Immediate effect of
percutaneous
intramuscular
stimulation during gait
in children with
cerebral palsy: a
feasibility study
Margo N Orlin* PT PhD PCS, Programs in Rehabilitation
Sciences, Drexel University;
Samuel R Pierce PT MS NCS;
Carrie Laughton Stackhouse MS;
Brian T Smith MS;
Therese Johnston PT MS, Shriners Hospitals for Children;
Patricia A Shewokis PhD, Programs in Rehabilitation
Sciences, Drexel University;
James J McCarthy MD, Shriners Hospitals for Children,
Philadelphia, PA, USA.
*Correspondence to first author at Drexel University,
Programs in Rehabilitation Sciences, 245 North Broad
Street, Philadelphia, PA 19102-1192, USA.
E-mail: margo.n.orlin@drexel.edu
The feasibility of percutaneous intramuscular functional
electrical stimulation (P-FES) in children with cerebral palsy
(CP) for immediate improvement of ankle kinematics during
gait has not previously been reported. Eight children with CP
(six with diplegia, two with hemiplegia; mean age 9 years 1
month [SD 1y 4mo; range 7y 11mo to 11y 10mo]) had
percutaneous intramuscular electrodes implanted into the
gastrocnemius (GA) and tibialis anterior (TA) muscles of
their involved limbs. Stimulation was provided during
appropriate phases of the gait cycle in three conditions (GA
only, TA only, and GA/TA). Immediately after a week of
practice for each stimulation condition, a gait analysis was
performed with and without stimulation. A significant
improvement in peak dorsiflexion in swing for the more
affected extremity and dorsiflexion at initial contact for the
less affected extremity were found in the GA/TA condition.
Clinically meaningful trends were evident for improvements
in dorsiflexion kinematics for the more and less affected
extremities in the TA only and GA/TA conditions. The results
suggest that P-FES might immediately improve ankle
kinematics in children with CP.
See end of paper for list of abbreviations.
684
Developmental Medicine & Child Neurology 2005, 47: 684–690
Gait deficits are common in children with cerebral palsy (CP)
in comparison with children of typical development. Children
with CP have decreased walking velocity and stride length
compared with children of typical development (Norlin and
Odenrick 1986, Sutherland et al. 1988, Abel and Damiano
1996). Winters et al. (1987) examined the gait of a heterogeneous sample of 46 children and adults with hemiplegia and
found that decreased dorsiflexion in swing was a commonly
seen deficit in ankle kinematics. Even small changes in ankle
angle during stance phase or swing phase can significantly affect
foot clearance (Winter 1992). Poor foot clearance contributes to
the frequent tripping and falling reported by children with CP.
In addition, children with CP often do not demonstrate a true
heel strike at foot contact, thereby loading the triceps surae
and creating a plantarflexion and knee extension coupling
during initial stance. This increases absorption work by the
triceps surae during initial stance, resulting in a more inefficient gait. In a comparative study, Olney et al. (1990) found
that the ankle plantar flexors in children with spastic hemiplegic CP produced less positive work at push-off than those
in children of typical development. Power generation by the
plantarflexors during push-off contributes significantly to step
length and walking velocity (Winter 1992).
Interventions have been developed to improve the gait
mechanics of children with CP. Ultimately, the goal of such
intervention is to improve gait mechanics, reduce energy consumption, improve poor foot clearance, and, possibly, prevent
secondary injuries due to abnormal loads placed on the musculoskeletal system. Functional electrical stimulation (FES) is
the use of electrical current for activation of muscles through
the stimulation of intact peripheral motor nerves to promote
functional activities (American Physical Therapy Association
2000). FES has been investigated as a method of addressing
abnormal gait mechanics in children with CP, typically by stimulation of the ankle plantarflexors, ankle dorsiflexors, and/or
peroneal nerve.
The primary focus of previous investigations has been on
the carry-over effect of prolonged FES training on gait and function. Carmick (1993, 1995) reported improvements in gait, voluntary walking speed, and energy efficiency in multiple case
studies of children with CP after prolonged FES training of several muscles including the gastrocnemius (GA). Comeaux et al.
(1997) examined the use of FES of the GA and tibialis anterior
(TA) in 14 children with CP and found that FES training
improved ankle position at initial foot contact by about 4˚. The
immediate effect of surface FES on gait kinematics, kinetics,
and temporal–spatial parameters has not been well investigated. Naumann et al. (1985) reported immediate improvements
in dorsiflexion at initial contact of about 10˚ in two adolescents
with CP when they walked with FES applied to their dorsiflexors during swing. Step length and walking velocity also improved in one of the participants during FES application. Joint
kinetics were not reported in this investigation.
These studies of FES in children with CP have primarily
involved stimulation applied by means of surface skin electrodes. Implanted intramuscular stimulation, applied using
fine wire electrodes, may have potential advantages over surface stimulation. Difficulties associated with surface electrodes
that might be addressed with intramuscular stimulation include
obtaining repeatable stimulated motor responses, the inability
to stimulate deeper muscles, and decreased skin tolerance
with prolonged use (McNeal and Bowman 1985). The levels
of discomfort associated with surface FES and percutaneous
intramuscular FES (P-FES) have been compared in adults with
hemiplegia due to stroke and it was found that the P-FES was
perceived as significantly more comfortable (Chae and Hart
1998, Yu et al. 2001). These authors suggested that P-FES was
more comfortable because it avoids the stimulation of cutaneous nociceptors.
To our knowledge, the use of percutaneous electrodes with
children with CP has been limited to several small studies conducted at our hospital. In one of the first, Bertoti et al. (1997)
investigated the use of P-FES of the TA, GA, quadriceps, and
gluteal muscles during gait and exercise in two children with
CP. Gross motor function was not tested specifically, but improvements in unassisted ambulation, stopping, and starting
while walking, and alteration of walking direction were reported. Range of motion of the lower extremity improved and
increases in step length and base of support in one participant
were reported after completion of the stimulation program.
Our laboratory has also reported on the use of P-FES in tandem
with soft tissue surgical procedures needed by children with
CP (Johnston et al. 2004).
There is a paucity of work investigating the immediate
effect of P-FES on gait kinematics, kinetics, and temporal–spatial parameters in children. Recently we reported immediate
Table I: Participant inclusion criteria
Diagnosis of cerebral palsy, spastic diplegia, or spastic hemiplegia
Level I or II in GMFCS
Age between 7 and 12 years
Migration Index less than 40% as measured on X-ray or hip dislocation
Seizure-free or seizure-controlled
Visuoperceptual skills and cognitive/communication skills sufficient
to follow multiple step commands and to attend to tasks associated
with data collection as determined by history and clinical observation
Absence of severe tactile hypersensitivity in the lower extremities
A minimum of 1 year after surgery to the lower extremities
A minimum of 6 months after botulinum toxin injection to the
lower extremities
Passive range of lower-extremity joints: less than 10˚ contracture of
hip in extension measured by the Thomas Test; at least 20˚ range
in hip abduction; less than 5˚ knee flexion contracture, and
popliteal angle less than 45˚; more than 0˚ ankle dorsiflexion
with knee extended and foot in varus
GMFCS, Gross Motor Function Classification System (Palisano et al.
1997).
improvements in gait in two children with CP while walking with
P-FES (Pierce et al. 2004). Both participants received percutaneous stimulation to the TA and GA muscles alone and to
GA/TA simultaneously at appropriate times during the gait
cycle. Improvements in peak dorsiflexion in swing, mean dorsiflexion in swing, ankle dorsiflexion angle at initial contact,
and ankle work during early stance were noted for both children with TA and GA/TA stimulation. Both children showed
improvements in ankle work during late stance in all stimulation conditions. It is important that the immediate effects of
P-FES on gait be understood in order to establish the efficacy
of the intervention before assessing its use in longer-term
training studies.
The purpose of this investigation was to determine the
feasibility of using P-FES to produce immediate effects on
ankle kinematics and kinetics in children with CP when applied
to the GA and TA during the gait cycle. There were three aims of
the study with the following hypotheses. (1) Stimulation to the
TA while walking as compared with walking without stimulation will result in the following: (i) increased ankle dorsiflexion
at initial contact; (ii) increased peak ankle dorsiflexion during
swing; (iii) increased mean ankle dorsiflexion during swing
phase; (iv) increased stride length; (v) increased walking velocity; and (vi) decreased power absorption by the ankle during
loading response. (2) Stimulation to the GA while walking as
compared with walking without stimulation will result in the
following: (i) increased stride length; (ii) increased walking velocity; (iii) increased ankle moment at push off; and (iv)
increased ankle power generation at push-off. (3) Stimulation
to the TA and GA while walking as compared with walking without stimulation will result in the following: (i) increased ankle
dorsiflexion at initial contact; (ii) increased peak dorsiflexion
during swing; (iii) increased mean ankle dorsiflexion during
swing phase; (iv) increased stride length; (v) increased walking
velocity; (vi) decreased power absorption by the ankle during
loading response; (vii) increased ankle power generation at
push-off; and (viii) increased ankle moment at push off.
Method
PARTICIPANTS
Participants were recruited through the CP clinic at Shriners
Hospitals for Children in Philadelphia, Pennsylvania, USA. The
Institutional Review Board of Temple University in Philadelphia approved the study. Informed consent was obtained
from each child’s parent or guardian. A convenience sample
was chosen consisting of eight children with CP with a mean
age of 9 years 1 month (SD 1y 4mo). Inclusion criteria are
Table II: Demographic information on all participants
Participant
1
2
3
4
5
6
7
8
Age (y:m)
Sex
CP type
More affected limb
Height (cm)
Weight (kg)
GMFCS level
9:1
7:11
8:2
8:9
8:8
11:10
10:4
8:1
M
M
M
F
F
M
F
F
Diplegia
Diplegia
Hemiplegia
Diplegia
Diplegia
Diplegia
Hemiplegia
Diplegia
Right
Right
Right
Left
Right
Left
Right
Right
123
120
121
115
127
149
134
134
26
19.6
23.3
20.6
32.3
65.9
23.6
45
II
II
I
II
II
I
I
I
GMFCS, Gross Motor Function Classification System (Palisano et al. 1997).
Feasibility of P-FES in Children with CP Margo N Orlin et al.
685
listed in Table I. There were two participants with spastic hemiplegia and six with spastic diplegia. Four were classified in level
I and four were classified in level II of the Gross Motor Function
Classification System (GMFCS; Palisano et al. 1997). Table II
lists the demographic information on all study participants.
PROCEDURE
Intramuscular electrodes (NeuroControl Corporation, Valley
View, OH, USA) with a needle insertion procedure were
used to deliver the stimulation. Memberg et al. (1994) provide details on electrode design but a brief description is provided here. The electrode leads are created from a double
helix of cables composed of stainless steel filaments covered
in FEP-Teflon (DuPont Company, Wilmington, DE, USA). The
entire double helix is contained within medical-grade Silastic
tubing (Dow Corning, Midland, MI, USA) to prevent the electrode from binding down to the tissue beneath the skin surface. The tip of the electrode has a polypropylene anchor
with five barbs around a central core, which hold the electrode in place within the muscle tissue. After the electrode
is implanted, the Silastic tubing exposed above the skin is
stripped away and the Teflon coating at the skin interface is
left in place to allow tissue growth around the lead to hold
it in place. The leads are placed in a block for connection to
the stimulator.
Four channels for the children with diplegia and two channels for the children with hemiplegia of a research-grade electrical stimulator provided control of muscle stimulation through
the percutaneous electrodes. The electrode leads exiting from
the skin and contained in the connector block on the anterior thigh were placed underneath the clothing and attached
to the stimulator worn by the individual in a waist pack. The
stimulator used a charge-balanced asymmetrical stimulation
waveform. Pulse durations and frequencies were individualized for patients based on strength of contraction and patient
comfort. The stimulation patterns contained in the stimulator used during walking were unique to each child. The goal
Figure 1: Illustration of coordination
of dorsiflexors and plantarflexors for
gait training by electrical
stimulation. Stimulation pattern is
shown in reference to the highlighted
leg. Timing of electrical stimulation
delivery was controlled through
detection of initial contact,
midstance, and terminal stance via
the force-sensing resistor in the shoe.
Stimulation was applied to
gastrocnemius and tibialis anterior
of both legs to children with spastic
diplegia and to the involved leg for
children with hemiplegia. Adapted
from Fig. 7.11 in Sutherland et al.
(1998), p 147, and reprinted with
permission of Cambridge University
Press. FS, foot-strike; OTO, opposite
toe-off; OFS, opposite foot-strike;
TO, toe-off.
686
FS
OTO
Developmental Medicine & Child Neurology 2005, 47: 684–690
of individualizing the stimulation parameters for the TA was
to produce a contraction against gravity through the full range
of motion while in the seated position. For the GA, the goal
was to produce a maximal contraction to the child’s tolerance
during the gait cycle. Using these goals, the pulse durations
used ranged from 12 to 200 seconds and the frequencies from
20 to 50Hz. The amplitude was set at 20mA.
The implant procedure was performed with the patient
under general anesthesia. An intramuscular electrode was
implanted in the TA near the fibular head of the participant’s
right leg and at the motor end-point of the lateral head of the
GA. The motor end point was used as the site at which an
optimal stimulated response was obtained. Electrical stimulation to a 25-gauge insulated probe was initially used to identify the motor end point and confirmed with a larger blunt
intramuscular probe. A cannula was placed over the probe.
The probe was removed and the cannula was used as a guide
to insert the percutaneous electrode. Electrode placement and
responses were evaluated during the procedure to ensure that
the best possible response was identified. This was carried
out by visual inspection of muscle contraction elicited while
the muscle was stimulated. The ankle motion elicited by TA
stimulation was observed, to be certain that it was balanced
without too much inversion due to an uneven pull of the TA.
After electrode implantation, the electrode leads from GA
and TA muscles were tunneled subcutaneously to a common
exit site on the proximal anterior thigh. Gauze and a clear
plastic bandage were used to cover the exit site to protect the
electrodes. Children with spastic diplegia all had electrodes
implanted in both limbs; children with hemiplegia had electrodes implanted on their affected side only. On postoperative day one, the electrodes were tested to determine that
the stimulated contractions continued to be optimal. The
electrodes were then crimped and placed into a block to
connect into the stimulator box.
Before implantation of the electrodes, the process for control of stimulation was initiated. Force-sensing resistors (FSRs;
OFS
TO
FS
Interlink Electronics, Camarillo, CA, USA), embedded in an
insole worn in the shoes, were used to detect gait cycle events
for the control and timing of stimulation for each individual
while walking. The F-scan plantar pressure insole (TekScan
Inc., Boston, MA, USA) was used to determine FSR placement. Before implantation of the electrodes, participants
wore the F-scan insoles in each shoe while walking so that
plantar pressures could be recorded over three to five steps.
Specific areas of greatest plantar pressure at three gait events
(initial contact, mid-stance, and terminal stance) were recorded and the insole with embedded FSRs was fabricated. The
FSRs detected gait events and delivered stimulation to the
appropriate muscles at the correct time during the gait cycle
through an interface with a portable stimulator used by the
child during walking practice. Participants walked with the
insoles to determine the combination of FSR signals and the
threshold pressure levels to be used to detect each gait event.
Table III: Parameters used to determine Normalcy Index for
each participant
Percentage of gait cycle when foot-off occurs
Step length
Cadence
Velocity
Average pelvic tilt
Pelvic obliquity range
Average pelvic obliquity
Pelvic rotation range
Maximum hip extension
Maximum hip flexion
Knee flexion at initial contact
Maximum knee flexion in swing
Average knee flexion in stance
Knee range of motion
Dorsiflexion at initial contact
Maximum dorsiflexion in stance
Maximum plantar flexion in swing
Maximum dorsiflexion in swing
Foot progression angle
Figure 1 shows the timing pattern of the stimulation delivered
during walking. The FSRs have been shown to detect gait
events accurately during stance in a sample of seven children with CP in 94.5% of 642 steps (Smith et al. 2002).
After 1 week of recuperation at home, participants returned
to begin walking practice. Participants practiced walking with
the electrical stimulation under three randomly ordered conditions. The three conditions were GA stimulation on (GA),
TA stimulation on (TA), and both GA and TA (GA/TA) stimulation on. Participants practiced for two 45-minute walking sessions per day for about 1 week under each condition. A therapist
used a manual switch to turn the stimulation program on and
off as needed. The stimulation program continued during
walking, until the therapist stopped the program manually
with another switch at the end of the practice session. Rests
were given as needed during the sessions.
Immediately after the practice week in each condition, a
standard three-dimensional gait analysis was conducted in
both stimulation on and stimulation off conditions using a
six-camera Vicon motion-capture system (Vicon Motion Systems, Tustin, CA, USA) at the participant’s self-selected walking
speed.
Data collection took about 1 to 2 hours. Retroreflective markers were attached to the bilateral lower extremities with tape
and secured with non-adhesive wrap on the following anatomical locations: sacrum, anterior superior iliac spine, lateral
aspect of the mid-thigh, mid-calf, lateral malleolus, base of the
heel, and the dorsal aspect of the foot between the second and
third metatarsal bones (Davis et al. 1991). A static calibration
trial was collected before the walking trials, with a triaxial marker set (knee alignment device; Motion Lab Systems, Inc., Baton
Rouge, LA, USA) to define the knee flexion and extension axes.
After the standing calibration, the knee alignment device
was removed and a marker was placed on the lateral femoral
condyle. Video data, collected at 60Hz, and ground reaction
force data, collected at 1200Hz, were recorded simultaneously.
Four force plates (Advanced Mechanical Technology, Inc.,
Watertown, MA, USA), embedded within the walkway, were
used to collect kinetic data during the walking trials. During
and immediately after each trial, force-plate contacts were
Table IV: Data and results for statistical comparison – tibialis anterior condition only
Variables
More affected
DF at IC,˚
Peak DF in swing,˚
Mean DF in swing,˚
Stride length, m
Walking velocity, m/s
Absorption work, W/kg
Less affected
DF at IC,˚
Peak DF in swing,˚
Mean DF in swing,˚
Stride length, m
Walking velocity, m/s
Absorption work, W/kg
Stim. off
Mean (SD)
Stim. on
Mean (SD)
Mean (SD)
Change
95% CI
Uncorrected p
–2.9 (5.6)
0.6 (6.5)
–8.2 (7.6)
1.03 (0.1)
1.10 (0.1)
–0.12 (0.04)
1.6 (5.7)
3.5 (5.6)
–4.5 (7.7)
1.05 (0.1)
1.12 (0.1)
–0.09 (0.03)
4.42 ↑ (3.19)
2.96 ↑ (2.25)
3.69 ↑ (3.45)
0.02 ↑ (0.03)
0.03 ↑ (0.06)
0.03 ↑ (0.03)
1.7 to 7.1
1.1 to 4.8
–0.8 to 6.6
–0.01 to 0.05
–0.03 to 0.07
0 to 0.06
0.012
0.014
0.038
>0.1
>0.1
0.082
–4.9 (3.3)
–2.4 (3.7)
–10.7 (6.1)
1.03 (0.1)
1.10 (0.1)
–0.10 (0.03)
.01 (3.3)
3.1 (4.7)
–5.5 (7.0)
1.04 (0.1)
1.11 (0.1)
–0.06 (0.02)
5.01 ↑ (3.21)
5.5 ↑ (3.67)
5.2 ↑ (4.82)
0.01 ↑ (0.04)
0.01 ↑ (0.07)
0.03 ↑ (0.03)
1.6 to 8.4
1.7 to 9.3
0.1 to 10.3
–0.03 to 0.04
–0.05 to 0.07
–0.02 to 0.09
0.024
0.028
0.092
>0.1
>0.1
>0.1
Stim. off, stimulation off; Stim. on, stimulation on; CI, confidence interval; DF, dorsiflexion; IC, initial contact; ↑, improvement. For kinematic
values, positive is dorsiflexion and negative is plantarflexion.
Feasibility of P-FES in Children with CP Margo N Orlin et al.
687
confirmed. The test continued until three force-plate contacts
were collected bilaterally for both the stimulation on and stimulation off conditions. The two conditions (stimulation on and
stimulation off) were initially alternated approximately after
every second trial. When sufficient data were collected for one
condition (i.e. three total foot strikes on the force plates), walking trials continued with the remaining condition only. Ankle
joint kinematic, ankle kinetic, and temporal–spatial data were
determined with Vicon Clinical Manager Software (Oxford
Metrics, Vicon Motion Systems, Lake Forest, CA, USA) and
custom-written software in Matlab (The MathWorks, Inc.,
Natick, MA, USA).
DATA ANALYSIS
For data analysis purposes, participants’ more affected and
less affected legs were analyzed separately. This was done so
that data from children with diplegia and hemiplegia could
be grouped together. To distinguish the ‘more affected’ side,
an index to determine the magnitude of the deviation from
typical gait was calculated for three gait cycles on each leg
and then averaged for each leg separately. The index was calculated by principal component analysis from the data of 36
children with typical development collected in the laboratory at Shriners Hospitals in Philadelphia. When the data from
the individuals with atypical gait are compared with this normal database, an index score or a number representative of
the amount of deviation from a typical gait pattern is determined. A larger number is indicative of a more atypical gait
pattern. The limb with the greater value was determined to
be the more affected side.
Table III lists the gait parameters used to calculate this
index. The parameters used include temporal–spatial and kinematic variables. Using principal component analysis, these
variables differ slightly from the variables in previous literature, but the technique is the same (Novacheck et al. 2002,
Schutte et al. 2000). The results of the calculated index were
compared with the clinical determination provided by the physical therapist who examined each child. This determination
was made after a detailed clinical examination and observation of videotapes of walking. In all cases except one, the calculated index and clinical determination agreed. For the one
that disagreed, the clinical determination was accepted.
Data were analyzed with the use of paired one-tailed t-tests
with comparisons made between the on and off stimulation
conditions. Each aim focused on one of the muscle stimulation protocols, namely the TA (aim 1), GA (aim 2) and GA/TA
(aim 3). Within each aim, the more affected and less affected
legs were tested separately. Each aim and side was considered
to be a family of tests. To control for an inflated type I error
rate, Bonferroni corrections were made for the number of tests
in each family of aims. Thus, the significance criteria were 0.006,
0.0125, and 0.0055 respectively, for each family of aims.
Results
Descriptive data and results for all statistical comparisons for
the three aims are given in Tables IV–VI. Uncorrected p values
are reported in the Tables. Two significant differences were
noted in the GA/TA condition: peak dorsiflexion in swing on
the more affected side (t=4.99, p=0.004) and dorsiflexion at
initial contact on the less affected side (t=0.004, p=0.004).
The actual changes from stimulation off to stimulation on
were 2.8˚ and 4.36˚ respectively.
On the basis of the corrected p values, there was no significant difference in the TA only and GA only conditions, but
several trends of clinical importance were noted. In the TA
condition, on the more affected side there was a trend toward improvement in dorsiflexion at initial contact (t=3.91,
p=0.012), peak dorsiflexion in swing (t=3.70, p=0.014), and
mean dorsiflexion in swing ( t=3.02, p=0.038). For these variables, the increases in dorsiflexion were 4.42˚, 2.96˚, and
3.69˚ respectively. In the TA condition, on the less affected
side, both dorsiflexion at initial contact (t=3.81, p=0.024)
and peak dorsiflexion in swing (t=3.67, p=0.028) improved,
by 5.01˚ and 5.5˚ respectively. Positive trends were also seen
in the GA/TA condition. On the more affected side, dorsiflexion at initial contact increased by 4.84˚ (t=2.81, p=0.062). On
the less affected side, peak dorsiflexion in swing increased by
2.97˚ (t=3.86, p=0.024) and mean dorsiflexion in swing
increased by 3.98˚ (t=4.47, p=0.014).
Discussion
The purpose of our study was to determine the feasibility of
implanting percutaneous electrodes in lower-extremity muscles in children with CP and to have these children walk with
stimulation of the muscles applied at appropriate points in
the gait cycle to affect immediate changes in gait. In feasibility
studies the requirements for sample size determination are
not as stringent as in randomized controlled trials. Feasibility
Table V: Data and results for statistical comparison – gastrocnemius condition only
Variables
More affected
Stride length, m
Walking velocity, m/s
Ankle positive work, W/kg
Ankle moment, Nm/kg
Less affected
Stride length, m
Walking velocity, m/s
Ankle positive work, W/kg
Ankle moment, Nm/kg
Stim. off
Mean (SD)
Stim. on
Mean (SD)
Mean (SD)
Change
95% CI
Uncorrected p
1.02 (0.12)
1.10 (0.13)
0.11 (0.04)
0.64 (0.15)
1.04 (0.13)
1.14 (0.14)
0.12 (0.04)
0.61 (0.20)
0.02 ↑ (0.06)
0.04 ↑ (0.12)
0.01 ↑ (0.05)
0.03 ↓ (0.08)
–0.03 to 0.07
–0.06 to 0.14
–0.04 to –0.04
–0.10 to 0.05
>0.1
>0.1
>0.1
>0.1
1.02 (0.13)
1.10 (0.15)
0.09 (0.02)
0.69 (0.14)
1.05 (0.13)
1.14 (0.14)
0.10 (0.03)
0.63 (0.21)
0.03 ↑ (0.04)
0.04 ↑ (0.12)
0.01 ↑ (0.03)
0.06 ↓ (0.10)
0.0 to 0.07
–0.05 to 0.15
–0.05 to 0.03
–0.18 to 0.06
>0.1
>0.1
>0.1
>0.1
Stim. off, stimulation off; Stim. on, stimulation on; CI, confidence interval; ↑, improvement; ↓, decline. For kinematic values, positive is
dorsiflexion and negative is plantarflexion.
688
Developmental Medicine & Child Neurology 2005, 47: 684–690
studies are comparable to pilot studies in that the goal of the
study is to determine the efficacy of the methodology and procedures, as well as to obtain an estimate of intraparticipant
variability. We were able to measure the short-term application of P-FES on gait function for these children, resulting in
estimates of intraparticipant variability on selected spatial–temporal, kinematic, and kinetic gait variables with and without
stimulation. These estimates are important for establishing a
baseline performance of the direct application of P-FES.
Our focus in this study was on detecting gait function values comparable to previous gait studies that employed FES
(Carmick 1993, 1995; Bertoti et al. 1997; Comeaux et al. 1997)
for a longer duration. Importantly, we also controlled for type
I errors for each aim of the study. The decision to correct for
multiple comparisons was made to minimize the risk of type I
error due to the invasive nature of the intervention. The number of potentially statistically significant comparisons in the
TA only and GA/TA condition would have increased markedly
from 3% to 33% of comparisons between the on and off conditions if we had not corrected for multiple comparisons in
our data analysis.
Two significant increases in DF angle during stimulation,
peak dorsiflexion in swing on the more affected side, and dorsiflexion at initial contact on the less affected side were found
in the GA/TA condition but not in the TA condition. It is important to note that the magnitude of change was very similar for
each of these measures in the two conditions, even though in
the TA condition (Table V) the differences were not statistically
significant. The lack of difference in the TA condition may be
due to the larger variability and wider confidence intervals in
that condition for these two variables. This would suggest
that whereas the GA/TA and TA conditions effected a positive
change in the amount of ankle dorsiflexion, the change was
less variable in the GA/TA condition. Presumably, the GA/TA
condition provided coordinated muscle activation and sensory
feedback by stimulating GA/TA muscles around the joint during appropriate times in the gait cycle. Consequently, stimulating GA/TA muscles may produce a more consistent outcome
than stimulation of each muscle separately. We contend that a
finding of this type merits further investigation.
The improvement of about 4.5 to 5˚ of dorsiflexion at initial contact found in both the TA and GA/TA conditions is clinically meaningful because a 2.6˚ change in the angle of the
stance limb ankle has been shown to affect swing-limb foot
clearance (Winter 1992). These changes in ankle dorsiflexion
angle could potentially improve foot clearance for children
with CP who often have difficulty with tripping during walking.
In the TA condition, both the peak and mean dorsiflexion
angle in swing were improved relative to the off condition
and were of comparable magnitudes to those in other studies
(Carmick 1993, 1995; Comeaux et al. 1997). The magnitude
of this improvement (2.96˚ and 3.69˚ respectively) is clinically
significant because a joint angle change of 2.07˚ has been
shown to alter foot clearance significantly (Winter 1992).
Our hypothesis that stimulation would improve ankle
kinetics and temporal–spatial gait parameters was not supported by the data. There was no change in any of these variables, indicating that the short-term application of P-FES was
insufficient to modify them. Temporal–spatial gait characteristics are often difficult to change, particularly in children with
diplegic CP (Abel and Damiano 1996), especially with shortterm applications, as in the 1 week in this study. Bertoti et al.
(1997) reported a step length increase of 7.7cm in a child with
CP after 7 months of gait training with P-FES with six lowerextremity muscles implanted. However, with 7 months of training and multiple muscles stimulated, this child was unable to
affect a velocity change. Multiple factors have the potential to
affect temporal–spatial variables, including the amount of motor
impairment, pelvis, hip and knee function, range of motion,
and balance. In this sample, the children were classified at
Table VI: Data and results for statistical comparison – gastrocnemius/tibialis anterior conditions
Variables
More affected
DF at IC,˚
Peak DF in swing,˚
Mean DF in swing,˚
Stride length, m
Walking velocity, m/s
Absorption work, W/kg
Ankle positive work, W/kg
Ankle moment, Nm/kg
Less affected
DF at IC,˚
Peak DF in swing,˚
Mean DF in swing,˚
Stride length, m
Walking velocity, m/s
Absorption work, W/kg
Ankle positive work, W/kg
Ankle moment, Nm/kg
Stim. off
Mean (SD)
Stim. on
Mean (SD)
Mean (SD)
Change
95% CI
Uncorrected p
–6.0 (7.2)
–2.2 (7.0)
–11.3 (9.3)
1.05 (0.14)
1.13 (0.14)
–0.09 (0.04)
0.13 (0.04)
0.47 (0.22)
–1.2 (6.4)
0.6 (7.3)
–8.5 (10.3)
1.09 (0.12)
1.16 (0.12)
–0.08 (0.04)
0.12 (0.04)
0.45 (0.30)
4.84 ↑ (4.55)
2.8 ↑ (1.51)
2.8 ↑ (3.0)
0.03 ↑ (0.02)
0.03 ↑ (0.09)
0.01 ↑ (0.04)
0.01 ↔ (0.01)
0.02 ↔ (0.10)
0.6 to 9.0
–4.2 to –1.4
–5.5 to 0.0
–0.08 to 0.01
–0.11 to 0.04
–0.05 to 0.03
–0.004 to 0.03
–0.09 to 0.12
0.062
0.004a
0.100
>0.1
>0.1
>0.1
>0.1
>0.1
–3.0 (6.9)
1.8 (5.4)
–6.6 (4.3)
1.08 (0.15
1.14 (0.14)
–0.08 (0.04)
0.12 (0.03)
0.53 (0.21)
1.4 (6.1)
4.8 (3.8)
–2.7 (4.1)
1.07 (0.13)
1.12 (0.12)
0.08 (0.05)
0.11 (0.04)
0.48 (0.27)
4.36 ↑ (1.89)
2.97 ↑ (1.89)
3.98 ↑ (2.18)
0.005 ↔ (0.04)
0.02 ↔ (0.08)
2.3 ↑ (6.67)
0.007 ↔ (0.01)
0.05 ↓ (0.07)
2.4 to 6.3
1.0 to 5.0
1.7 to 6.3
–0.04 to 0.03
–0.09 to 0.04
–0.06 to 0.07
–0.02 to 0.01
–0.14 to 0.04
0.004a
0.024
0.014
>0.1
>0.1
>0.1
>0.1
>0.1
Stim.off, stimulation off; Stim.on, stimulation on; CI, confidence interval; DF, dorsiflexion; IC, initial contact; ↔, no change; ↑, improvement; ↓,
decline. aSignificant p value correcting for multiple comparisons. For kinematic values, positive is dorsiflexion and negative is plantarflexion.
Feasibility of P-FES in Children with CP Margo N Orlin et al.
689
GMFCS levels I and II with stride length and velocity values
close to typical levels (Steinwender et al. 2000). There might,
therefore, have been a ceiling effect, and additional improvement might have been even more difficult to achieve. The
short-term application of P-FES might not be enough to modify
these values, so a longer-term application with practice might
be required to make this change.
Because our investigation examined only the immediate
effects of percutaneous stimulation on gait in children with CP,
the long-term effects of training with percutaneous stimulation
on gait and function are unknown. Additional controlled studies with a larger sample of children randomly assigned into
control and stimulation groups, along with a more extended
practice period, will be necessary to establish the efficacy of
FES as a rehabilitation intervention. Future comparisons of
surface and percutaneous stimulation are also necessary to
determine the relative effectiveness of each modality.
Conclusion
This study provided evidence that P-FES applied to the TA and
GA muscles together at appropriate times in the gait cycle is a
feasible method of immediately improving ankle dorsiflexion in children with spastic diplegic or spastic hemiplegic CP.
Trends also indicated that stimulation of the TA alone might also
improve ankle dorsiflexion during gait. All of the improvements
that were noted produced clinically meaningful change. Neither
temporal–spatial or kinetic characteristics of gait changed with
stimulation, suggesting that these attributes might be more
difficult to modify, particularly with a short-term application
of P-FES. Because this feasibility study used a short-term application of P-FES to produce only an immediate change, more
study is needed to determine the long-term effects of P-FES
with practice as a way of improving overall ambulatory function in children with spastic CP.
DOI: 10.1017/S0012162205001398
Accepted for publication 17th November 2004.
Acknowledgements
This study was funded by Shriners Hospitals for Children, grant no. 8530.
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List of abbreviations
FES
FSR
GA
P-FES
TA
Functional electrical stimulation
Force-sensing resistor
Gastrocnemius
Percutaneous intramuscular functional electrical
stimulation
Tibialis anterior