger sample sizes are required. Stackhouse et al20 investigated the effects of strength training using percutaneously implanted stimulation to quadriceps femoris and triceps surae. In this preliminary study, greater increases in normalised force production were seen in both muscle groups when compared with results from a group undertaking volitional training only. An improvement in walking speed in the stimulation group was also noted. In addition to quadriceps stimulation, stimulation to gluteus medius bilaterally has been shown to result in a signicant improvement in gait temporal spatial parameters and in hip adductor tone.6 Stimulation was applied during the gait cycle so in that sense it was used functionally, but it was not synchronised with stepping. These individual studies seem to support the conclusions reached in the review by Kerr et al1 and echoed by Cauraugh et al4 that many studies recorded improvements in strength and function. The use of NMES to strengthen lower limb muscles and increase range of motion, and the resultant effect of this on gait has also been investigated. 21 26 29 Stimulation was not applied during a functional task in these studies, and any changes in range of motion and strength did not result in improvements in walking pattern. Some authors have suggested that it may be more effective to combine NMES with task-specic or functional training. 30

Combined use of NMES and BTX-A

BTX-A, acting as a neuromuscular junction block, can reduce tone and offer a time window in which NMES may be used to stretch the agonist and strengthen the antagonist muscles in children with spasticity.7 Table 2 gives details of studies investigating what benet, if any, can be offered by introducing an NMES regime post injection of BTX-A in the lower limb of children with CP. Some authors have concluded that combined BTX-A and NMES is not superior to BTX-A alone for the treatment of equinus in CP.9 However, others have found NMES offered some benets over BTX-A in early improvement of range of motion and maintenance of gait improvement in dynamic equinus.10 There were similarities in terms of muscles injected
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NMES applied during gait cycle

The two main approaches reported using NMES during walking to improve swing dorsiexion have been largely contradictory, either targeting the anterior tibial muscles during swing or conversely the calf muscles during stance phase. In some other cases, both muscle groups have been recruited, mimicking neural ring patterns. Van der Linden et al22 reported
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Review
and review protocols; however, as shown in table 2, there were differences in the stimulation regime. The effect of NMES on the injected muscles with stimulation timed to the walking cycle in three children who started NMES at different intervals post injection has also been investigated.11 NMES was found to improve isometric plantarexor muscle strength, but did not produce changes in self-selected walking speeds or isometric dorsiexor muscle strength. These results also suggested that starting NMES 32 days post injection was most effective in this small study. Further investigation is required to establish if NMES is a valuable adjunct to BTX-A, and if so, what regimes should be used and when should they start. with CP, cyclic NMES was applied to the wrist extensor muscles of eight children with hemiplegic CP. 35 Statistically signicant improvements in hand function and active wrist extension were measured, although no signicant changes were observed in measurements of wrist extension moment. These authors also included anecdotal comments from the children and their parents, such as an increased awareness of the limb, improved coordination of both hands used together, or greater prociency in carrying out tasks that required grasp and release activity and hand manipulation which were consistent with those of an earlier case report. 34 In a subsequent study, cyclic NMES was applied reciprocally to wrist exor and extensor muscles of a group of eight children with CP using a rationale similar to that previously discussed in the lower limb example of stimulation of ankle dorsiexors and plantarexors.13 The children were specically asked to work with the NMES as it initiated movement. Statistically signicant improvements in active wrist extension were demonstrated (as in the previous study) 35 but also in wrist extension moment. The authors concluded that a possible mechanism of NMES improving wrist extensor muscle strength was through decreased exor coactivation, noting that a trend toward reduced coactivation of exors and extensors was observed in six children. In a further study on the effect of reciprocal NMES of wrist extensors and exors of nine children with CP, therapists maintained the wrist in an extended position, offering manual resistance while children were encouraged to compete with the therapist.14 Signicant increases in wrist extensor and exor strength were measured while the wrist was maintained in an extended position. The wrist extensors also demonstrated signicant increases in strength in neutral. No signicant changes in passive stiffness of wrist exors, hand function or mean wrist angle during manual tasks was measured, possibly because the intervention may not have been sufciently prolonged or aggressive. The authors suggested that the intervention had resulted in a shift of the wrist extensor lengthtension curve. These studies lend mounting support to the premise that NMES may assist with muscle strength and function in the upper limb of children with CP and additional benets may occur when children also attempt to complement NMES with volitional movement. However, the comment that previous reviewers have made still applies; there is insufcient statistical power to provide conclusive evidence of this.1

Developments in percutaneous and implanted electrical stimulation

Most reported NMES work has involved surface electrodes, that is, electrodes placed on the skin. This approach is non-invasive, but it has the following limitations: accurate placement of electrodes, isolation of a response from specic muscles, the need for sensory tolerance and a practical limit on the number of channels that can be used at a given time. 33 Therefore there has been interest in the use of percutaneous and implanted stimulation systems. Several authors have successfully used percutaneous lower limb muscle stimulation in children with CP.8 12 24 33 In one single case study,12 greater improvements in dorsiexion were found with percutaneous than with surface stimulation (eg, mean increase of 10.6 in peak dorsiexion during swing with percutaneous stimulation and 4.6 with surface stimulation when compared with the no stimulation condition). The authors found that (sagittal plane) ankle absorption work decreased during the gait load phase with both types of stimulation, but that ankle generation work was increased only with percutaneous stimulation. In a recent review of NMES in CP, potential limitations of percutaneous stimulation systems were noted, including that the leads present a persistent infection route and that they may also wear and break, requiring additional surgical interventions. 3 Although not reported in the studies previously mentioned, these are important issues, and restrict the use of these systems outside of research studies. An implanted system may offer a solution to the problems presented by both surface and percutaneous systems, and an approach for a fully implanted stimulator that may be appropriate is also outlined in that review. 3

NMES for restoration of upper limb function

There are fewer reported applications of NMES to the upper limb of children with CP than the lower limb. We can consider these under three headers: NMES to assist with muscle strength and function. Combined use of NMES and orthoses. Combined use of NMES and BTX-A.

Combined use of NMES and orthoses

In the rst case report of NMES used in combination with an orthosis, a child who had previously used NMES was supplied with a dorsal wrist splint made out of orthoplast that maintained 10 of wrist extension and helped provide wrist stability. 36 After 9 months of wearing the splint, supplemented by weekly NMES sessions, the splint was discontinued as the child could maintain hand function without it. Details of this and other papers reviewed in this section are given in table 4. Following this, a retrospective study was published on 19 children and young adults with CP who took part in a clinical programme involving 1 h per day of NMES with an orthotic intervention known as dynamic splinting (DS).25 In DS, a restorative force is applied by an orthosis often by means of a variable tension spring loaded hinge (gure 2). In this case, NMES was applied to achieve wrist and nger extension while DS promoted extension of the wrist and elbow joints. A static splint was worn during the night to prevent wrist exion.
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NMES to assist with muscle strength and function

The rst case studies to demonstrate the feasibility of applying NMES to the upper limbs of children with CP were reported in the early 1990s. 28 34 Functional improvements such as increased awareness and spontaneous use of the impaired arm and hand, and enhanced grasp and release abilities were also reported. 34 Nevertheless, they presented insufcient evidence to reach a judgement on the general applicability of NMES for the upper limb of children with CP. Further details of these and other papers reviewed in this section are given in table 3. In the rst report on the application of cyclic NMES as a single intervention to the upper limb of a group of children
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Table 1
Muscles stimulated Right QR Results Session duration, frequency and mode

Details of studies in neuromuscular electrical stimulation to assist with muscle strength and function (lower limb) section

Reference 1 21 GM bilaterally

Study design

Age range n (years)

Daichmann et

al5 Increase in right QR strength, decrease in right HS spasticity, improvements in mobility elements of PEDI results Temporal spatial parameters (apart from step width) and hip adductor tone of the treated group

Case study

13

Al-Abdulwahab et al6

Postans and Granat7 8 8 DF, PF, QR (determined through gait analysis) Percutaneous stimulation of TA and GA of involved limb DF with balanced eversion and inversion For NMES to AF only group (n=5), clinically signicant changes in stance phase kinematics for three children *Peak DF in swing (more affected extremity) and DF at initial contact (less affected extremity) for TA+GA condition. Trends of improvement in DF kinematics seen for TA and GA only conditions

Pre/post test design. Data compared with healthy (n=20) and control CP (n=10) groups ABAB Used functionally during testing on 2 days

7.42

Approximately 30 min every other day for 6 weeks. Exercise only 15 min three times per day for 7 days. Stimulation applied mainly during walking but not timed to the gait cycle

8.917.5

Orlin et al8

AB

7.911.8

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1 Used functionally for 1 week for each NMES set up (TA only, TA and GA, and GA only) for approximately 2 45 min daily. Four-channel and two-channel stimulation used for diplegic and hemiplegic children, respectively Assessed functionally during walking (one test day) 11 QR Increases in DF at initial contact, peak in swing and mean in swing, greater with percutaneous stimulation. Ankle absorption work improved (decreased) with both types of stimulation. Ankle generation work increased only with percutaneous stimulation. Greater isometric force produced with percutaneous than surface stimulation Marginal improvement in HS spasticity and passive knee extension 30 min three times per week for 4 weeks. Exercise only 5 Right QR 30 min daily for 3 months. Exercise only. Stimulation also used orthotically during tests 15 min for each muscle group, three times per week for 12 weeks. Exercise only 11 Percutaneous stimulation of QS and TS (Seated tests) average motion velocity and a decrease in motion jerk and in knee torque after training; QRHS co-contraction following training, but not during stimulated assisted motion TS maximum voluntary isometric contraction normalised to body weight for NMES group compared with volitional group, ns for QS. Walking speed for NMES group, ns walking speed for volitional group following intervention 60 QR (vastus medialis) bilaterally 14 DF with balanced eversion and inversion and QR For NMES: ns in strength or function compared with placebo; impact of disability at end of treatment (not at 6-week follow-up) Peak DF angle and footoor angle for both groups when comparing walking with and without FES. Walking speed for both groups when comparing walking with and without FES; ns between NMES and control groups in deviation of gait pattern from normal, footoor angle, DF in swing angle, or passive DF when comparing before and after intervention results Heeltoe contact pattern and symmetry both improved following intervention with FES (no statistical analysis) NMES: 1 h daily 5 days per week for 16 weeks. Exercise only NMES: 1 h daily to either DF (n=5) or QS (n=2) 6 days per week for 2 weeks. Exercise only. Followed by FES of DF and QR during gait for 8 weeks. Stimulation also used orthotically during tests for both NMES and control groups FES of DF during gait for 12 weeks 4-week (minimum) exercise for no more than 1 h per day, followed by functional use 12 DF 17 BF, GM, Gmax, PAM, VL, ns differences in passive range, temporal spatial parameters or gross motor VM, Sol, TA (not all used function between groups before or 1 year after intervention. FES group in all children) underwent 4.5 fewer ablative procedures per child 20 TA of involved limb Passive DF in NMES group. Active DF in NMES group compared with control group post intervention but not pre intervention. TA muscle power in NMES group 1 h daily for 35 consecutive days. Exercise only continued

Pierce et al12

Comparison of surface and percutaneous stimulation

11

Khalili and Hajihassanie18

Katz et al19

Randomised (within child), one child dropped out Case controlled

11.614

2.84.1

Stackhouse et al20

Kerr et al21

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Van der Linden et al22

Group comparisons. 812 NMES (n=6); volitional control (n=5); one child in NMES group excluded from analysis Randomised (NMES 516 n=18; placebo n=22; and TES n=20) Randomised (NMES 513 n=7; control n=7); one child (NMES group, QS) dropped out

Durham et al23

ABA, two children dropped out

615

Johnston et al24

Group comparisons. NMES with limited surgery (n=9); traditional surgery (n=8)

612

Hazlewood et al26

Randomised (NMES n=10; control n=10)

512

Review

367

368
Muscles stimulated *DF during gait for both targeted FES interventions Results Session duration, frequency and mode 14 GA and TA 22 GMax Targeted FES of GA during 15-min therapy session three times a week for 4 weeks followed/preceded by a similar programme with GA and TA NMES: 1 h a day 6 days per week for 8 weeks. Exercise only 3 4 2 For NMES: ns in hip extensor strength, gait analysis, passive limits of hip rotation, section E of gross motor function measure when comparing NMES group with control group TA, TS, GA, Sol, Gmax, HS Improvements in physiological cost index measured in two children (not all used in all patients) together with observations of improved gait function and symmetry TA, TS, Gmax, HS (not all Improvements in heel strike, foot alignment, function, balance, active and passive used in all patients) DF range of movement and walking speed. (Not all observed in all children) Gmax, GM, VM, VL, GA, Measured improvements in lower extremity ranges of motion, spatial gait TA characteristics, improved gross motor function Approximately weekly sessions of unspecied duration of targeted FES for between 6 weeks and 8 months Unspecied frequency and duration of targeted FES sessions as required Two 15-min sessions of FES 5 days per week for between 7 and 10 months. Children asked to work with FES

Table 1

Continued

Review

Reference

Study design

Age range n (years)

Comeaux et

al27

ABCA (n=7), ACBA (n=7)

9.13.8

Van der Linden et al29

Randomised (NMES n=11; control n=11)

8.52.8

Carmick31

Case series

1.610

Carmick32

Case series

1.74.7

Bertoti et al33

Case series percutane ous stimulation

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Skin surface electrodes used unless stated otherwise. , , * indicates statistically signicant (p<0.001, p<0.05 and p<0.0055, respectively) increase; and indicates statistically signicant (p<0.001 and p<0.05, respectively) decrease; ns indicates no statistically signicant difference (p>0.05); indicates plus or minus one SD. AB, baseline-intervention; ABC, baseline-intervention1-Intervention2; ABAB, baseline1-intervention-baseline2-intervention; ABA, baseline-intervention-follow-up; ABCA, baseline-intervention1-intervention2-follow-up; AF, ankle exors; BF, biceps femoris; CP, cerebral palsy; DF, dorsiexion; FES, functional electrical stimulation; GA, gastrocnemius; GM, gluteus medius; Gmax, gluteus maximus; HA, hip adductors; HS, hamstrings; NMES, neuromuscular electrical stimulation; PAM, posterior adductor magnus; PEDI, pediatric evaluation of disability inventory; PF, plantarexion; QR, quadriceps; Sol, soleus; TA, tibialis anterior; TES, threshold electrical stimulation; TS, triceps surae; VL, vastus lateralis; VM, vastus medialis.

Figure 1 Surface electrodes positioned to apply neuromuscular electrical stimulation to stimulate right gastrocnemius muscle activity. The electrodes are connected to an Odstock Dropped Foot Stimulator (Odstock Medical Limited, The National Clinical FES Centre, Salisbury District Hospital, Salisbury, UK).

Following at least 3 months of intervention, most participants improved their Zancolli classication by two grades or more. 37 Participants also demonstrated improvements in quality of movement and better control and use of their hand. However, the authors noted that continued application of the intervention, albeit less intensively, was necessary to maintain these improvements. A randomised trial was carried out by some members of the same research group in order to determine whether the combined use of NMES and DS was more effective than use of either intervention alone.15 Twenty-four children with CP were allocated randomly to three groups: NMES, DS (wrist and metacarpophalangeal joints), or DS with NMES (each applied for 1 h per day). Over the 6-month intervention statistically signicant improvements in hand function and posture were observed only in the group receiving the combined intervention. In a more recent study on the combined use of NMES and DS, its use was investigated in six children with CP with xed contractures at the wrist or elbow.16 The combined use of NMES and DS was shown to be feasible and there was good participant compliance. The intervention appeared to demonstrate a greater impact on upper limb function in children who were treated for wrist contractures. However, clinicians involved identied that difculty with supination was one of the main reasons why some children failed to benet more from the intervention. A combined NMES and DS intervention that incorporated assistance with supination could be useful for further work. There is strong evidence that the clinical application of NMES with DS may be appropriate for improving function, strength and hand posture in the upper limb of children with spastic hemiplegic CP. The literature to date suggests that regular review and an ongoing programme of the combined intervention will be necessary to maintain any clinical gains.

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Table 2 Details of studies in combined use of neuromuscular electrical stimulation and botulinum toxin type A (lower limb) section
Reference Detrembleur et al9 Study design Controlled (control n=6; NMES group n=6) Age range n (years) 4.756 12 Muscles stimulated Soleus and GA BTX-A sites Soleus and medial and lateral GA. HA in 7 patients (3 NMES and 4 control) Soleus and medial and lateral GA. HS and PT in two children Results (differences with NMES) For a range of clinical and gait variables, combined treatment not superior to BTX-A alone at 1, 3 and 6 months post BTX-A injections #Passive ankle ROM after 2 weeks in NMES group only (in both groups at 3 months). #Total PRS and foot equinus scores in NMES group at 3 months after injection Two children did not use NMES. Trend towards increased isometric PF muscle strength. No changes in selfselected walking speeds or isometric DF muscle strength Session duration, frequency and mode 30 min six times a day for 3 days, beginning on day of treatment with BTX-A. Exercise only 30 min twice a week for 2 weeks, immediately postinjection. Exercise only

Kang et al10

Controlled (control n=11; 1.310 NMES group n=7)

18

GA

Seifart et al11

Single child

3.36.3

TA and GA

Calf muscles

30 min 5 days a week for 4 weeks. Used functionallytimed to foot switches. Five different start times used: 3, 7, 14, 32 and 35 days postinjection

Skin surface electrodes used unless stated otherwise. #Indicates statistically signicant (p<0.01) increase. BTX-A, botulinum toxin type A (lower limb); DF, dorsiexion; GA, gastrocnemius; HA, hip adductors; HS, hamstrings; NMES, neuromuscular electrical stimulation; PF, plantarexion; PRS, physician rating scale; PT, posterior tibial muscles; ROM, ranges of motion; TA, tibialis anterior.

Table 3
Reference

Details of studies in neuromuscular electrical stimulation to assist with muscle strength and function (upper limb) section
Study design ABC Age range (years) 515 n 8 Muscles stimulated Wrist exors and extensors Wrist exors and extensors Results ROM, ns spasticity, ns passive resistance, wrist extensor strength, ns coactivation Wrist extensor and exor strength, ns passive resistance wrist exors, ns function Session duration and frequency 1530 min daily for 3 months

Kamper et al13

Vaz et al14

Pretest/post-test design

711

Atwater et al28 Carmick34

Case series* Case series

11 and 12.5 1.6 and 6.7

2 2

Wrist extensors Anterior deltoid, shoulder exors, triceps brachii, wrist extensors, nger exors, thumb extensors, thumb abductors (not all used in both patients) Wrist extensors

ns function, ns ROM, ns overall motor development Improvements in function, awareness and spontaneous use of impaired upper limb described

Three sessions per week (unspecied duration) for 8 weeks of resisted exercises in extended wrist range with NMES as adjunct stimulus As part of a 20 min intervention three times a week for 8 weeks Weekly to twice weekly, unspecied duration sessions of targeted FES for between 6 weeks and 6 months

Wright and Granat 35

ABA

515

Function, ROM, ns wrist extension moment

30 min daily for 6 weeks

Indicates statistically signicant (p<0.05) increase; ns indicates no statistically signicant difference (p>0.05). *The two children who received upper limb NMES were a subgroup of 10 children in Atwaters study. Although this study was not a case study, the subgroup results for these children have been considered as such for the purposes of this review section. ABA, baseline-intervention-follow-up; ABC, baseline-intervention1-intervention2; FES, functional electrical stimulation; NMES, neuromuscular electrical stimulation; ROM, ranges of motion.

Combined use of NMES and BTX-A

This review identied only one pilot study that considered the combined effect of NMES and BTX-A on the impaired upper limb of 10 children with CP.17 Signicant improvement in hand function and non-signicant changes in spasticity and active wrist range of motion were reported. Clearly more work is required to determine the efcacy and the optimal conditions under which NMES and BTX-A may be applied to the upper limb of children with CP.

DISCUSSION
The earlier review by Kerr et al1 provided limited evidence to support the use of NMES during gait. The recent meta-analysis conducted by Cauraugh et al4 corroborates the ndings by Kerr et al and cautiously advocates the use of electrical
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stimulation (applied as either a lower limb exercise regime or as a functional intervention) to minimise impairment and activity limitations during gait. It is however prescient to note that the changes seen in lower limb studies have not always translated to improvements in gait. Most lower limb NMES applications focus on tibialis anterior stimulation either with or without gastrocnemius stimulation. This review article has provided a detailed commentary on this work. While it is certainly the case that positive effects of tibialis anterior stimulation with or without gastrocnemius stimulation have been identied, there is as yet insufcient evidence to establish best practice guidelines. It is necessary for larger scale randomised prospective trials to be undertaken in order to inform such guidelines. It is recommended that the estimates of sample sizes in the work by van der
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Table 4
Reference Ozer et al15

Details of studies in combined use of neuromuscular electrical stimulation and orthoses section
Study design Randomised trial Age range n (years) 318 Muscles stimulated Orthoses applied Dynamic splinting to promote elbow and wrist extension. Static splint worn at night to prevent wrist exion Dynamic splinting to promote wrist and elbow extension as clinically appropriate Results Duration and frequency of orthosis and NMES use

24 Wrist extensors

Function, grip strength, 1 h daily for 6 months posture (Zancolli)

Postans et al16 Case study series 716

Wrist and elbow extensors as clinically appropriate

Scheker et al25 Retrospective

321

19 Wrist and nger extension

Carmick36

Case study

7.7

Dynamic splinting to promote elbow and wrist extension. Static splint worn at night to prevent wrist exion Wrist extensors, nger Orthoplast dorsal wrist exors and extensors splint

ns function, ns ROM, ns quality of life (signicant changes unlikely in this small cohort) 17 children and young adults improved Zancolli classication by two or more grades Improvements in function and use of impaired upper limb described

1 h daily for 12 weeks

1 h daily for variable lengths of time

9 months wearing splint for 6 h a day with weekly NMES sessions of unspecied length

Indicates statistically signicant (p<0.05) increase; ns indicates no statistically signicant difference (p>0.05). NMES, neuromuscular electrical stimulation; ROM, ranges of motion.

Figure 2 A dynamic splint applied across the wrist. Neuromuscular electrical stimulation is being applied simultaneously to stimulate wrist extension motion. Linden et al 22 are considered in the design of such trials. In the authors experience, the most benet from NMES during gait can usually be gained when using it as a training tool after school or at the weekend. The application of NMES during walking for children with CP is frequently not tolerated well by children at school, although exceptions are not unknown. It has also been suggested that the use of BTX-A as an adjunct treatment to NMES may enhance the treatment effects by temporarily reducing muscle tone. Although the rational for such an approach is logical, and there are certainly parallel applications to manage similar symptoms in other muscular disorders, there is little published work to support this approach in the lower limb (and almost none for the upper limb). Further investigation is required to establish if NMES is a valuable adjunct to the lower limb application of BTX-A, and if so what regimes should be used and when they should start. The option of delivering lower limb NMES by percutaneous electrodes, or even with an implanted stimulator, as outlined by Merrill 3 also remains a possibility. There are fewer reported applications of NMES to the upper limb of children with CP than the lower limb and to date no meta-analysis of these studies has been published. Although there is a lack of randomised controlled trials, the balance of available evidence is in favour of upper limb exercise NMES
370

offering benets such as increased muscle strength, range of motion and function in children with CP. In addition, reduced spasticity has been observed. However, as with lower limb applications, it appears to be important that NMES is applied for a sufcient time duration which relates to other literature on neuroplasticity. 38 Generally, treatment effects are observed when NMES is applied for 3060 min per day for at least 68 weeks. The overall daily dose can be applied over two or even three sessions. Despite the small number of studies, the use of DS with NMES for upper limb applications has been shown to be more effective than either treatment on its own in improving function and posture.15 Patient selection will be important to determine who will benet most from DS with NMES but current evidence suggests that active grip and some release capability is advantageous.

CONCLUSION
The application of NMES, as an exercise modality or as a functional intervention, to minimise impairment and activity limitations during gait is cautiously advocated. In addition, a growing number of mainly small upper limb studies tend to support the proposition that the use of NMES as an exercise regime in the upper limb is also benecial and can lead to improvements in both strength and range of motion. Furthermore, there is evidence to support the combined application of NMES and DS in the upper limb. Further research is however required in all these areas in order to determine best practice guidelines. The use of BTX-A as an adjunct treatment to NMES may enhance the treatment effects by temporarily reducing muscle tone. Although the rational for such an approach is logical, and there are certainly parallel applications to manage similar symptoms in other muscular disorders, there is little published work to support this approach in the lower limb (and almost none for the upper limb). More research is needed to determine whether the application of BTX-A acts as a useful adjunct to NMES by temporarily reducing muscle tone and if so what treatment protocols should be adopted.
Acknowledgements The authors would like to thank Ms Ingrid Wilkinson, Department of Clinical Sciences and Medical Engineering, Salisbury District Hospital for proofreading this article. Arch Dis Child 2012;97:364371. doi:10.1136/archdischild-2011-300437

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Review
Competing interest The majority shareholder of Odstock Medical Limited is Salisbury NHS Foundation Trust. One author (IDS) is Clinical Director of Odstock Medical Limited. Patient Consent Obtained. Provenance and peer review Commissioned; externally peer reviewed.
20. 18. Khalili MA , Hajihassanie A. Electrical simulation in addition to passive stretch has a small effect on spasticity and contracture in children with cerebral palsy: a randomised within-participant controlled trial. Aust J Physiother 2008;54:1859. Katz A, Tirosh E, Marmur R, et al. Enhancement of muscle activity by electrical stimulation in cerebral palsy: a casecontrol study. J Child Neurol 2008;23:25967. Stackhouse SK , Binder-Macleod SA, Stackhouse CA, et al. Neuromuscular electrical stimulation versus volitional isometric strength training in children with spastic diplegic cerebral palsy: a preliminary study. Neurorehabil Neural Repair 2007;21:47585. Kerr C, McDowell B, Cosgrove A, et al. Electrical stimulation in cerebral palsy: a randomized controlled trial. Dev Med Child Neurol 2006;48:8706. van der Linden ML , Hazlewood ME, Hillman SJ, et al. Functional electrical stimulation to the dorsiexors and quadriceps in children with cerebral palsy. Pediatr Phys Ther 2008;20:239. Durham S, Eve L, Stevens C, et al. Effect of functional electrical stimulation on assymetries in gait of children with hemiplegic cerebral palsy. Physiotherapy 2004;90:8290. Johnston TE, Finson RL, McCarthy JJ, et al. Use of functional electrical stimulation to augment traditional orthopaedic surgery in children with cerebral palsy. J Pediatr Orthop 2004;24:28391. Scheker LR, Chesher SP, Ramirez S. Neuromuscular electrical stimulation and dynamic bracing as a treatment for upper-extremity spasticity in children with cerebral palsy. J Hand Surg Br 1999;24:22632. Hazlewood ME, Brown JK, Rowe PJ, et al. The use of therapeutic electrical stimulation in the treatment of hemiplegic cerebral palsy. Dev Med Child Neurol 1994;36:66173. Comeaux P, Patterson N, Rubin M, et al. Effect of neuromuscular electrical stimulation during gait in children with cerebral palsy. Pediatr Phys Ther 1997;9:1039. Atwater SW, Tatarka ME, Kathrein JE, et al. Electromyography-triggered electrical muscle stimulation for children with cerebral palsy: a pilot study. Pediatr Physical Therapy 1991;3:1909. van der Linden ML , Hazlewood ME, Aitchison AM, et al. Electrical stimulation of gluteus maximus in children with cerebral palsy: effects on gait characteristics and muscle strength. Dev Med Child Neurol 2003;45:38590. Alon G. Electrical stimulation in cerebral palsy: are we asking clinically relevant questions? Dev Med Child Neurol 2006;48:868. Carmick J. Clinical use of neuromuscular electrical stimulation for children with cerebral palsy, part 1: lower extremity. Phys Ther 1993;73:50513; discussion 5237. Carmick J. Managing equinus in children with cerebral palsy: electrical stimulation to strengthen the triceps surae muscle. Dev Med Child Neurol 1995;37:96575. Bertoti DB, Stanger M, Betz RR, et al. Percutaneous intramuscular functional electrical stimulation as an intervention choice for children with cerebral palsy. Pediatr Phys Ther 1997;9:1237. Carmick J. Clinical use of neuromuscular electrical stimulation for children with cerebral palsy, part 2: upper extremity. Phys Ther 1993;73:51422; discussion 5237. Wright PA , Granat MH. Therapeutic effects of functional electrical stimulation of the upper limb of eight children with cerebral palsy. Dev Med Child Neurol 2000;42:7247. Carmick J. Use of neuromuscular electrical stimulation and [corrected] dorsal wrist splint to improve the hand function of a child with spastic hemiparesis. Phys Ther 1997;77:66171. Zancolli EA , Goldner LJ, Swanson AB. Surgery of the spastic hand in cerebral palsy: report of the Committee on Spastic Hand Evaluation (International Federation of Societies for Surgery of the Hand). J Hand Surg Am 1983;8:76672. Kleim JA , Jones TA. Principles of experience-dependent neural plasticity: implications for rehabilitation after brain damage. J Speech Lang Hear Res 2008;51:S22539.

19.

REFERENCES
1. Kerr C, McDowell B, McDonough S. Electrical stimulation in cerebral palsy: a review of effects on strength and motor function. Dev Med Child Neurol 2004;46:20513. Seifart A , Unger M, Burger M. The effect of lower limb functional electrical stimulation on gait of children with cerebral palsy. Pediatr Phys Ther 2009;21:2330. Merrill DR. Review of electrical stimulation in cerebral palsy and recommendations for future directions. Dev Med Child Neurol 2009; 51 Suppl 4:15465. Cauraugh JH, Naik SK, Hsu WH, et al. Children with cerebral palsy: a systematic review and meta-analysis on gait and electrical stimulation. Clin Rehabil 2010;24:96378. Daichman J, Johnston TE, Evans K, et al. The effects of a neuromuscular electrical stimulation home program on impairments and functional skills of a child with spastic diplegic cerebral palsy: a case report. Pediatr Phys Ther 2003;15:1538. Al-Abdulwahab SS, Al-Khatrawi WM. Neuromuscular electrical stimulation of the gluteus medius improves the gait of children with cerebral palsy. NeuroRehabilitation 2009;24:20917. Postans NJ, Granat MH. Effect of functional electrical stimulation, applied during walking, on gait in spastic cerebral palsy. Dev Med Child Neurol 2005;47:4652. Orlin MN, Pierce SR, Stackhouse CL, et al. Immediate effect of percutaneous intramuscular stimulation during gait in children with cerebral palsy: a feasibility study. Dev Med Child Neurol 2005;47:68490. Detrembleur C, Lejeune TM, Renders A, et al. Botulinum toxin and short-term electrical stimulation in the treatment of equinus in cerebral palsy. Mov Disord 2002;17:1629. Kang BS, Bang MS, Jung SH. Effects of botulinum toxin A therapy with electrical stimulation on spastic calf muscles in children with cerebral palsy. Am J Phys Med Rehabil 2007;86:9016. Seifart A , Unger M, Burger M. Functional electrical stimulation to lower limb muscles after botox in children with cerebral palsy. Pediatr Phys Ther 2010;22:199206. Pierce SR, Orlin MN, Lauer RT, et al. Comparison of percutaneous and surface functional electrical stimulation during gait in a child with hemiplegic cerebral palsy. Am J Phys Med Rehabil 2004;83:798805. Kamper DG, Yasukawa AM, Barrett KM, et al. Effects of neuromuscular electrical stimulation treatment of cerebral palsy on potential impairment mechanisms: a pilot study. Pediatr Phys Ther 2006;18:318. Vaz DV, Mancini MC, da Fonseca ST, et al. Effects of strength training aided by electrical stimulation on wrist muscle characteristics and hand function of children with hemiplegic cerebral palsy. Phys Occup Ther Pediatr 2008;28:30925. Ozer K , Chesher SP, Scheker LR. Neuromuscular electrical stimulation and dynamic bracing for the management of upper-extremity spasticity in children with cerebral palsy. Dev Med Child Neurol 2006;48:55963. Postans N, Wright P, Bromwich W, et al. The combined effect of dynamic splinting and neuromuscular electrical stimulation in reducing wrist and elbow contractures in six children with cerebral palsy. Prosthet Orthot Int 2010;34:1019. Rodrguez-Reyes G, Alessi-Montero A, Daz-Martnez L, et al. Botulinum toxin, physical and occupational therapy, and neuromuscular electrical stimulation to treat spastic upper limb of children with cerebral palsy: a pilot study. Artif Organs 2010;34:2304. 21. 22.

2.

3.

23.

4.

24.

5.

25.

26.

6.

27.

7. 8.

28.

9.

29.

10.

30. 31.

11.

32.

12.

33.

13.

34.

14.

35.

15.

36.

16.

37.

17.

38.

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Neuromuscular electrical stimulation for children with cerebral palsy: a review

Philip A Wright, Sally Durham, David J Ewins, et al. Arch Dis Child 2012 97: 364-371

doi: 10.1136/archdischild-2011-300437

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