JOURNAL OF TROPICAL PEDIATRICS, VOL. 59, NO. 6, 2013
Changes in the Clinical Spectrum of Cerebral Palsy over Two
Decades in North India—An Analysis of 1212 Cases
by Pratibha Singhi and Arushi Gahlot Saini
Department of Pediatrics, Postgraduate Institute of Medical Education and Research, Chandigarh-160012, India
Correspondence: Prof. Pratibha Singhi, Chief Pediatric Neurology and Neurodevelopment, Advanced Pediatrics Centre,
PGIMER, Chandigarh-160012, India. Tel: þ91-172-2755304/2746699, Fax: þ91-172-2744401/2745078,
E-mail <[email protected]>.
Summary
Background: Clinical spectrum of cerebral palsy (CP) is different in developing and developed countries.
We evaluated the clinical profile, etiological factors and co-morbidities of children with CP in North
India, and compared with our previous study.
Methods: 1212 children with CP registered in last 10 years in our rehabilitation center were compared
with our previous study of 1000 children from same center.
Results: Spastic quadriplegia is the commonest type of CP (51.5%) although lesser than previous
decade (61%). Birth asphyxia remains the main (51.98%) etiological factor as earlier (45.3%). CP
due to CNS infections decreased from 63.5% to 57.4%, due to bilirubin-encephalopathy remained same
(30%). Speech problems (83.7%), microcephaly (64.27%), seizures (44.5%) and intellectual disability (38.61%) are common co-morbidities. Common neuroimaging findings include hypoxic-ischemic
changes and periventricular leucomalacia.
Conclusion: The spectrum of CP is evolving in the developing countries with an increase in diplegic and a
decrease in quadriplegic CP.
Key words: cerebral palsy, quadriplegia, asphyxia, intellectual disability, seizures
Introduction
Cerebral palsy (CP) is the commonest physical disability in childhood, occurring in 2–2.5/1000 births
[1]. Originally reported by Little in 1861 as ‘cerebral
paresis’, the term encompasses ‘a group of disorders
of development of movement and posture, causing
activity limitation, that are attributed to non-progressive disturbances that occurred in the developing
fetal or infant brain. The motor disorders of CP are
often accompanied by disturbances of sensation,
cognition, communication, perception, behavior or
seizure disorders’ [2]. Although the brain injury in
CP is non-progressive, the co-morbidities and the
functional limitations change over time, affecting
Acknowledgements
P.S.: clinician-in-charge, plan of study, neurological
assessment, reviews of electrophysiology data and
neuroimaging, and review of manuscript and literature. A.G.S.: collection of data, neurological assessment, draft of manuscript and literature review
the functioning and quality of life. Therefore, an
understanding of the various types and the co-existent impairments of CP is imperative to physicians to
assess the magnitude of problem, involve multidisciplinary care, introduce preventive measures, predict
functional limitations and communicating the
impact to the parents.
Additionally, the clinical spectrum of CP in
resource-poor, developing countries is different
from that in the developed countries. The trend of
increasing survival of preterm babies and advances in
maternal and neonatal care in the developed world is
not yet evident in most developing countries [3].
There is a paucity of clinical data in resource-poor
settings, despite the fact that perinatal (e.g. asphyxia,
sepsis) and postnatal causes such as meningitis, head
trauma and hyperbilirubinemia contribute a large
proportion of disease, a scenario very different
from the developed countries where CP is more
often related to prematurity and survival. Most reports of CP in resource-poor settings are either hospital or clinic based or include lesser number or
narrower age-range of patients [4–8]. The other two
ß The Author [2013]. Published by Oxford University Press. All rights reserved. For Permissions, please email: [email protected]
doi:10.1093/tropej/fmt035
Advance Access published on 19 June 2013
434
P. SINGHI AND A. G. SAINI
large studies were from Nigeria and our previous
study from North India [3, 9]. This variation between
low- and high-income countries might reflect the
differences in etiology as well as in the populations
identified. Hence, this study was aimed to evaluate
the clinical profile, types and etiologies of CP, associated risk factors in Northern India as well as to
ascertain the changes in the spectrum of CP in the
last decade as compared to our previous experience
from the same center [3]. Our study presents the comparative data of the largest number of patients from a
single center identified through intensive neuro-pediatric follow-up and gives a perspective on CP in developing countries with emphasis on the burden of
preventable causes and need for improved perinatal
care. Such studies help in determining which services
in resource-poor settings would contribute to improving the livelihoods of children with CP and
their families.
Methods
The study included 1212 consecutive children with
CP seen at The Rehabilitation Center for Disabled
Children, Chandigarh from 2000–09. The center provides free of cost, comprehensive evaluation and
intervention services to children with various types
of disabilities brought from all over North India
after referral from hospitals and practicing doctors,
or directly from the community by parents.
A detailed history including socio-demographic,
family structure and birth details was elicited
using a pre-structured proforma, followed by a complete physical, developmental and neurological
examination. Assessment of intelligence/development
quotient (IQ/DQ), ENT and ophthalmological evaluation were performed in all children. Informed consent was obtained from the care-givers and assent from
the patients wherever applicable.
CP was defined as a non-progressive disorder that
manifests as motor and postural abnormality, and
results from CNS insult sustained during the early
period of brain development, usually defined as the
first 3 or 5 years of life [10]. CP was classified using
Swedish classification: spastic (quadriplegia, diplegia,
hemiplegia), ataxic and dyskinetic (including athetoid, dystonic), hypotonic and mixed [11]. The etiological classification was: (i) congenital CP (prenatal
and perinatal causes); (ii) acquired CP due to identifiable factors acquired after birth in a child born normally (such as CNS infection, neonatal jaundice,
head injury, hypoglycemia, intracranial hemorrhage);
(iii) mixed—wherein both congenital and postnatal
factors played a role. For birth asphyxia, Apgar
scores when available, or the following criteria were
used: (i) history of delayed cry >5 min after birth; (ii)
baby turning blue and requiring oxygen therapy, with
difficulty in respiration, lethargy and/or seizures
within 72 h of birth.
Journal of Tropical Pediatrics
Vol. 59, No. 6
Clinical psychologists conducted psychometric
tests and children were classified into mild
(IQ ¼ 50–70), moderate (IQ ¼ 30–50) and severe
(IQ ¼ <30) intellectual disability (ID). Children
with definite history of >1 recurrent seizures were
considered to have epilepsy. Behavioral problems
were considered significant if they were severe
enough to be perceived as problems by parents, or
interfered with therapy, or education of the child.
Hearing defects were objectively identified by brainstem evoked response (BSERA) or formal
audiometry. Microcephaly was defined as head
circumference <2 SD of normal for age and sex.
Protein-energy malnutrition (PEM) was graded according to criteria proposed by the Indian Academy
of Pediatrics (expressing weight of the child as percentage of the expected weight): normal (>80%);
grade I (71%–80%); grade II (61%–70%); grade III
(50%–60%), and grade IV (<50% of expected weight
for age) [12]. Socio-economic status was ascertained
using the modified Kuppuswamy’s socio-economic
status scale [13]. All children were evaluated by a
pediatric neurologist (PS), and a team of therapists,
and provided appropriate rehabilitation with periodic follow-up. Electroencephalography (EEG) and
magnetic-resonance imaging (MRI) were done when
relevant, and findings corroborated with the clinical
findings.
Statistical analysis
Data were entered and descriptive statistics were calculated using SPSS 160 software package.
Continuous data with normal distribution are presented as the mean and SD, whereas data with
other distributions are presented as the median and
range (minimum–maximum). Inferential statistics
were used for purposes of comparing findings from
the previous study and the present study in order to
determine if differences in findings were statistically
significant. The level of significance was p ¼ 0.005.
Results
Socio-demographic characteristics
From January 2000 to December 2009, 1212 children
with CP were seen. There was a male preponderance
(72.4%); majority of children were in the age group
1–2 years (38.9%) at the time of their first visit,
12.9% were <1 year, 33.2% between 2 and 5 years,
9.7% between 5 and 8 years and 5.4% were >8 years.
Age of onset of problems noted by the parents
ranged from birth to 8 years (mean 4.98 6.92
months). Mean delay in presentation to a rehabilitation center was 2.60 2.43 years. Most (68.9%) children were from lower socio-economic status. More
than half (56.9%) of the children were firstborns,
28.4% second, 11.1% third and 3.6% were 4 in
birth order. The presenting problems were
435
P. SINGHI AND A. G. SAINI
developmental delay (88%), seizures (34.7%), other
problems predominantly associated with gait and
posture (22.8%), speech delay (9.5%), and behavior
problems (5.9%). A contributory family history such
as ID, convulsions or CP was found in 8.6% of cases.
Types of CP
Types of CP seen were: spastic 73% (885/1212), dyskinetic/athetoid 7% (85/1212), hypotonic/ataxic
11.2% (135/1212) and mixed 8.8% (107/1212). Out
of spastic CP, quadriplegic was 51.5% (456/885),
diplegic 34.5% (306/885) and hemiplegic 13.8%
(123/884). The distribution of these types and comparison with our previous study has been shown in
Fig. 1. As compared to our previous study, though
spastic CP remains the commonest type of CP
(70%–73%, p-value 0.11); diplegia has increased
(22%–34.5%, p-value 0.0001) and quadriplegia has
decreased (61%–51.5% p-value 0.0001) significantly.
The change in hemiplegic CP (17%–13.8%, p-value
0.03) and dyskinetic CP (8.4%–7%, p-value 0.22) has
not been very significant. The contribution of hypotonic and mixed CP has also changed significantly
(7.7%–11.2%, p-value 0.006 and 13.9%–8.8%,
p-value 0.0002, respectively).
Perinatal problems
Antenatal problems (Fig. 2) were reported in 30.4%
of the mothers. 81% were institutional deliveries,
75.6% were term and 24.4% preterm (range 26–37
weeks), and prolonged duration of labor was reported in 13.6% of the cases. Most (75.9%) were
vaginal deliveries, 20.5% were caesarean-section,
0.1% was breech, and 3.5% required instrumentation. Delayed cry was reported in half (51.2%) of
the cases: 23.2% required physical stimulation
alone, 25.4% also required oxygen. The predisposing
neonatal factors are shown in Table 1.
Etiology of CP
Majority of the cases were congenital (59.8%); 22.4%
had both congenital and postnatal causes. Of the
17.8% cases of acquired CP, 57.4% were due to
CNS infections such as meningitis and encephalitis,
30% bilirubin-encephalopathy (usually secondary to
Rh-incompatibility or G6PD deficiency), 7.4% late
hemorrhagic disease of newborn or intracranial
bleeds, and the rest were secondary to hypoglycemia
and head injury. The various causes and their relationship to the type of CP are shown in Table 2. As
compared to our previous study, the contribution of
prematurity (13.2%–24.3%, p-value 0.0001), low
birth weight (20.4%–37.87%, p-value 0.0001), neonatal jaundice (21.6%–35.14%, p-value 0.0001) and
birth asphyxia (45.3%–51.98%, p-value 0.001) has
increased significantly.
FIG. 2. Antenatal problems reported in the mothers
of children with CP.
FIG. 1. Distribution of CP cases in the present and previous study.
436
Journal of Tropical Pediatrics
Vol. 59, No. 6
P. SINGHI AND A. G. SAINI
Co-morbidities
The co-morbidities are shown in Table 3, and their
association with the type of CP is shown in Table 4.
Most children (64.3%) had a head circumference <2
SD of normal. Formal IQ assessment was done in
54.5%; 28.9% had mild, 22.6% had moderate and
19.4% had severe ID. About half of cases (43%)
were malnourished: PEM grade I 44.6%, grade II
33.7%, grade III 15.7% and grade IV 5.9% cases.
The types of seizures are depicted in Fig. 3. EEG
was done in 81% cases with seizures: generalized epileptiform discharges 37%, focal epileptiform activity
20.2%, hypsarrhythmia 7.2%, diffuse slowing 4%
and normal 25%. These abnormalities were most
commonly seen in children with quadriplegic followed by diplegic CP. Visual problems were seen in
46.7% of children. Of these, 60% had strabismus,
12% refractory errors, 11.1% optic atrophy, 6.7%
nystagmus and 2.2% cataracts.
Neuroimaging
On neuroimaging, 87.88% (791/900) of children had
abnormalities: hypoxic-ischemic changes (35.7%),
periventricular leucomalacia (PVL) (13.4%), brain
malformations (7.4%), non-specific cerebral atrophy
(12.8%) and basal ganglia changes (5.8%). Other
findings (11.5%) included delayed myelination, intracranial bleeds and hypoglycemic injury. Gray matter
injury and cerebral atrophy was significantly
Birth asphyxia
Low birth weight
Neonatal jaundice
Neonatal sepsis
Neonatal seizures
Prematurity
Twin-gestation
630
459
426
371
326
294
41
Discussion
Our rehabilitation center has a large catchment area
that includes most of the Northern India and provides services to both referred cases as well as children from the community. Spastic quadriplegia has
been the commonest type of CP in developing countries (rates between 36% and 71%) whereas spastic
diplegia (5%–47%) is commoner in the developed
world [3–8, 14, 15]. It is likely that the higher rates
of diplegia in high-income settings partly reflect
better neonatal services and higher rates of premature survivors, whereas higher rates of spastic quadriplegia in low-income settings reflect increased
perinatal and postnatal causality (e.g. asphyxia, meningitis) [1]. As compared to our previous study,
though spastic CP remains the commonest type of
CP; the proportion of diplegia has increased (22%–
34.5%) whereas that of quadriplegia has decreased
(61%–51.5%) over the last decade [3]. Mixed type
(where children may have both spasticity and athetoid features) of CP forms an important group
though its proportion has declined over the decade
(13.9%–8.8%).
TABLE 3
Associated problems in children with CP
TABLE 1
Neonatal factors predisposing to CP
CP cases (n ¼ 1212)
associated with spastic quadriplegia, PVL with spastic diplegia and basal ganglia changes were predominantly seen with dystonic CP.
Problems
%
51.98
37.87
35.14
30.6
26.9
24.3
3.4
n ¼ 1212
Speech problems
Microcephaly
Visual defect
Seizures
Malnutrition
Intellectual disability
Feeding problems
Hearing problems
Behavior problems
%
1015
779
567
539
522
468
228
169
169
83.7
64.27
46.7
44.4
43.06
38.61
18.8
13.9
13.9
TABLE 2
The causes of CP and their relation to the types of CP
Congenital
Spastic QP
Spastic DP
Spastic HP
Dystonic
Hypotonic
Mixed
NNJ
n (%)
CNS
infection
n (%)
n (%)
Head
injury
n (%)
274
198
77
19
110
47
67
23
19
2
6
7
1
4
1
51
2
6
4
0
1
0
0
1
(7.8)
(27.3)
(10.6)
(2.6)
(15.2)
(6.5)
Journal of Tropical Pediatrics
(54)
(18.5)
(15.3)
(1.6)
(4.8)
(5.6)
(1.5)
(6.2)
(1.5)
(78.5)
(3.1)
(9.2)
Vol. 59, No. 6
(66.7)
(0)
(16.7)
(0)
(0)
(16.7)
Hypoglycemia
LHDN/bleed
n (%)
n (%)
2
1
1
0
0
1
(40)
(20)
(20)
(0)
(0)
(20)
5
2
8
1
0
0
(31.2)
(12.5)
(50)
(6.2)
(0)
(0)
Congenital þ
postnatal
n (%)
103
78
16
12
17
45
(38)
(28.8)
(5.9)
(4.4)
(6.3)
(16.6)
Total
n (%)
456
306
123
85
135
107
(37.6)
(25.2)
(10.1)
(7)
(11.1)
(8.8)
437
P. SINGHI AND A. G. SAINI
There has been a rise in CP associated with prematurity (13.2%–24.3%), low birth weight (20.4%–
37.87%) and twin-gestation (1.2%–3.4%) [3].
However, unlike the western figures, majority of children in both of our studies were term babies. Role of
perinatal complications, particularly birth asphyxia
has been implicated strongly in developing countries
in 20%–46% of cases [3–4, 6, 9]. In our series, the
contribution of birth asphyxia has increased from
45.3% to 51.98% even though the majority was
term institutional deliveries. This possibly reflects
the need for better perinatal care as well as
delineating operational definitions to record birth
asphyxia in resource-poor settings. CNS infections,
neonatal septicemia, neonatal hypoglycemia,
hyperbilirubinemia and vitamin-K deficiency-associated intracranial bleeds constitute important preventable causes of acquired CP in the developing
world. An emerging cause of CP observed over the
last decade (22.36%) is a combination of both congenital and postnatal factors which cause an additive
insult to the growing brain. Extreme levels of hyperbilirubinemia have been causally linked with kernicterus causing permanent neurologic sequelae,
including ID, choreo-athetoid CP, gaze palsies and
sensorineural hearing loss, while more subtle deEcits
in motor function, attention and learning are attributable to moderate hyperbilirubinemia [16–17]. Even
though there has been an improvement in neonatal
services, hyperbilirubinemia continues to be an important cause of acquired CP over the last two decades (30%) [3].
Prevalence rates of CP have been used as outcome
measures of obstetric practice and neonatal care and
it was expected that improvement in these areas
would result in lower rates of CP [18]. Nonetheless,
predisposing antenatal factors were found in onefourth of cases in our previous and present studies
[3]. The reported contribution of pre-eclampsia has
increased from 22% to 30% whereas that of antepartum hemorrhage reduced from 31% to 12%. A large
number of mothers (18%) gave history of fever in the
first trimester but tests for intra-uterine infections
were negative in the babies. Increased use of fetal
interventions such as instrument-assisted deliveries
and caesarean-sections has also been implicated
among the risk factors [19, 20]. The contribution of
caesarean-section has almost doubled over the
decade (9.9%–20.5%).
The percentage of reported speech problems has
increased as compared to the previous decade
(9.5% vs. 7.8%) possibly because of the increased
awareness of parents. However, speech problems
were detected in a much higher proportion (83.7%)
on examination. Children with quadriplegia continue
to have the worst intellectual outcome. Epilepsy in
children with CP is a frequent problem and is often
severe and difficult to control, particularly in children
with ID [21]. Seizures were found to be most
common in children with quadriplegic CP, and least
common in ataxic and athetoid types similar to our
previous study [3]. Comparable incidence of
myoclonic seizures and infantile spasms has been
observed before [22, 23]. EEG abnormalities were
most commonly seen in children with quadriplegic
CP.
Neuroimaging, particularly MRI, not only helps to
define the etiology, pattern and severity of neuropathology in CP but also indicates the likely timing
of injury. The American Academy of Neurology now
recommends that all cases of CP of unknown origin
should undergo neuroimaging [24]. In developed
TABLE 4
Associated problems in relation to types of CP
Total Seizures Intellectual Speech Vision
n (%) n (%)
disability
n (%) n (%)
n (%)
Spastic QP 456
(37.6)
Spastic DP 306
(25.2)
Spastic HP 123
(10.1)
Dystonic
85
(7)
Hypotonic 135
(11.1)
Mixed
107
(8.8)
Total
1212
(100)
438
257
(56.35)
93
(30.39)
68
(55.28)
25
(29.41)
57
(42.22)
39
(36.44)
539
(44.47)
178
(39.03)
101
(33)
56
(45.52)
34
(40)
52
(38.51)
47
(43.92)
468
(38.61)
404
(39.8)
234
(23.1)
84
(8.3)
78
(7.7)
119
(11.7)
96
(9.5)
1015
(83.74)
253
(55.48)
152
(49.67)
38
(30.89)
26
(30.58)
53
(39.25)
45
(42.05)
567
(46.78)
Hearing Behavior Malnutrition Microcephaly Feeding
n (%)
n (%)
n (%)
n (%)
n (%)
76
(45)
17
(10.1)
5
(3)
30
(17.8)
23
(13.6)
18
(10.7)
169
(13.94)
71
(42)
37
(21.9)
13
(7.7)
16
(9.5)
23
(13.6)
9
(5.3)
169
(13.94)
216
(47.36)
117
(38.23)
32
(26.01)
39
(45.88)
56
(41.48)
62
(57.94)
522
(43.06)
350
(44.9)
175
(22.5)
52
(6.7)
46
(5.9)
80
(10.3)
76
(9.8)
779
(64.27)
Journal of Tropical Pediatrics
103
(45.2)
49
(21.5)
3
(1.3)
20
(8.8)
21
(9.2)
32
(14)
228
(18.8)
Vol. 59, No. 6
P. SINGHI AND A. G. SAINI
5.
6.
7.
8.
FIG. 3. Types of seizures in children with CP.
9.
countries, the main findings include PVL or white
matter injury (40%–60%), cortical and deep gray
matter lesions (10%–20%), and brain malformations
(10%) [25, 26]. Cerebral imaging abnormalities were
found in 87.88% of our patients similar to the
Western data [27–29]. In concordance to the predominant type of CP, HIE changes are most commonly
seen in our setup whereas PVL is the most common
neuropathology in developed world [27, 28].
Additionally, children with dyskinetic CP secondary
to neonatal hyperbilirubinemia showed basal ganglia
changes in the MRI.
Limitation
Our study was not community based; hence there is a
chance of missing mild cases of CP which did not
seek institutional care. Nevertheless, it is reasonably
reflective of the types of cases seen in Northern India
due to the large drainage area of our rehabilitation
center and the patient profile including both referred
cases as well as children from the community.
Conclusion
Term, quadriplegic CP is most common in our set up
with a trend towards increase in the diplegic and decrease in the quadriplegic CP. Preventable factors
such as birth asphyxia, CNS infections and hyperbilirubinemia remained unchanged and reflect the need
for improvement in perinatal care.
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Journal of Tropical Pediatrics
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