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Review
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.
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.
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
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
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
Pierce et al12
11
Katz et al19
11.614
2.84.1
Stackhouse et al20
Kerr et al21
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
615
Johnston et al24
Group comparisons. NMES with limited surgery (n=9); traditional surgery (n=8)
612
Hazlewood et al26
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
Comeaux et
al27
9.13.8
8.52.8
Carmick31
Case series
1.610
Carmick32
Case series
1.74.7
Bertoti et al33
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.
Review
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
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
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
ABA
515
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.
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
Arch Dis Child 2012;97:364371. doi:10.1136/archdischild-2011-300437
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
369
Review
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
321
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
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
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.
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Notes