Journal of Pediatrics
Volume 137 • Number 3 • September 2000
Copyright © 2000 Mosby, Inc.
Original Articles
An evaluation of botulinum-A toxin injections to improve upper
extremity function in children with hemiplegic cerebral palsy
Darcy Fehlings MD, MSc
Mercer Rang MB, BS
Janet Glazier BSc(OT)
Catherine Steele PhD
From the Division of Neurology and General Pediatrics, Department of Pediatrics and the Division of
Orthopedics, Department of Surgery, Bloorview MacMillan Centre and The Hospital for Sick Children,
Toronto, Ontario, Canada.
Supported by the Easter Seal Research Institute (Kids Action Research).
Submitted for publication Oct 13, 1999.
Revision received Feb 23, 2000.
Accepted Apr 28, 2000.
Reprint requests: Darcy Fehlings, MD, MSc, Bloorview MacMillan Centre, 350 Rumsey Rd, Toronto,
Ontario, M4G 1R8, Canada.
Copyright © 2000 by Mosby, Inc.
0022-3476/2000/$12.00 + 0 9/21/108393
Objective: In a randomized, controlled, single-blind trial, to test the hypothesis
that botulinum-A toxin (BTA) injections into the upper extremity of children with
spastic hemiplegia improve upper extremity function.
Study design: Thirty children with hemiplegia, aged 2.5 to 10 years, were
randomly assigned to receive: (1) a BTA injection into 1 or more of 3 muscle
groups (biceps, volar forearm muscles, adductor pollicis) plus occupational
therapy or (2) occupational therapy alone. Blinded outcomes obtained at baseline
and at 1, 3, and 6 months included the Quality of Upper Extremity Skills Test
(QUEST), goniometry measurements, grip strength, and Ashworth scores. The
caregiver completed the self-care domain of the Pediatric Evaluation of Disability
Inventory.
Results: Twenty-nine subjects completed the study. The QUEST demonstrated a
significant improvement favoring the treatment group on a 2-way analysis of
variance (F = 4.69, df = 1,83; P = .039). BTA treatment was also associated with an
improvement in score on the self-care domain of the Pediatric Evaluation of
Disability Inventory (F = 4.68, df = 1,82; P = .04).
Conclusions: This study supports the effectiveness of BTA injections to improve
upper extremity function of children with hemiplegia who have at least moderate
spasticity. (J Pediatr 2000;137:331-7)
ANOVA
Analysis of variance
BTA
Botulinum-A toxin
CP
Cerebral palsy
PEDI
Pediatric Evaluation of Disability Inventory
QUEST
Quality of Upper Extremities Test
See editorial, p. 300.
Intramuscular injections of Clostridium botulinum-A toxin into spastic muscles cause a
local temporary muscle paralysis associated with decreased spasticity. The biologic
effects of BTA are well understood. [1] Botulinum toxin has been used therapeutically in
adults over the last 25 years in neuromuscular conditions associated with focal dystonia
(strabismus, torticollis).[2]
The use of BTA in cerebral palsy[3] has received much interest recently because of the
high prevalence of CP (1-2 in 1000 in developed countries)[4] [5] and conservative nature
of the treatment. It is postulated that by decreasing spasticity, there will be improved
control of movement patterns, stretching and increased excursion of shortened muscles,
improved posture, and secondary strengthening of antagonistic muscles. By implication,
these changes should be associated with improved motor function. Most studies to date
have focused on the use of BTA injections into the lower extremity gastrocnemius
muscle and have demonstrated a temporary reduction in spasticity, temporary
improvement in gait, and improved range of motion.[6] [9] Minimal information is
available on the impact on function of upper extremity injections in children with CP.
Wall et al[10] report positive gains in function and cosmetic appearance in a prospective
case series of 5 children with a "thumb in palm" deformity associated with CP treated
with BTA injected into the adductor pollicis muscle and rigid splinting of the thumb.[10]
Denislic and Meh[11] injected BTA into the upper limbs of 10 children with CP and found
an improvement in upper limb function in 9. A double-blind controlled study by Corry
et al[12] reports mixed results on the impact on function in hemiplegic CP. Functional
improvements were not found 2 weeks after injection. A small improvement was found
at 12 weeks, favoring the BTA group in a grasp-and-release activity, but was not found
in another grasp activity (the ability to pick up coins).
We report the results of a randomized, controlled, single-blind trial of BTA injections
into the involved hand or arm of 30 children with hemiplegic CP using the Quality of
Upper Extremity Skills Test, a standardized measure of quality of function of the upper
extremity, as our principal outcome.
METHODS
Participants
Eligible children met the following criteria: 2.5 to 10 years of age; a diagnosis of
hemiplegic CP; moderate spasticity at the elbow, wrist, or thumb with a modified
Ashworth score 2[13] ; full passive range (defined in this study as elbow extension to
neutral, wrist extension to 30 degrees past neutral with the fingers extended, forearm
supination to 30 degrees past neutral, and thumb extension to neutral); and the ability to
initiate voluntary movement of the digits. Children were excluded if they were using a
rigid splint to maximize homogeneity and allow active movement in the hand.
Study Design
The study was approved by the Bloorview MacMillan Centre Research Ethics Review
Board. The ethics board, guided by Canadian ethical standards, did not grant approval
for a double-blind BTA study in which the control group would receive an
intramuscular injection of saline solution because this was judged to be too painful and
invasive for a placebo.[14] When the eligibility criteria were met and written informed
consent was obtained, children were randomly assigned, by using a uniform random
number generator, to a treatment or control group. The treatment group received an
intramuscular injection of BTA (Botox, Allergan, USA), at a dosage of 2 to 6 U/kg
body weight, into at least 1 of 3 muscle groups (biceps, volar forearm muscles, or
adductor pollicis muscle). Two investigators (D.F. and M.R.) determined jointly which
muscle groups to inject during reach-and-grasp activities of the involved hand or arm. If
the child demonstrated persistent elbow flexion, the biceps was injected; for thumb
adduction, the adductor pollicis muscle was injected. In the volar forearm muscles, for
pronation, the pronator teres muscle was injected; wrist flexion was an indication for
flexor carpi ulnaris muscle injections; and finger flexion was an indication for injection
of the finger flexors. The location of the injection was determined by anatomic
knowledge and muscle palpation.[15] [17] The biceps was injected in the top third of the
muscle at 2 sites, the volar flexor muscle was injected at 2 sites, 2 to 3 cm below the
medial epicondyle. The pronator teres was injected at one site in the upper third of the
muscle, and the adductor pollicis was injected in one site in the belly of the muscle.
Children in both groups were asked to continue with community-based occupational
therapy at a minimum frequency of one session every 2 weeks. Research funding was
not available to provide occupational therapy by research personnel. An occupational
therapy manual with guidelines was developed for the study and sent to each of the
participating occupational therapists. The guidelines were based on standard practice for
therapy management of spastic hemiplegia and incorporated activities for upper
extremity strengthening and the development of skills for activities of daily living.[18] [19]
Children were seen at baseline and at 1, 3, and 6 months. A single investigator (J.G.),
blinded to the subject group assignment, obtained all objective outcome measurements.
The primary outcome measure was the QUEST.[20] [22] This is an objective standardized
measure evaluating the quality of upper extremity function in 4 domains: dissociated
movement (an isolated joint movement of the upper extremity that counters a pattern of
spastic synergy), grasp, protective extension, and weight bearing. Scores for the QUEST
are calculated as percentages with a maximum score of 100. The QUEST was designed
with minimal developmental sequencing so that scoring reflects the severity of the
disability rather than age.
A caregiver completed the self-care domain of the Pediatric Evaluation of Disability
Inventory to assess the child's activities of daily living.[23] The self-care domain has 73
items in 15 skill areas, such as hand washing. Raw scores can be converted to a scaled
score with a 0 to 100 distribution based on Rasch scale modeling. The PEDI has been
designed to measure function in children with physical disabilities and has established
reliability, validity, and responsiveness.[23] [26]
Secondary outcome measures included manual goniometric measurements of passive
range of motion[27] ; modified sphygmomanometer measurements of grip strength[28] ; and
the modified Ashworth score of spasticity at elbow extension, wrist extension, forearm
supination, and thumb extension.[13] Test-retest reliability for passive goniometry
measurements and grip strength was evaluated before the study in children with upper
extremity spasticity and was found to be high, with correlation coefficients ranging
from 0.58 to 0.97.[29]
Statistical Analyses
The analyses were conducted by using the SAS microcomputer-based package. [30] The
following tests were used.
1. A preliminary analysis included a thorough check of the data (review of outliers
and missing data), a descriptive summary, and plots of each variable.
2. Chi-square and unpaired t tests were used to check the comparability of the BTA
treatment and control groups at baseline for age, sex, involved side, and baseline
Ashworth, QUEST, and PEDI scores.
3. A 2-way analysis of variance was computed to detect differences between the
BTA treatment and control groups during the study period in the QUEST, the
PEDI, grip strength, Ashworth scores, and passive goniometry measurements.
To account for baseline effects, the differences between baseline and 1 month,
baseline and 3 months, and baseline and 6 months were used. Statistical
significance was set a priori at P < .05 for the 2 functional outcomes, the
QUEST and the PEDI, and set at P < .01 for the secondary outcomes to account
for the multiple testing.
4. A post hoc Wilcoxon rank sums test was performed to examine the significance
of group differences at 1, 3, and 6 months for variables that demonstrated
statistical significance on the ANOVA.
RESULTS
Participant Characteristics
Fifty children were screened; 20 did not meet the eligibility criteria (13 had an
Ashworth score <2, 6 had an inability to initiate voluntary movement in the involved
hand, and 2 had fixed contractures). Thirty children were recruited into the study and
randomly assigned to the treatment (n = 15) and control (n = 15) groups. Thus 29
children completed the study, with one child in the treatment group dropping out before
the 1-month assessment. Table I outlines the comparability of the 2 groups at baseline.
Table I. Baseline comparability of the treatment and control groups*
Treatment group
(n = 14)
Control group
(n = 15)
P value
68 ± 31
64 ± 28
.71
Gender (M/F)
10/5
10/5
1.00
Involved side
(right/left)
10/4
7/8
.17
Modified Ashworth
score*
2.3 ± 0.75
2.2 ± 0.59
.89
QUEST baseline
19.2 ± 15.1
27.6 ± 19.0
.41
PEDI baseline
50.2 ± 11.1
52.2 ± 15.4
.25
56.40 ± 16.59
53.38 ± 21.33
.46
Characteristic
Age (mo)
Grip strength (mm
Hg)
Values are expressed as means ± SD.
*Represents the mean of Ashworth measurements for elbow and wrist extension,
forearm supination, and thumb extension.
No significant differences were found.
Table II outlines the BTA treatment for each child with respect to dosage and location.
Table II. Dosage and location of injection for each participant in the BTA treatment
group
Muscle injected (U/kg)
BTA
(U/kg)
QUEST
change (to
1 mo)
Volar
flexors
Pronator
teres
muscle
Adductor
pollicis
muscle
Biceps
1
4
36.67
--
4.0
--
--
2
4
4.48
--
4.0
--
--
3
2
19.36
2.0
--
--
--
4
4
12.19
--
4.0
--
--
5
4
8.53
--
4.0
--
--
Subject
No.
Table II. Dosage and location of injection for each participant in the BTA treatment
group
Muscle injected (U/kg)
BTA
(U/kg)
QUEST
change (to
1 mo)
Biceps
Volar
flexors
Pronator
teres
muscle
Adductor
pollicis
muscle
6
4
23.90
--
1.3
1.3
1.3
7
5.2
-1.97
--
3.6
1.6
--
8
3.8
21.37
--
2.9
--
1.0
9
4.3
2.21
3.2
1.1
--
--
10
2.7
0.78
--
1.8
--
0.9
11
3.3
-9.71
--
2.2
--
1.1
12
3.6
30.18
1.8
--
--
1.8
13
6.6
14.29
--
4.9
--
1.6
14
3.4
Dropout
--
1.1
1.1
1.1
15
6.3
12.79
1.6
3.2
--
1.6
Subject
No.
Both groups received occupational therapy in the community at a recommended
frequency of once every 2 weeks. The treatment group received a mean of 11.93 (SD
6.89) treatment sessions, and the control group received a mean of 16.07 (SD 7.60)
treatment sessions over the 6-month period of the study. This difference favored the
control group but was not statistically significant (P = .74).
Main Results
The total score for the involved side on the QUEST, the primary outcome measure,
demonstrated a statistically significant improvement favoring the BTA treatment group
on the ANOVA (F = 4.69, df = 1,83; P = .039). The time-group interaction was not
significant (P = .50). Post hoc testing with the Wilcoxon rank sum test showed
significant differences between the treatment and control groups at 1 month (P = .01)
but not at 3 (P = .13) or 6 months (P = .14). These results are outlined in the Figure.
Figure. Mean change from baseline in the QUEST total scores. Changes in scores were analyzed with 2way ANOVA. Post hoc Wilcoxon rank sums test was done at 1, 3, and 6 months. Asterisk indicates P <
.05 on post hoc testing.
On the 4 subtests of the QUEST, the subtest "weight bearing" (P = .009) showed a
significant improvement favoring the treatment group. On the other 3 subtests, results
favored the treatment group but were not statistically significant: "dissociated
movement" (P = .63), "grasp" (P = .33), and "protective extension" (P = .55).
The results of the PEDI and secondary outcomes are listed in Table III.
Table III. Results of the 2-way ANOVA for the secondary outcome measures
Change from baseline
One month
Three months
Six months
P value*
BTA group
2.00 ± 5.99
3.85 ± 5.11
6.77 ± 5.82
.04
Control group
-1.93 ± 5.78
1.13 ± 5.19
2.64 ± 5.75
BTA group
2.57 ± 6.91
2.78 ± 3.72
5.50 ± 4.54
Control group
-1.51 ± 4.07
1.09 ± 4.07
3.30 ± 6.05
BTA group
-7.60 ± 14.57
-6.86 ± 13.06
2.00 ± 12.74
Control group
1.50 ± 18.76
3.83 ± 22.81
-0.27 ± 20.77
BTA group
-0.29 ± 0.47
-0.23 ± 0.48
-0.38 ± 0.46
Control group
-0.20 ± 0.62
-0.37 ± 0.44
-0.29 ± 0.51
BTA group
-0.43 ± 0.43
-0.31 ± 0.38
-0.35 ± 0.43
Control group
-0.36 ± 0.44
-0.33 ± 0.45
-0.25 ± 0.55
BTA group
-0.32 ± 0.42
-0.35 ± 0.38
-0.27 ± 0.60
Control group
-0.20 ± 0.49
-0.20 ± 0.53
-0.18 ± 0.58
BTA group
-0.31 ± 0.48
-0.25 ± 0.40
-0.33 ± 0.39
Control group
-0.28 ± 0.57
-0.29 ± 0.54
-0.27 ± 0.48
BTA group
0.07 ± 6.62
5.46 ± 11.74
2.84 ± 6.69
Control group
-0.80 ± 6.62
3.00 ± 12.83
0.79 ± 9.32
BTA group
3.43 ± 9.00
5.15 ± 8.10
3.00 ± 12.08
Control group
1.67 ± 5.63
1.67 ± 6.28
0.64 ± 6.62
PEDI (raw score)
PEDI (scaled
score)
.08
Grip strength
(mm Hg)
.34
Ashworth/elbow
.89
Ashworth/wrist
.81
Ashworth/forearm
.51
Ashworth/thumb
.90
Elbow
extension
.11
Forearm
supination
Wrist
extension
.34
Table III. Results of the 2-way ANOVA for the secondary outcome measures
Change from baseline
One month
Three months
Six months
P value*
BTA group
4.08 ± 7.35
4.58 ± 11.92
2.00 ± 15.02
.55
Control group
0.67 ± 8.78
1.27 ± 9.91
2.07 ± 11.49
BTA group
2.14 ± 5.91
1.46 ± 8.52
2.77 ± 8.12
Control group
1.00 ± 7.97
-0.60 ± 10.01
1.21 ± 6.96
Palmar thumb
abduction
.48
Values are expressed as means ± SD.
*P value refers to the significance of overall differences between the BTA group and
control group on the ANOVA.
Goniometry measurements.
A statistical difference was found in the raw scores of the parent-completed self-care
domain of the PEDI (F = 4.68, df = 1; P = .04). The time-group interaction was not
significant (P = .84). Post hoc testing with the Wilcoxon rank sums test approached
significance at 1 month (P = .08) and 6 months (P = .06). The corresponding ANOVA
evaluating the PEDI scaled scores approached significance (F = 3.22, df = 1; P = .08).
No significant differences between the treatment and control groups were found in grip
strength, Ashworth scores, or passive goniometry measurements.
The injections in the treatment group were well tolerated. Aside from the discomfort of
the injection, only one child (Table II, subject 1) reported temporary decreased grip
strength lasting 2 weeks. No other side effects were noted.
DISCUSSION
This controlled clinical trial provides evidence to support the use of intramuscular BTA
injections to improve both quality of functional movement of the upper extremity and
functional capability in children with hemiplegic CP. A clinical and statistically
significant improvement in quality of function was found at 1 month. Children in the
BTA group improved from 19.2% on the QUEST at baseline to 32.5% at 1 month
compared with a 1.7% change in the control group. Moderate improvements were
maintained up to 6 months after injection. This is clinically important because the effect
of the BTA injection on function lasts longer than the neuromuscular blockade, which
disappears, on average, at 3 months.[1] In the control group a gradual improvement in
quality of function was found over the 6-month period of the study. The positive change
in function in the control group may reflect both the impact of the occupational therapy
intervention and developmental improvements with time; and this highlights the
importance of including a control group when studying changes in child development.
The improvement in the control group and low statistical power (16%) may explain the
lack of statistical significance at the 6-month testing. Within the subtests of the QUEST,
weight-bearing activities demonstrated the most change.
For children receiving the BTA injections, the parents also reported small positive
functional change in the children's self-care skills (eg, dressing, eating). This supports
carry-over of functional change into the children's regular environments and daily
activities.
Grip strength declined at 1 and 3 months in the BTA group but normalized by 6 months
after injection. This finding was expected because BTA blocks conduction at the
neuromuscular junction, which reduces spasticity but also causes muscle weakness.
Though the grip was weaker after BTA, function improved.
Differences in the modified Ashworth score of spasticity favored the BTA group but
were not significantly different. Both groups showed a decline in spasticity throughout
the period of the study. It is interesting to speculate on the reason for the decline in
spasticity within the control group. This may be secondary to developmental
improvements in spasticity with time, familiarity with the test, the impact of the
occupational therapy, or measurement variation.
The ideal dosage of BTA for upper extremity spasticity requires further research. It is
hard to predict the functional impact of higher dosing. Increasing the dosage will result
in a greater decline in spasticity but will also lead to greater reductions in grip strength,
which in turn may have a negative impact on functional outcome.
Passive range of motion also did not show a significant change between the BTA and
control groups. This reflects the excellent baseline flexibility of the selected subjects
who had full range in the majority of joint measurements assessed.
It is important to note that the positive effects on upper-extremity function observed
after BTA injection are generalizable to children who are clinically similar to the
subjects selected for the study. Many children with a clinical diagnosis of spastic
hemiplegic CP have Ashworth spasticity scores <2 or poor distal voluntary muscle
control. This clinical trial excluded both of these groups of children. Further research is
required before results are generalized to these subgroups.
A limitation of the study is the single-blind design. Both the children and their parents
knew whether they were in the treatment or the control group. This could have an
impact on the parent-completed PEDI. A single objective evaluator who was blinded to
the group assignment completed all other outcome measurements, including the
QUEST. The large number of subjects assessed and the similarity of changes in
Ashworth score between the 2 groups prevented the unintentional unblinding of this
evaluator, minimizing the impact of the single-blind design on the primary results of
this study.
Botulinum toxin injections were given without electromyographic guidance. This has
the advantage that conscious sedation is not required, which has fewer side effects and
allows the use of BTA in ambulatory and rehabilitation settings. Evaluation of the
individual responses of subjects showed that the BTA injection was successful (positive
change >5% on the QUEST) in 9 of 14 subjects. However, 5 subjects (33%) received a
BTA injection but did not show improvement in function. One potential explanation for
this is that the intended muscle groups were not targeted accurately. There is some
support for improved accuracy of BTA injections with electromyographic guidance in
the literature.[31]
Continued research is required to evaluate the dose response and the impact on function
of repeated BTA upper-extremity injections.
We thank the children and families who participated in the study. We also thank
Allergan for providing the botulinum-A toxin for the study.
REFERENCES
1. De
Paive A, Meunier FA, Molgo J, Aoki KR, Dolly JO. Functional repair of motor endplates after
botulinum neurotoxin type A poisoning: biphasic switch of synaptic activity between nerve sprouts and
their parent terminals. Proc Natl Acad Sci U S A 1999;96:3200-5. Abstract
2. Jankovic
J, Brin MF. Therapeutic uses of botulinum toxin. N Engl J Med 1991;324:1186-94. Citation
3. Gordon
N. The role of botulinum toxin type A in treatment--with special reference to children. Brain
Dev 1999;21:147-51. Abstract
4. Kuban
K, Leviton A. Cerebral palsy. N Engl J Med 1994;330:188-95. Citation
5. Murphy
CC, Yeargin-Allsopp M, Decoufle P, Drews CD. Prevalence of cerebral palsy among ten-year
old children in metropolitan Atlanta, 1985 through 1987. J Pediatr 1993;123:S13-S20. Abstract
6. Cosgrove
AP, Corry IS, Graham HK. Botulinum toxin in the management of the lower limb in cerebral
palsy. Dev Med Child Neurol 1994;36:386-96. Abstract
7. Koman
LA, Mooney JF III, Smith BP, Goodman A, Mulvaney T. Management of spasticity in cerebral
palsy with botulinum-A toxin: report of a preliminary, randomized, double-blind trial. J Pediatr Orthop
1994;14:299-303. Abstract
8. Calderon-Gonzalez
R, Calderon-Sepulveda R, Rincon-Reyes M, Garcia-Ramirez J, Mino-Arango E.
Botulinum toxin A in management of cerebral palsy. Pediatr Neurol 1994;10:284-8. Abstract
9. Sutherland
DH, Kaufman KR, Wyatt MP, Chambers HG. Injection of botulinum A toxin into the
gastrocnemius muscle of patients with cerebral palsy: a 3-D motion analysis study. Dev Med Child
Neurol Suppl 1995;73:17-8.
10. Wall
SA, Chait LA, Temlett JA, Perkins B, Hillen G, Becker P. Botulinum A chemodenervation: a
new modality in cerebral palsied hands. Br J Plast Surg 1993;46:703-6. Abstract
11. Denislic
M, Meh D. Botulinum toxin in the treatment of cerebral palsy. Neuropediatrics 1995;26:24952. Abstract
12. Corry
IS, Cosgrove AP, Walsh EG, McClean D, Graham HK. Botulinum toxin A in the hemiplegic
upper limb: a double-blind trial. Dev Med Child Neurol 1997;39:185-93. Abstract
13. Bohannon
RW, Smith MB. Interrater reliability of a modified Ashworth scale of muscle spasticity.
Phys Ther 1987;67:206-7. Abstract
14. Medical
Research Council of Canada. Guidelines on research involving human subjects. Ottawa,
Ontario, Canada: Ministry of Supply and Services Canada; 1987.
15. Russman
BS, Tilton A, Gormley ME. Cerebral palsy: a rational approach to a treatment protocol, and
the role of Botulinum toxin in treatment. Muscle Nerve Suppl 1997;6:S181-S193. Abstract
16. Thompson
17. Brash
JS. Core textbook of anatomy. Philadelphia: Lippincott; 1977.
JC, editor. Text-book of anatomy. 9th ed. London: Oxford University Press; 1951.
18. Boehme
R. Improving upper body control: an approach to assessment and treatment of tonal
dysfunction. Tucson: Therapy Skill Builders; 1988.
19. Exner
CE. Development of hand skills. In: Pratt PN, Allen AS, editors. Occupational therapy for
children. 3rd ed. St Louis: Mosby; 1989. p. 268-306.
20. DeMatteo
C, Law M, Russell D, Pollock N, Rosenbaum P, Walter S. Quality of Upper Extremity
Skills Test. Hamilton, Ontario (Canada): Neurodevelopmental Clinical Research Unit; 1992.
21. DeMatteo
C, Law M, Russell D, Pollock N, Rosenbaum P, Walter S. The reliability and validity of the
Quality of Upper Extremity Skills Test. Phys Occup Ther Pediatr 1993;13:1-18.
22. Law
M, Cadman D, Rosenbaum P, Walter S, Russell D, DeMatteo C. Neurodevelopmental therapy
and upper extremity inhibitive casting for children with cerebral palsy. Dev Med Child Neurol
1991;33:379-87. Abstract
23. Haley
SM, Coster SJ, Ludlow LH, Haltiwanger JT, Andrellos PJ. Pediatric evaluation of disability
inventory (PEDI): development, standardization, and administration manual. Boston: New England
Medical Center and PEDI Research Group; 1992.
24. Haley
SM, Ludlow LH, Coster WJ. Pediatric Evaluation of Disability Inventory: clinical interpretation
of summary scores using Rasch rating scale methodology. Phys Med Rehabil Clin North Am 1993;4:52940.
25. Reid
DT, Boschen K, Wright V. Critique of the Pediatric Evaluation of Disability Inventory. Phys
Occup Ther Pediatr 1993;13:57-87.
26. Wright
V, Boschen KA. 2nd National Rehabilitation Research Conference: outcome assessment in
rehabilitation. The Pediatric Evaluation of Disability Inventory (PEDI): validation of a new functional
assessment outcome instrument. Can J Rehabil 1993;7:41-2.
27. Trombly
CA, Scott AD. Occupational Therapy for physical dysfunction. Baltimore: The Williams and
Wilkins Company; 1977.
28. Helewa
A, Goldsmith CH, Smythe HA. The modified sphygmomanometer--an instrument to measure
muscle strength: a validation study. J Chronic Dis 1981;34:353-61. Citation
29. Glazier
JN, Fehlings DL, Steele C. Test-retest reliability of upper extremity goniometric measurements
of passive range of motion and of sphygmomanometer measurement of grip strength in children with
cerebral palsy and upper extremity spasticity. Dev Med Child Neurol Suppl 1997;75:33-4.
30. SAS
Institute Inc. SAS STAT user's guide, version 6. 4th ed. Cary (NC): SAS Institute Inc; 1989.
31. Ajax
T, Ross MA, Rodnitzky RL. The role of electromyography in guiding botulinum toxin injections
for focal dystonia and spasticity. J Neurol Rehabil 1998;12:1-4.