Professional Documents
Culture Documents
com
Review
Review
Much of the literature on the application of NMES both as statistically significant improvements in peak dorsiflexion
exercise and during the gait cycle has been reviewed extensive- in swing and in foot–floor angle at initial contact through
ly.1 4 Kerr et al1 concluded that many studies recorded improve- stimulation of the dorsiflexors in swing. Furthermore, clini-
ments in strength and function, but these often had limited cally significant improvements in dorsiflexion during swing
statistical power. In addition, they suggested there was a need and at initial contact were seen in three of five children while
for further work with more rigorous study designs and fol- stimulation was being applied to the dorsiflexor muscles in
low-up, larger sample sizes and homogeneous patient groups. individually tailored programmes of NMES during walking.7
The meta-analyses conducted by Cauraugh et al4 demonstrated Nevertheless, equivocal results were observed in the remain-
that electrical stimulation produced ‘medium effect’ sizes on ing three children in this study who received stimulation for
gait outcomes. They considered that their fi ndings corrobo- both ankle dorsiflexion during swing and knee extension (dur-
rated earlier work by Kerr et al1 and Hazlewood et al. 26 ing swing or stance as appropriate).7 Another study described
A subsequent review of FES for gait assistance also noted an immediate effect of applying percutaneous intramuscular
that further research on stimulation protocols was needed to NMES in eight children with CP.8 The authors reported a
provide clinically relevant results. 2 There has, however, been trend towards improved ankle kinematics while stimulation
relevant work published in this area which was not included in was applied to tibialis anterior during swing. However, they
these reviews or which given the purpose of this paper merits observed statistically significant outcomes when calf stimula-
further amplification. All the papers reviewed are summarised tion during stance was added. This was presumed to be due to
in table 1. improved coordination of muscle activation and sensory feed-
back provided by stimulation to the muscles around the joint at
NMES applied for exercise the appropriate time during the gait cycle. These small studies
Improvements in hamstring spasticity and lower limb have concentrated on the immediate changes seen on apply-
function, 5 and quadriceps–hamstring co-contraction,19 have ing stimulation functionally. Longer-term changes such as
been recorded through an extended period of quadriceps improvements in the asymmetries of temporal spatial data fol-
exercise stimulation. Khalili and Hajihassanie18 also found lowing stimulation of the anterior tibial muscles during swing
improvements in hamstring spasticity (and passive knee exten- in children with hemiplegic CP have also been investigated. 23
sion) when stimulation of the quadriceps was added to a pas- Plastic changes occurring in response to a repeated stimulus
sive stretching regime, however, they considered the change are suggested as the mechanism for this ‘motor learning’.
for the experimental group as a whole not to be clinically rel- Other investigators report positive effects on swing phase
evant. They concluded that the marginal size of the effect may kinematics following stimulation of the calf muscles (figure 1).
be due to the short duration (30 min, three times per week The rationale for targeting the calf muscles for a duration
for 4 weeks) and relatively low-intensity regimen investigated, slightly longer than the stance phase is based on the premise
and that larger sample sizes are required. Stackhouse et al20 that stimulation has the potential to: interrupt the constant
investigated the effects of strength training using percutane- state of activity in the spastic gastrocnemius; allow reciprocal
ously implanted stimulation to quadriceps femoris and triceps inhibition of tibialis anterior; generate a stretch reflex to the tib-
surae. In this preliminary study, greater increases in norma- ialis anterior; and strengthen the weak calf muscle. 27 Further,
lised force production were seen in both muscle groups when assuming a potential for motor relearning, these changes may
compared with results from a group undertaking volitional be maintained after the intervention period. Case studies by
training only. An improvement in walking speed in the stimu- Carmick reported improvements in selective control, range of
lation group was also noted. active dorsiflexion and foot position at initial contact during
In addition to quadriceps stimulation, stimulation to glu- and following prolonged periods (3–12 months) of stimulation
teus medius bilaterally has been shown to result in a signifi- of the calf during stance combined with gait training. 31 32 In
cant improvement in gait temporal spatial parameters and in addition, increased dorsiflexion at initial contact was observed
hip adductor tone.6 Stimulation was applied during the gait following both calf stimulation during stance, and calf stimu-
cycle so in that sense it was used functionally, but it was not lation with anterior tibial muscle stimulation during swing,
synchronised with stepping. These individual studies seem in a group of 14 children. 27 Defi nitive studies still need to be
to support the conclusions reached in the review by Kerr undertaken in this area, but the review by Seifart et al2 would
et al1 and echoed by Cauraugh et al4 that many studies recorded suggest that stimulation of the gastrocnemius with or with-
improvements in strength and function. out tibialis anterior may effect greater gait improvements than
The use of NMES to strengthen lower limb muscles and stimulating the tibialis anterior alone.
increase range of motion, and the resultant effect of this on gait
has also been investigated. 21 26 29 Stimulation was not applied Combined use of NMES and BTX-A
during a functional task in these studies, and any changes in BTX-A, acting as a neuromuscular junction block, can reduce
range of motion and strength did not result in improvements tone and offer a time window in which NMES may be used to
in walking pattern. Some authors have suggested that it may stretch the agonist and strengthen the antagonist muscles in
be more effective to combine NMES with task-specific or func- children with spasticity.7 Table 2 gives details of studies inves-
tional training. 30 tigating what benefit, if any, can be offered by introducing an
NMES regime post injection of BTX-A in the lower limb of
NMES applied during gait cycle children with CP.
The two main approaches reported using NMES during walk- Some authors have concluded that combined BTX-A and
ing to improve swing dorsiflexion have been largely contradic- NMES is not superior to BTX-A alone for the treatment of
tory, either targeting the anterior tibial muscles during swing equinus in CP.9 However, others have found NMES offered
or conversely the calf muscles during stance phase. In some some benefits over BTX-A in early improvement of range of
other cases, both muscle groups have been recruited, mim- motion and maintenance of gait improvement in dynamic
icking neural fi ring patterns. Van der Linden et al22 reported equinus.10 There were similarities in terms of muscles injected
Review
and review protocols; however, as shown in table 2, there were with CP, cyclic NMES was applied to the wrist extensor
differences in the stimulation regime. The effect of NMES on muscles of eight children with hemiplegic CP. 35 Statistically
the injected muscles with stimulation timed to the walking significant improvements in hand function and active wrist
cycle in three children who started NMES at different intervals extension were measured, although no significant changes
post injection has also been investigated.11 NMES was found were observed in measurements of wrist extension moment.
to improve isometric plantarflexor muscle strength, but did not These authors also included anecdotal comments from the
produce changes in self-selected walking speeds or isometric children and their parents, such as an increased awareness of
dorsiflexor muscle strength. These results also suggested that the limb, improved coordination of both hands used together,
starting NMES 32 days post injection was most effective in or greater proficiency in carrying out tasks that required grasp
this small study. and release activity and hand manipulation which were con-
Further investigation is required to establish if NMES is a sistent with those of an earlier case report. 34
valuable adjunct to BTX-A, and if so, what regimes should be In a subsequent study, cyclic NMES was applied recipro-
used and when should they start. cally to wrist flexor and extensor muscles of a group of eight
children with CP using a rationale similar to that previously
Developments in percutaneous and implanted electrical discussed in the lower limb example of stimulation of ankle
stimulation dorsiflexors and plantarflexors.13 The children were specifi-
Most reported NMES work has involved surface electrodes, cally asked to work with the NMES as it initiated movement.
that is, electrodes placed on the skin. This approach is non-inva- Statistically significant improvements in active wrist exten-
sive, but it has the following limitations: accurate placement of sion were demonstrated (as in the previous study) 35 but also
electrodes, isolation of a response from specific muscles, the in wrist extension moment. The authors concluded that a pos-
need for sensory tolerance and a practical limit on the number sible mechanism of NMES improving wrist extensor muscle
of channels that can be used at a given time. 33 Therefore there strength was through decreased flexor coactivation, noting
has been interest in the use of percutaneous and implanted that a trend toward reduced coactivation of flexors and exten-
stimulation systems. Several authors have successfully used sors was observed in six children.
percutaneous lower limb muscle stimulation in children with In a further study on the effect of reciprocal NMES of
CP.8 12 24 33 In one single case study,12 greater improvements in wrist extensors and flexors of nine children with CP, thera-
dorsiflexion were found with percutaneous than with surface pists maintained the wrist in an extended position, offering
stimulation (eg, mean increase of 10.6° in peak dorsiflexion dur- manual resistance while children were encouraged to ‘com-
ing swing with percutaneous stimulation and 4.6° with surface pete’ with the therapist.14 Significant increases in wrist exten-
stimulation when compared with the no stimulation condi- sor and flexor strength were measured while the wrist was
tion). The authors found that (sagittal plane) ankle absorption maintained in an extended position. The wrist extensors also
work decreased during the gait load phase with both types of demonstrated significant increases in strength in neutral. No
stimulation, but that ankle generation work was increased only significant changes in passive stiffness of wrist flexors, hand
with percutaneous stimulation. In a recent review of NMES in function or mean wrist angle during manual tasks was mea-
CP, potential limitations of percutaneous stimulation systems sured, possibly because the intervention may not have been
were noted, including that the leads present a persistent infec- sufficiently prolonged or aggressive. The authors suggested
tion route and that they may also wear and break, requiring that the intervention had resulted in a shift of the wrist exten-
additional surgical interventions. 3 Although not reported in sor length–tension curve.
the studies previously mentioned, these are important issues, These studies lend mounting support to the premise that
and restrict the use of these systems outside of research stud- NMES may assist with muscle strength and function in the
ies. An implanted system may offer a solution to the problems upper limb of children with CP and additional benefits may
presented by both surface and percutaneous systems, and an occur when children also attempt to complement NMES with
approach for a fully implanted stimulator that may be appro- volitional movement. However, the comment that previous
priate is also outlined in that review. 3 reviewers have made still applies; there is insufficient statisti-
NMES for restoration of upper limb function cal power to provide conclusive evidence of this.1
There are fewer reported applications of NMES to the upper
limb of children with CP than the lower limb. We can consider Combined use of NMES and orthoses
these under three headers: In the fi rst case report of NMES used in combination with an
▶ NMES to assist with muscle strength and function.
orthosis, a child who had previously used NMES was sup-
▶ Combined use of NMES and orthoses.
plied with a dorsal wrist splint made out of orthoplast that
▶ Combined use of NMES and BTX-A.
maintained 10° of wrist extension and helped provide wrist
stability. 36 After 9 months of wearing the splint, supplemented
NMES to assist with muscle strength and function by weekly NMES sessions, the splint was discontinued as the
The fi rst case studies to demonstrate the feasibility of applying child could maintain hand function without it. Details of this
NMES to the upper limbs of children with CP were reported and other papers reviewed in this section are given in table 4.
in the early 1990s. 28 34 Functional improvements such as Following this, a retrospective study was published on 19
increased awareness and spontaneous use of the impaired arm children and young adults with CP who took part in a clinical
and hand, and enhanced grasp and release abilities were also programme involving 1 h per day of NMES with an orthotic
reported. 34 Nevertheless, they presented insufficient evidence intervention known as dynamic splinting (DS).25 In DS, a
to reach a judgement on the general applicability of NMES for restorative force is applied by an orthosis often by means of
the upper limb of children with CP. Further details of these a variable tension spring loaded hinge (figure 2). In this case,
and other papers reviewed in this section are given in table 3. NMES was applied to achieve wrist and fi nger extension while
In the fi rst report on the application of cyclic NMES as a DS promoted extension of the wrist and elbow joints. A static
single intervention to the upper limb of a group of children splint was worn during the night to prevent wrist flexion.
Daichmann et al5 Case study 13 1 Right QR Increase in right QR strength, decrease in right HS spasticity, improvements Approximately 30 min every other day for 6 weeks.
in mobility elements of PEDI results Exercise only
Al-Abdulwahab et al6 Pre/post test design. 7.4±2 21 GM bilaterally ↑↑Temporal spatial parameters (apart from step width) and ↓↓hip adductor 15 min three times per day for 7 days. Stimulation applied
Data compared with tone of the treated group mainly during walking but not timed to the gait cycle
healthy (n=20) and
control CP (n=10)
groups
Postans and Granat7 ABAB 8.9–17.5 8 DF, PF, QR (determined For NMES to AF only group (n=5), clinically significant changes in stance Used functionally during testing on 2 days
through gait analysis) phase kinematics for three children
Orlin et al8 AB 7.9–11.8 8 Percutaneous ↑*Peak DF in swing (more affected extremity) and DF at initial contact (less Used functionally for 1 week for each NMES set up (TA only,
stimulation of TA and affected extremity) for TA+GA condition. Trends of improvement in DF TA and GA, and GA only) for approximately 2 × 45 min daily.
GA of involved limb kinematics seen for TA and GA only conditions Four-channel and two-channel stimulation used for diplegic
and hemiplegic children, respectively
Pierce et al12 Comparison of surface 11 1 DF with balanced Increases in DF at initial contact, peak in swing and mean in swing, greater Assessed functionally during walking (one test day)
and percutaneous eversion and inversion with percutaneous stimulation. Ankle absorption work improved (decreased)
stimulation with both types of stimulation. Ankle generation work increased only with
percutaneous stimulation. Greater isometric force produced with
percutaneous than surface stimulation
Durham et al23 ABA, two children 6–15 12 DF Heel–toe contact pattern and symmetry both improved following intervention FES of DF during gait for 12 weeks
dropped out with FES (no statistical analysis)
Johnston et al24 Group comparisons. 6–12 17 BF, GM, Gmax, PAM, VL, ns differences in passive range, temporal spatial parameters or gross motor 4-week (minimum) exercise for no more than 1 h per day,
NMES with limited sur- VM, Sol, TA (not all used function between groups before or 1 year after intervention. FES group followed by functional use
gery (n=9); traditional in all children) underwent 4.5 fewer ablative procedures per child
surgery (n=8)
Hazlewood et al26 Randomised (NMES 5–12 20 TA of involved limb ↑Passive DF in NMES group. ↑Active DF in NMES group compared with 1 h daily for 35 consecutive days. Exercise only
n=10; control n=10) control group post intervention but not pre intervention. ↑TA muscle
power in NMES group
Review
continued
367
Continued
368
Table 1
Age range
Reference Study design (years) n Muscles stimulated Results Session duration, frequency and mode
Review
Comeaux et al27 ABCA (n=7), 9.1±3.8 14 GA and TA ↑*DF during gait for both ‘targeted’ FES interventions ‘Targeted’ FES of GA during 15-min therapy session three
ACBA (n=7) times a week for 4 weeks followed/preceded by a similar
programme with GA and TA
Van der Linden et al29 Randomised (NMES 8.5±2.8 22 GMax For NMES: ns in hip extensor strength, gait analysis, passive limits of hip NMES: 1 h a day 6 days per week for 8 weeks.
n=11; control n=11) rotation, section E of gross motor function measure when comparing NMES Exercise only
group with control group
Carmick31 Case series 1.6–10 3 TA, TS, GA, Sol, Gmax, HS Improvements in physiological cost index measured in two children Approximately weekly sessions of unspecified duration of
(not all used in all patients) together with observations of improved gait function and symmetry ‘targeted’ FES for between 6 weeks and 8 months
Carmick32 Case series 1.7–4.7 4 TA, TS, Gmax, HS (not all Improvements in heel strike, foot alignment, function, balance, active and passive Unspecified frequency and duration of ‘targeted’ FES
used in all patients) DF range of movement and walking speed. (Not all observed in all children) sessions as required
Bertoti et al33 Case series percutane - 6 2 Gmax, GM, VM, VL, GA, Measured improvements in lower extremity ranges of motion, spatial gait Two 15-min sessions of FES 5 days per week for between
ous stimulation TA characteristics, improved gross motor function 7 and 10 months. Children asked to ‘work with’ FES
Skin surface electrodes used unless stated otherwise.
↑↑, ↑, ↑* indicates statistically significant (p<0.001, p<0.05 and p<0.0055, respectively) increase; ↓↓ and ↓ indicates statistically significant (p<0.001 and p<0.05, respectively) decrease; ns indicates no statistically significant
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 flexors;
BF, biceps femoris; CP, cerebral palsy; DF, dorsiflexion; FES, functional electrical stimulation; GA, gastrocnemius; GM, gluteus medius; Gmax, gluteus maximus; HA, hip adductors; HS, hamstrings; NMES, neuromuscular electrical stim-
ulation; PAM, posterior adductor magnus; PEDI, pediatric evaluation of disability inventory; PF, plantarflexion; QR, quadriceps; Sol, soleus; TA, tibialis anterior; TES, threshold electrical stimulation; TS, triceps surae; VL, vastus lateralis;
VM, vastus medialis.
intervention.
improvements.
DS, its use was investigated in six children with CP with fi xed
ture were observed only in the group receiving the combined
Review
Table 2 Details of studies in combined use of neuromuscular electrical stimulation and botulinum toxin type A (lower limb) section
Age range Muscles Results (differences Session duration,
Reference Study design (years) n stimulated BTX-A sites with NMES) frequency and mode
Detrembleur et al9 Controlled (control n=6; 4.75–6 12 Soleus Soleus and medial and For a range of clinical and 30 min six times a day
NMES group n=6) and GA lateral GA. HA in 7 gait variables, combined for 3 days, beginning on day
patients treatment not superior to BTX-A of treatment with BTX-A.
(3 NMES and 4 control) alone at 1, 3 and 6 months post Exercise only
BTX-A injections
Kang et al10 Controlled (control n=11; 1.3–10 18 GA Soleus and medial and ↑#Passive ankle ROM after 2 30 min twice a week for
NMES group n=7) lateral GA. HS and PT in weeks in NMES group only 2 weeks, immediately
two children (in both groups at 3 months). postinjection. Exercise only
↑#Total PRS and foot equinus
scores in NMES group at
3 months after injection
Seifart et al11 Single child 3.3–6.3 5 TA and GA ‘Calf’ muscles Two children did not use 30 min 5 days a week for
NMES. Trend towards 4 weeks. Used function-
increased isometric PF muscle ally—timed to foot switches.
strength. No changes in self- Five different start times
selected walking speeds or used: 3, 7, 14, 32 and 35
isometric DF muscle strength days postinjection
Table 3 Details of studies in neuromuscular electrical stimulation to assist with muscle strength and function (upper limb) section
Study Age range Muscles Session duration and
Reference design (years) n stimulated Results frequency
Kamper et al13 ABC 5–15 8 Wrist flexors and ↑ROM, ns spasticity, ns passive 15–30 min daily for 3 months
extensors resistance, ↑wrist extensor strength,
ns coactivation
Vaz et al14 Pretest/post-test 7–11 9 Wrist flexors and ↑Wrist extensor and flexor strength, Three sessions per week
design extensors ns passive resistance wrist flexors, (unspecified duration) for 8 weeks
ns function of resisted exercises in extended
wrist range with NMES as adjunct
stimulus
Atwater et al28 Case series* 11 and 12.5 2 Wrist extensors ns function, ns ROM, ns overall motor As part of a 20 min intervention
development three times a week for 8 weeks
Carmick34 Case series 1.6 and 6.7 2 Anterior deltoid, shoulder Improvements in function, awareness Weekly to twice weekly,
flexors, triceps brachii, and spontaneous use of impaired unspecified duration sessions of
wrist extensors, finger upper limb described ‘targeted’ FES for between 6 weeks
flexors, thumb extensors, and 6 months
thumb abductors (not all
used in both patients)
Wright and Granat 35 ABA 5–15 8 Wrist extensors ↑Function, ↑ROM, ns wrist extension 30 min daily for 6 weeks
moment
↑Indicates statistically significant (p<0.05) increase; ns indicates no statistically significant difference (p>0.05).
*The two children who received upper limb NMES were a subgroup of 10 children in Atwater’s 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 stimulation (applied as either a lower limb exercise regime
This review identified only one pilot study that considered the or as a functional intervention) to minimise impairment
combined effect of NMES and BTX-A on the impaired upper and activity limitations during gait. It is however prescient
limb of 10 children with CP.17 Significant improvement in to note that the changes seen in lower limb studies have
hand function and non-significant changes in spasticity and not always translated to improvements in gait. Most lower
active wrist range of motion were reported. Clearly more work limb NMES applications focus on tibialis anterior stimula-
is required to determine the efficacy and the optimal condi- tion either with or without gastrocnemius stimulation. This
tions under which NMES and BTX-A may be applied to the review article has provided a detailed commentary on this
upper limb of children with CP. work. While it is certainly the case that positive effects of
tibialis anterior stimulation with or without gastrocnemius
DISCUSSION stimulation have been identified, there is as yet insufficient
The earlier review by Kerr et al1 provided limited evidence to evidence to establish best practice guidelines. It is necessary
support the use of NMES during gait. The recent meta-anal- for larger scale randomised prospective trials to be under-
ysis conducted by Cauraugh et al4 corroborates the fi ndings taken in order to inform such guidelines. It is recommended
by Kerr et al and cautiously advocates the use of electrical that the estimates of sample sizes in the work by van der
Review
Table 4 Details of studies in combined use of neuromuscular electrical stimulation and orthoses section
Age range Muscles Orthoses Duration and frequency
Reference Study design (years) n stimulated applied Results of orthosis and NMES use
Ozer et al15 Randomised trial 3–18 24 Wrist extensors Dynamic splinting to promote ↑Function, ↑grip strength, 1 h daily for 6 months
elbow and wrist extension. Static ↑posture (Zancolli)
splint worn at night to prevent
wrist flexion
Postans et al16 Case study series 7–16 6 Wrist and elbow Dynamic splinting to promote ns function, ns ROM, ns 1 h daily for 12 weeks
extensors as clinically wrist and elbow extension as quality of life (significant
appropriate clinically appropriate changes unlikely in this
small cohort)
Scheker et al25 Retrospective 3–21 19 Wrist and finger Dynamic splinting to promote 17 children and young 1 h daily for variable lengths
extension elbow and wrist extension. adults improved Zancolli of time
Static splint worn at night to classification by two or
prevent wrist flexion more grades
Carmick36 Case study 7.7 1 Wrist extensors, finger Orthoplast dorsal wrist Improvements in function 9 months wearing splint for
flexors and extensors splint and use of impaired upper 6 h a day with weekly NMES
limb described sessions of unspecified length
↑Indicates statistically significant (p<0.05) increase; ns indicates no statistically significant difference (p>0.05). NMES, neuromuscular electrical stimulation; ROM,
ranges of motion.
Review
Competing interest The majority shareholder of Odstock Medical Limited is 18. Khalili MA, Hajihassanie A. Electrical simulation in addition to passive stretch
Salisbury NHS Foundation Trust. One author (IDS) is Clinical Director of Odstock has a small effect on spasticity and contracture in children with cerebral
Medical Limited. palsy: a randomised within-participant controlled trial. Aust J Physiother
2008;54:185–9.
Patient Consent Obtained.
19. Katz A, Tirosh E, Marmur R, et al. Enhancement of muscle activity by electrical
Provenance and peer review Commissioned; externally peer reviewed. stimulation in cerebral palsy: a case–control study. J Child Neurol 2008;23:259–67.
20. Stackhouse SK, Binder-Macleod SA, Stackhouse CA, et al. Neuromuscular
electrical stimulation versus volitional isometric strength training in children with
REFERENCES spastic diplegic cerebral palsy: a preliminary study. Neurorehabil Neural Repair
1. Kerr C, McDowell B, McDonough S. Electrical stimulation in cerebral palsy: 2007;21:475–85.
a review of effects on strength and motor function. Dev Med Child Neurol 21. Kerr C, McDowell B, Cosgrove A, et al. Electrical stimulation in cerebral palsy: a
2004;46:205–13. randomized controlled trial. Dev Med Child Neurol 2006;48:870–6.
2. Seifart A, Unger M, Burger M. The effect of lower limb functional electrical 22. van der Linden ML, Hazlewood ME, Hillman SJ, et al. Functional electrical
stimulation on gait of children with cerebral palsy. Pediatr Phys Ther stimulation to the dorsiflexors and quadriceps in children with cerebral palsy.
2009;21:23–30. Pediatr Phys Ther 2008;20:23–9.
3. Merrill DR. Review of electrical stimulation in cerebral palsy and 23. Durham S, Eve L, Stevens C, et al. Effect of functional electrical stimulation
recommendations for future directions. Dev Med Child Neurol 2009; on assymetries in gait of children with hemiplegic cerebral palsy. Physiotherapy
51 Suppl 4:154–65. 2004;90:82–90.
4. Cauraugh JH, Naik SK, Hsu WH, et al. Children with cerebral palsy: a systematic 24. Johnston TE, Finson RL, McCarthy JJ, et al. Use of functional electrical
review and meta-analysis on gait and electrical stimulation. Clin Rehabil stimulation to augment traditional orthopaedic surgery in children with cerebral
2010;24:963–78. palsy. J Pediatr Orthop 2004;24:283–91.
5. Daichman J, Johnston TE, Evans K, et al. The effects of a neuromuscular 25. Scheker LR, Chesher SP, Ramirez S. Neuromuscular electrical stimulation and
electrical stimulation home program on impairments and functional skills of dynamic bracing as a treatment for upper-extremity spasticity in children with
a child with spastic diplegic cerebral palsy: a case report. Pediatr Phys Ther cerebral palsy. J Hand Surg Br 1999;24:226–32.
2003;15:153–8. 26. Hazlewood ME, Brown JK, Rowe PJ, et al. The use of therapeutic electrical
6. Al-Abdulwahab SS, Al-Khatrawi WM. Neuromuscular electrical stimulation stimulation in the treatment of hemiplegic cerebral palsy. Dev Med Child Neurol
of the gluteus medius improves the gait of children with cerebral palsy. 1994;36:661–73.
NeuroRehabilitation 2009;24:209–17. 27. Comeaux P, Patterson N, Rubin M, et al. Effect of neuromuscular electrical
7. Postans NJ, Granat MH. Effect of functional electrical stimulation, applied during stimulation during gait in children with cerebral palsy. Pediatr Phys Ther
walking, on gait in spastic cerebral palsy. Dev Med Child Neurol 2005;47:46–52. 1997;9:103–9.
8. Orlin MN, Pierce SR, Stackhouse CL, et al. Immediate effect of percutaneous 28. Atwater SW, Tatarka ME, Kathrein JE, et al. Electromyography-triggered
intramuscular stimulation during gait in children with cerebral palsy: a feasibility electrical muscle stimulation for children with cerebral palsy: a pilot study.
study. Dev Med Child Neurol 2005;47:684–90. Pediatr Physical Therapy 1991;3:190–9.
9. Detrembleur C, Lejeune TM, Renders A, et al. Botulinum toxin and short-term 29. van der Linden ML, Hazlewood ME, Aitchison AM, et al. Electrical stimulation
electrical stimulation in the treatment of equinus in cerebral palsy. Mov Disord of gluteus maximus in children with cerebral palsy: effects on gait characteristics
2002;17:162–9. and muscle strength. Dev Med Child Neurol 2003;45:385–90.
10. Kang BS, Bang MS, Jung SH. Effects of botulinum toxin A therapy with electrical 30. Alon G. Electrical stimulation in cerebral palsy: are we asking clinically relevant
stimulation on spastic calf muscles in children with cerebral palsy. Am J Phys Med questions? Dev Med Child Neurol 2006;48:868.
Rehabil 2007;86:901–6. 31. Carmick J. Clinical use of neuromuscular electrical stimulation for children with
11. Seifart A, Unger M, Burger M. Functional electrical stimulation to lower cerebral palsy, part 1: lower extremity. Phys Ther 1993;73:505–13; discussion
limb muscles after botox in children with cerebral palsy. Pediatr Phys Ther 523–7.
2010;22:199–206. 32. Carmick J. Managing equinus in children with cerebral palsy: electrical
12. Pierce SR, Orlin MN, Lauer RT, et al. Comparison of percutaneous and surface stimulation to strengthen the triceps surae muscle. Dev Med Child Neurol
functional electrical stimulation during gait in a child with hemiplegic cerebral 1995;37:965–75.
palsy. Am J Phys Med Rehabil 2004;83:798–805. 33. Bertoti DB, Stanger M, Betz RR, et al. Percutaneous intramuscular functional
13. Kamper DG, Yasukawa AM, Barrett KM, et al. Effects of neuromuscular electrical electrical stimulation as an intervention choice for children with cerebral palsy.
stimulation treatment of cerebral palsy on potential impairment mechanisms: a Pediatr Phys Ther 1997;9:123–7.
pilot study. Pediatr Phys Ther 2006;18:31–8. 34. Carmick J. Clinical use of neuromuscular electrical stimulation for children with
14. Vaz DV, Mancini MC, da Fonseca ST, et al. Effects of strength training cerebral palsy, part 2: upper extremity. Phys Ther 1993;73:514–22; discussion
aided by electrical stimulation on wrist muscle characteristics and hand 523–7.
function of children with hemiplegic cerebral palsy. Phys Occup Ther Pediatr 35. Wright PA, Granat MH. Therapeutic effects of functional electrical stimulation
2008;28:309–25. of the upper limb of eight children with cerebral palsy. Dev Med Child Neurol
15. Ozer K, Chesher SP, Scheker LR. Neuromuscular electrical stimulation and 2000;42:724–7.
dynamic bracing for the management of upper-extremity spasticity in children 36. Carmick J. Use of neuromuscular electrical stimulation and [corrected] dorsal
with cerebral palsy. Dev Med Child Neurol 2006;48:559–63. wrist splint to improve the hand function of a child with spastic hemiparesis.
16. Postans N, Wright P, Bromwich W, et al. The combined effect of dynamic Phys Ther 1997;77:661–71.
splinting and neuromuscular electrical stimulation in reducing wrist and elbow 37. Zancolli EA, Goldner LJ, Swanson AB. Surgery of the spastic hand in cerebral
contractures in six children with cerebral palsy. Prosthet Orthot Int 2010;34:10–19. palsy: report of the Committee on Spastic Hand Evaluation (International
17. Rodríguez-Reyes G, Alessi-Montero A, Díaz-Martínez L, et al. Botulinum toxin, Federation of Societies for Surgery of the Hand). J Hand Surg Am 1983;8:766–72.
physical and occupational therapy, and neuromuscular electrical stimulation to 38. Kleim JA, Jones TA. Principles of experience-dependent neural plasticity:
treat spastic upper limb of children with cerebral palsy: a pilot study. Artif Organs implications for rehabilitation after brain damage. J Speech Lang Hear Res
2010;34:230–4. 2008;51:S225–39.
These include:
References This article cites 38 articles, 8 of which can be accessed free at:
http://adc.bmj.com/content/97/4/364.full.html#ref-list-1
Email alerting Receive free email alerts when new articles cite this article. Sign up in
service the box at the top right corner of the online article.
Notes