You are on page 1of 8

Official Journal of the European Paediatric Neurology Society

Original article
Bilateral spastic cerebral palsyPrevalence through four
decades, motor function and growth
Kate Himmelmann

, Eva Beckung, Gudrun Hagberg, Paul Uvebrant


The Queen Silvia Childrens Hospital/Sahlgrenska University Hospital, Go teborg, Sweden
a r t i c l e i n f o
Article history:
Received 29 September 2006
Received in revised form
21 December 2006
Accepted 24 December 2006
Keywords:
Cerebral palsy
Bilateral spastic
Prevalence
Motor function
Growth
a b s t r a c t
The aim was to depict changes in the prevalence and severity of bilateral spastic cerebral
palsy (CP) over a 40-year period. Another objective was to characterise the group born in
19911998 with respect to gross motor function, spasticity and growth. Data were obtained
from the CP register of western Sweden and rehabilitation records.
Results: After a rise to 1.27 per 1000 live births in 19831986, the prevalence decreased
signicantly, in children born both preterm and at term, to 0.69 in 19951998. After 1975,
more children were born preterm than at term. There was a signicant decrease in severe
bilateral spastic CP during the same period, mainly in children born at term. In all, 46% of
the children born at term and 33% of those born preterm had a severe motor impairment,
i.e. no walking ability. In the 167 children born in 19911998, the gross motor function
classication system (GMFCS) level was I in 14%, II in 34%, III in 10%, IV in 25% and Vin 17%.
The GMFCS level correlated with the gross motor function measure (GMFM) and the
Ashworth spasticity scores, as well as with the deviation in postnatal weight and height.
We conclude that the prevalence of bilateral spastic CP has decreased since the mid-
1980s, parallel to a reduction in the severity of the motor impairment. Children born
preterm have predominated since the mid-1970s. The severity of the motor impairment
correlated with the degree of spasticity, GMFM and growth. The percentage of children who
were underweight was substantial.
& 2007 European Paediatric Neurology Society. Published by Elsevier Ltd. All rights reserved.
1. Introduction
The panorama of cerebral palsy (CP) in western Sweden has
been closely monitored for four decades in an ongoing study,
currently covering the birth years 19591998. Epidemiology,
distribution of types of CP and accompanying impairments
have been described
19
and gross and ne motor function in
children born in 19911998 were recently reported.
10
The
group of spastic diplegia constitutes more than one-third of
all CP and even more if combined with the group of spastic
tetraplegia into the concept of bilateral spastic CP,
11,12
as
proposed by the Surveillance of CP in Europe (SCPE)
13
and
the Washington workshop on denition and classication
of CP.
14
This concept has been widely accepted as an
alternative to the often confusing terms diplegia, tetraplegia,
quadriplegia and double hemiplegia, with varying denitions
between countries and authors.
10,11,13,15
It has given us the
means not only to describe but also to compare between
populations, evaluate change and predict needs in this
particular group.
Other issues that have been brought to attention in recent
years are the prerequisites for activity and participation,
8,16
as
ARTICLE IN PRESS
1090-3798/$ - see front matter & 2007 European Paediatric Neurology Society. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.ejpn.2006.12.010

Corresponding author. Tel.: +46 31 502623; fax: +46 31536832.


E-mail address: kate.himmelmann@vgregion.se (K. Himmelmann).
E UR OP E A N J OUR NA L OF PAE DI AT R I C NE UR OL O GY 11 ( 2007) 215 222
well as the nutrition and growth of children with CP.
Intrauterine growth may sometimes deviate,
17
but the post-
natal growth deviation,
18
which may result in shortness and
often severe underweight, is even more signicant.
The aims of this study were to depict changes in the live
birth prevalence and severity of motor impairment in
bilateral spastic CP over time in western Sweden, to describe
differences between children born preterm and at full-term
and to characterise the group with respect to motor function,
spasticity and growth.
2. Material and methods
The prevalence of bilateral spastic CP and the severity of the
gross motor impairment, categorised as independent walking
(mild), walking with aids (moderate) and wheel-chair depen-
dence (severe), were analyzed in 763 children with bilateral
spastic CP from a total of 1683 children with CP born in
19591998. They constituted 97% of all children with CP born
in this period in the region.
17,9
A further classication of gross motor function into the ve
levels of the Gross Motor Function Classication System
(GMFCS)
19
was applied to the 167 children born in 19911998
and previously described.
10
Children in the relevant age band
(612 years) can walk unaided at GMFCS levels III and walk
with aids at level III, while children at levels IVV are
dependent on wheeled mobility. Twenty-three children
(14%) were originally diagnosed as spastic tetraplegia and
144 as spastic or atactic diplegia.
The Gross Motor Function Measure (GMFM)
20
is a test of ve
dimensions of gross motor function: (A) lying and rolling, (B)
sitting, (C) crawling and kneeling, (D) standing and (E)
walking, running and jumping. A total score is obtained by
calculating the mean percentage of the points obtained for
each dimension. GMFM data were obtained from 100 of the
167 children.
Muscle tone was assessed using the modied Ashworth
score (05) according to Peacock-Staudt,
21
where 1 is normal
muscle tone. The muscle groups assessed were left and right
adductors, quadriceps, hamstrings and plantar exors. The
Ashworth score for the knee extensors was used for calcula-
tions, as it has been shown to correlate with measurements of
function, including the GMFM.
22
Muscle tone was assessed in
76 of the 167 children.
Swedish growth charts for weight and height were
used.
23,24
Body weight was available in 124 children and
height in 106 of these. Body mass index (BMI) was calculated
in these 106 children.
25
2.1. Procedure
Data were derived from the CP register of western Sweden.
7,9
Exceptions were growth data (body weight and height), GMFM
and muscle tone, which were collected from local and
regional rehabilitation records. GMFCS levels were re-evalu-
ated in all children, 26 years after the initial classication.
For muscle tone, only assessments performed between the
ages of four and 12 years by one of the authors (KH) were
included.
2.2. Statistics
The w
2
test and w
2
test for trend in proportion were used for
comparisons of proportions. A paired t-test was used for
comparisons of paired continuous data. Spearmans correla-
tion coefcient was used for correlations. The level of
signicance was set at po0:05.
2.3. Ethics
The study was approved by the Ethics Committee at the
Medical Faculty at the University of Go teborg. Informed
consent was obtained from the parents of the children born
in 19911998.
3. Results
3.1. Birth years 19591998
The changing trend in the prevalence of bilateral spastic CP
over the 40-year period 19591998 for children born at term
and preterm, respectively, is shown in Fig. 1. After a
signicant decrease in the 1960s (po0:01), the prevalence of
bilateral spastic CP in the birth year period 19671970 was 0.52
per 1000 live born and it rose to 1.27 in 19831986 (po0:01),
followed by another decrease to 0.69 per 1000 live born
(po0:01) in the latest 4-year cohort of children born in
19951998. The prevalence changes were signicant for both
the preterm and the full-term group. A contemporary steep
decrease in perinatal mortality took place (Fig. 2). The two
preterm groups, children born moderately preterm, i.e. 3236
weeks of gestation, and very preterm, i.e. before 32 weeks,
followed a similar pattern, but with a shift in time. The
moderately preterm group had its peak in the birth-year
period 19791982, while the very preterm group had its peak
later, in the birth-year period 19911994. The prevalence of
the term group decreased over the period (po0:01) after a
temporary increase in 19831990.
The percentage of children born at term decreased during
the period (po0:05) and, after 1975, more children with
bilateral spastic CP were born preterm than at full term. In
the preterm group, the percentage of children born before 32
weeks of gestation rose from 14 in 36 (39%) in children born in
19751978 to 29 in 41 (72%) born in 19951998 (po0:001).
The live birth prevalence and distribution of the severity of
the gross motor impairment in the 763 children, 426 (56%) of
whom were born preterm, is presented in Fig. 3.
After a rise in predominantly severe bilateral spastic CP
from 1959 to 1986 (po0:001), there was a signicant decrease
(po0:01). The decrease in severity occurred in children born at
term (po0:01), with no contemporary decrease in severity in
children born preterm.
The distribution of motor impairment over time is shown in
Fig. 4a for children born preterm and in Fig. 4b for children
born at term. As can be seen, a larger percentage of the
children born at term had a severe motor impairment
compared with those born preterm, 156 of 337 (46%) and 142
of 426 (33%), respectively (po0:001). This difference persisted
throughout the whole 40-year period.
ARTICLE IN PRESS
E UR OP E AN J OUR NAL O F PAE DI AT R I C NE UR OL OG Y 11 ( 2007) 215 222 216
There was a male predominance in the preterm group, with
254 boys (59%) and 172 girls (po0:01), as well as in the term
group, with 186 boys (56%) and 151 girls. There was no
signicant difference between boys and girls in the distribution
of the severity of the motor impairment, but in both groups
there were larger percentages with severe motor impairments
among those born at term (boys; po0:05, girls; po0:001).
3.2. Birth years 19911998
3.2.1. Gross motor function
In the re-evaluation, the GMFCS level of the 167 children born
in 19911998 was modied in four cases, three of which had
changed from levels III to II and one from III to IV. Twenty-four
children (14%) performed at GMFCS level I, 57 (34%) at level II,
ARTICLE IN PRESS
0
0.2
0.4
0.6
0.8
1
1.2
1.4
59-62 63-66 67-70 71-74 75-78 79-82 83-86 87-90 91-94 95-98
Term
32-36 w
< 32 w
Total
Birth year
P
r
e
v
a
l
e
n
c
e

p
e
r

1
0
0
0

l
i
v
e

b
i
r
t
h
s

Fig. 1 Crude prevalence of bilateral spastic CP in children born in 19591998. Of children with bilateral spastic CP, 337
children were born at term and 426 preterm, whereof 248 before 32 weeks of gestation.
0.1
1
10
100
59-62 63-66 67-70 71-74 75-78 79-82 83-86 87-90 91-94 95-98
Birth year
P
e
r

1

0
0
0

b
i
r
t
h
s

(
P
N
M
)

/

l
i
v
e

b
i
r
t
h
s

(
C
P
)
PNM
CP
BSCP
Fig. 2 Perinatal mortality per 1000 born, crude prevalence of CP and bilateral spastic CP per 1000 live births in 19591998 in
western Sweden.
EUROPEAN J OURNAL OF PAEDI ATRI C NEUROLOGY 11 ( 2007) 215 222 217
17 (10%) at level III, 41 (25%) at level IVand 28 (17%) at level V.
Sixty-nine of 98 (70%) ambulatory children and 40 of 69 (58%)
non-ambulatory children were born preterm. The distribution
of GMFCS levels in the sub-groups of children in which body
weight and height, GMFM and muscle tone data were
analyzed did not differ from that in the whole group.
The mean GMFM score at a mean age of 6.5 years (range
412) for the ve dimensions and for the total score by GMFCS
level in 100 children (60%) is shown in Fig. 5. There was a
correlation between the GMFCS level and the total GMFM
score, as well as between GMFCS and the ve separate GMFM
dimensions, Spearmans r 1.0 (po0:01).
3.2.2. Spasticity
Spasticity, expressed as Ashworth scores, in eight selected
muscle groups in the lower extremities is shown in Fig. 6. The
median Ashworth score in children performing at GMFCS
level I was 1, in children with assisted walking 2 and in non-
walkers the median score was 3. The Ashworth scores
correlated with the severity of the motor impairment
(po0:01) and the median Ashworth score for the knee
extensors correlated with the GMFCS levels, Spearmans r
0.949, p 0:014, and thereby with walking ability.
3.2.3. Growth
Information on body weight was available in 124 (74%) of the
167 children, representing 67% of the children at GMFCS level
I, 72% at level II, 76% at level III, 76% at level IVand 82% of the
children at level V. The weight deviation at follow-up
correlated to the GMFCS level, Spearmans r 0.975,
po0:001. The more severe the motor impairment, the larger
the percentage of children who weighed less than 2 SD,
po0:02. No such correlation was found between birth weight
and GMFCS level. The mean weight deviation at follow-up at a
mean age of 7.1 years (range 412 years) compared with birth
weight deviation in 120 children by the different GMFCS levels
is shown in Fig. 7. There was a signicant difference between
mean weight deviation at birth and at the time of follow-up.
This was true for children born both preterm and at full term,
po0:01 and 0:01, respectively.
There was a signicant correlation between the mean
deviation in height at follow-up and the severity of the motor
impairment (GMFCS level), Spearmans r 0.9, po0:05, and a
larger percentage of children with a body height of o2SD
was found among those with a severe motor impairment
(GMFCS IVV), po0:05. In these 106 children, BMI was
calculated. No correlation was found between the severity
of the motor impairment and BMI. Fifteen children had a BMI
of less than 2 SD, while six had a BMI over 2 SD. Another 16
children had a body weight and height below2 SD producing
a BMI within 2 SD from the mean.
4. Discussion
Changes over time within the CP population are plausible,
with more preterm and more fragile children surviving. At the
same time, the severity of impairment may be reduced with
more advanced care. This was clearly illustrated in the
ARTICLE IN PRESS
0
0.2
0.4
0.6
0.8
1
1.2
1.4
59-62 63-66 67-70 71-74 75-78 79-82 83-86 87-90 91-94 95-98
Birth year
P
r
e
v
a
l
e
n
c
e

p
e
r

1

0
0
0

l
i
v
e

b
i
r
t
h
s
Mild
Moderate
Severe
Total
Fig. 3 Prevalence per 1000 live births by the severity of the motor impairment in 763 children with bilateral spastic CP born
in 19591998.
E UR OP E AN J OUR NAL O F PAE DI AT R I C NE UR OL OG Y 11 ( 2007) 215 222 218
present study, where the marked decrease in perinatal
mortality coincided with an initial rise in the prevalence of
bilateral spastic CP, predominantly in children born preterm,
followed by a decrease. Children born at 3236 weeks of
gestation were the rst to follow this pattern, followed by
those born before 32 weeks.
In this study, we found a reduction in the percentage of
children born at term in the bilateral spastic group. Although
the motor impairment was more severe than in children born
preterm, the severity decreased over the last 15-year period.
This was in accordance with the ndings reported by Blair et
al. in Western Australia,
26
who also found more severe
impairments in children born at term and decreasing
disability scores over time. A previous collaborative survey
from south-west Germany and western Sweden revealed
comparable prevalence gures for bilateral spastic CP in the
two countries.
11
Spasticity is a characteristic in the majority of children with
CP. It is generally postulated that spasticity is related to the
severity of the motor impairment
27
and various treatments,
ARTICLE IN PRESS
0%
20%
40%
60%
80%
100%
59-62 63-66 67-70 71-74 75-78 79-82 83-86 87-90 91-94 95-98
Mild
Moderate
Severe
Mild
Moderate
Severe
Birth year
0%
20%
40%
60%
80%
100%
59-62 63-66 67-70 71-74 75-78 79-82 83-86 87-90 91-94 95-98
Birth year
a
b
Fig. 4 (a) Distribution of the severity of the gross motor impairment in 426 children with bilateral spastic CP born preterm in
19591998. (b) Distribution of the severity of the gross motor impairment in 337 children with bilateral spastic CP born at term
in 19591998.
EUROPEAN J OURNAL OF PAEDI ATRI C NEUROLOGY 11 ( 2007) 215 222 219
such as selective dorsal rhizotomy,
28
intrathecal baclofen
29
and botulinum toxin
30
have been designed in order to
improve function and/or quality of life. However, the methods
for measuring spasticity that are available to most clinicians,
such as the Ashworth scale, are less accurate than instru-
mented measures, with inconsistencies especially in the mid-
range values.
22
The nding in this study of a correlation
between the degree of spasticity and the gross motor
function, expressed as GMFCS level, supports the hypothesis
that spasticity contributes to the motor impairment, but
motor function may also be impaired by weakness, lack of
selective motor control, balance problems, perception dif-
culties and contractures. Strength, in particular, has been
shown to correlate well with motor function in walkers with
spastic diplegia
31
and to be possible to improve by training.
32
The classication of motor function by means of the GMFCS
has improved the opportunity to describe gross motor
function in a simple, comprehensive and uniform way in
children with CP within and between countries, as in the
European collaboration SCPE.
13,34
In this study, the GMFCS
classication remained stable over time, as Palisano recently
reported.
33
A change in GMFCS level afliation was made in
only four children (2%), originally performing at level III, three
for the better, while one had deteriorated. The GMFCS can
serve as a framework for comparisons of measures of
spasticity, the rate and number of accompanying impair-
ments and GMFMs, one of which is the GMFM, for example.
The GMFM is a valid measure with good inter- and intra-rater
reliability
35
that has gained widespread use since its intro-
duction in 1993.
20
One limitation is the fact that the
maximum achievement is that of a healthy 5-year old, which
creates a ceiling effect in the results of the most able children.
ARTICLE IN PRESS
0
20
40
60
80
100
I
II
III
IV
V
G
M
F
M

%
T E D C B A
GMFCS
Fig. 5 Gross motor function measure (GMFM) by gross motor function classication system (GMFCS) levels in 100 children
with bilateral spastic CP. A lying and rolling, B sitting, C crawling and kneeling, D standing, E walking, running
and jumping, T total score.
5.00
10.00
15.00
20.00
25.00
30.00
I
n=8
II
n=30
III
n=6
IV
n=22
V
n=10
GMFCS
S
u
m

o
f

A
s
h
w
o
r
t
h

s
c
o
r
e
s
Fig. 6 Sums of Ashworth spasticity scores from eight
muscle groups (adductors, hamstrings, quadriceps and
plantar exors) in both legs by gross motor function
classication system (GMFCS) level in 76 children. Medians
with boxes denoting the 2575th percentile, whiskers
extend from the largest to the smallest value. Maximum
score 85 40.
-2
-1.5
-1
-0.5
0
0.5
Birth weight deviation Weight deviation at follow-up
GMFCS
S
D

s
c
o
r
e
I
II
III
IV
V
Fig. 7 Weight deviation (SD) at birth and at follow-up at a
mean age of 7.1 years in 120 children with bilateral spastic
CP.
E UR OP E AN J OUR NAL O F PAE DI AT R I C NE UR OL OG Y 11 ( 2007) 215 222 220
In this study, as in that by Abel,
36
performance in the ve
dimensions and the total score on the GMFM correlated with
the level of GMFCS.
A correlation was also found between GMFCS levels and the
deviation in body weight at the time of follow-up, but not
with weight at birth, indicating that low body weight was an
acquired problem. In this study, 28% of the children with
bilateral spastic CP weighed less than 2 SD and 31% had a
height of less than 2 SD. This percentage is comparable with
the situation in developing countries such as Ethiopia and
India, where more than 30% of children weigh less than
2SD.
37
A corresponding pattern was not found for BMI and
this could be explained by the fact that low weight and short
stature in combination, a frequent nding in malnutrition,
can produce a BMI that is within normal limits for age. This
was the case in 15%. Another 15% had a low BMI due to low
body weight. Measuring growth in children with CP is a
challenge. Skin-fold measures are recommended by some
18
but considered by others to overestimate the nutritional
status, due to the muscle wasting in this group. Muscle
wasting takes place especially in the legs, representing 25% of
the body weight, and low weight in non-ambulant children
with spastic quadriplegia has been explained by atrophy of
the leg muscles because of non-use.
38
Malnutrition due to
feeding problems and sometimes increased energy demands
is an important factor for underweight in children with CP
and, as shown in this survey, bilateral CP is no exception. The
consequences for motor performance and other abilities,
39
such as cognitive function, need to be considered.
40,41
We conclude that the live birth prevalence of bilateral spastic
CP has decreased since the mid-1980s, parallel to a decrease in
the severity of the motor impairment. Since the mid-1970s,
bilateral spastic CP has been dominated by children born
preterm, while, in the 1990s, 70% of those performing at GMFCS
levels IIII were born preterm. The severity of the motor
impairment, which correlated with the degree of spasticity, has
decreased during the last 15 years. The percentage of children
with underweight and stunting is substantial, especially in
those with a severe motor impairment.
Acknowledgements
This investigation was supported by grants from the Folke
Bernadotte, the Linnea and Josef Carlsson, the Petter Silfvers-
kio ld, the Gunvor and Josef Aner, the Sven Jerring and the
Ha ggqvist Family Foundations and the Va stra Go taland
Region. We are indebted to the Medical Birth Registry Ofce
at the Swedish National Board of Health and Welfare for
information on vital statistics.
R E F E R E N C E S
1. Hagberg B, Hagberg G, Olow I. The changing panorama of
cerebral palsy in Sweden 19541970. I. Analysis of the general
changes. Acta Paediatr Scand 1975;64:18792.
2. Hagberg B, Hagberg G, Olow I. The changing panorama of
cerebral palsy in Sweden 19541970. II. Analysis of the various
syndromes. Acta Paediatr Scand 1975;64:193200.
3. Hagberg B, Hagberg G, Olow I. IV. The changing panorama of
cerebral palsy in Sweden. IV. Epidemiological trends 195978.
Acta Paediatr Scand 1984;73:43340.
4. Hagberg B, Hagberg G, Olow I, von Wendt L. The changing
panorama of cerebral palsy in Sweden. V. The birth year
period 19791982. Acta Paediatr Scand 1989;78:28390.
5. Hagberg B, Hagberg G, Olow I. The changing panorama of
cerebral palsy in Sweden. VI. Prevalence and origin during the
birth year period 19831986. Acta Paediatr 1993;82:38793.
6. Hagberg B, Hagberg G, Olow I, von Wendt L. The changing
panorama of cerebral palsy in Sweden. VII. Prevalence and
origin in the birth year period 198790. Acta Paediatr
1996;85:95460.
7. Hagberg B, Hagberg G, Beckung E, Uvebrant P. The changing
panorama of cerebral palsy in Sweden. VIII. Prevalence and
origin in the birth year period 19911994. Acta Paediatr
2001;90:2717.
8. Beckung E, Hagberg G. Neuroimpairments, activity limitations
and participation restrictions in children with cerebral palsy.
Dev Med Child Neurol 2002;44:30916.
9. Himmelmann K, Hagberg G, Beckung E, Hagberg B, Uvebrant P.
The changing panorama of cerebral palsy in Sweden IX.
Prevalence and origin in the birth-year period 19951998. Acta
Paediatr 2005;94:28794.
10. Himmelmann K, Beckung E, Hagberg G, Uvebrant P. Gross and
ne motor function and accompanying impairments in
cerebral palsy. Dev Med Child Neurol 2006;48:41723.
11. Kra geloh-Mann I, Hagberg G, Meisner C, et al. Bilateral spastic
CPa comparative study between south-west Germany and
western Sweden. I. Clinical patterns and disabilities. Dev Med
Child Neurol 1993;35:103747.
12. Kra geloh-Mann I, Hagberg G, Meisner C, et al. Bilateral spastic
cerebral palsya comparative study between south-west
Germany and western Sweden. II. Epidemiology. Dev Med Child
Neurol 1994;36:47383.
13. Surveillance of Cerebral Palsy in Europe (SCPE). Prevalence
and characteristics of children with cerebral palsy in Europe.
Dev Med Child Neurol 2002;44:63340.
14. Bax M, Goldstein M, Rosenbaum P, et al. Proposed denition
and classication of cerebral palsy. Dev Med Child Neurol
2005;47:5716.
15. Colver AF, Sethumadhavan T. The term diplegia should be
abandoned. Arch Dis Child 2003;88:28690.
16. Baxter P. ICF: health vs. disease. Dev Med Child Neurol
2004;46:29 [Editorial].
17. Jarvis S, Glinianaia SV, Torrioli MG, et al. Cerebral Palsy and
intrauterine growth in single births: European Collaborative
Study. Lancet 2003;362:110611.
18. Samson-Fang LJ, Stevenson RD. Identication of malnutrition
in children with cerebral palsy: poor performance of weight-
for-height centiles. Dev Med Child Neurol 2000;42:1628.
19. Rosenbaum PL, Walter SD, Hanna SE, et al. Prognosis for gross
motor function in cerebral palsy: creation of motor develop-
ment curves. J Am Med Assoc 2002;288:135763.
20. Russell DJ, Rosenbaum PL, Cadman DT, et al. The gross motor
function measure: a means to evaluate the effects of physical
therapy. Dev Med Child Neurol 1989;31:34152.
21. Peacock WJ, Staudt LA. Functional outcomes following
selective posterior rhizotomy in children with cerebral palsy.
J Neurosurg 1991;74:3805.
22. Damiano DL, Quinlivan JM, Payne P, Nelson KC, Abel MF. What
does the Ashworth scale really measure and are instrumen-
ted measures more valid and precise? Dev Med Child Neurol
2002;44:1128.
23. Niklasson A, Ericson A, Fryer JG, et al. An update of the
Swedish reference standards for weight, length and head
circumference at birth for given gestational age (19771981).
Acta Paediatr Scand 1991;80:75662.
ARTICLE IN PRESS
EUROPEAN J OURNAL OF PAEDI ATRI C NEUROLOGY 11 ( 2007) 215 222 221
24. Albertsson-Wikland K, Karlberg J. Natural growth in children
born small for gestational age with and without catch-up
growth. Acta Paediatr (Suppl) 1994;399:6470.
25. Karlberg J, Lou ZH, Albertsson-Wikland K. Body mass index
reference values (mean and SD) for Swedish children. Acta
Paediatr 2001;90:142734.
26. Blair E, Watson L. Epidemiology of cerebral palsy. Semin Fetal
Neonatal Med 2006;11:11725.
27. Scholtes VAB, Becher JG, Beelen A, Lankhorst GJ. Clinical
assessment of spasticity in children with cerebral palsy: a
critical review of available instruments. Dev Med Child Neurol
2006;48:6473.
28. Peacock WJ, Arens LJ. Selective posterior rhizotomy for the
relief of spasticity in cerebral palsy. S Afr Med J 1982;62:11924.
29. Albright AL. Intrathecal baklofen for spasticity in cerebral
palsy. J Am Med Assoc 1991;265:141822.
30. Cosgrove AP, Corry IS, Graham HK. Botulinum toxin in the
management of the lower limb in cerebral palsy. Dev Med Child
Neurol 1994;36:38696.
31. Ross SA, Engsberg JR. Relation between spasticity and
strength in individuals with spastic diplegic cerebral palsy.
Dev Med Child Neurol 2002;44:14857.
32. Damiano DL, Dodd K, Taylor NF. Should we be testing and
training muscle strength in cerebral palsy? Dev Med Child
Neurol 2002;44:6872.
33. Palisano RJ, Cameron D, Rosenbaum PL, Walter SD, Russell D.
Stability of the gross motor function classication system.
Dev Med Child Neurol 2006;48:4248.
34. Surveillance of Cerebral Palsy in Europe (SCPE). A collabora-
tion of cerebral palsy registers. Dev Med Child Neurol
2000;42:81624.
35. Nordmark E, Ha gglund G, Lagergren J. Cerebral palsy in
southern Sweden II. Gross motor function and disabilities.
Acta Paediatr 2001;90:127782.
36. Abel MF, Damiano DL, Blanco JS, et al. Relationships
among musculoskeletal impairments and functional health
status in ambulatory cerebral palsy. J Pediatr Orthop 2003;23:
53541.
37. de Onis M, Blo ssner M, Borghi E, Frongillo EA, Morris R.
Estimates of global prevalence of childhood underweight in
1990 and 2015. J Am Med Assoc 2004;291(21):26006.
38. Kong CK, Wong HS. Weight-for-height values and limb
anthropometric composition of tube-fed children with quad-
riplegic cerebral palsy. Pediatrics 2005;116:83945.
39. Samson-Fang L, Fung E, Stallings VA, et al. Relationship
nutritional status to health and societal participation in
children with cerebral palsy. J Pediatr 2002;141:63743.
40. Walker SP, Grantham-McGregor SM, Powell CA, Chang SM.
Effects on growth restriction in early childhood on growth, IQ
and cognition at age 11 to 12 years and the benets of
nutritional supplementation and psychosocial stimulation. J
Pediatr 2000;137:3641.
41. Upadhyay SK, Agarwal DK, Agarwal KN. Inuence of mal-
nutrition on intellectual development. Indian J Med Res
1989;90:43041.
ARTICLE IN PRESS
E UR OP E AN J OUR NAL O F PAE DI AT R I C NE UR OL OG Y 11 ( 2007) 215 222 222

You might also like