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A Retrospective NeurocognitiveStudy in Children With SpasticDiplegiaSilja Pirila , Jaap van der Meere , Paivi Korhonen ,Pirjo Ruusu-Niemi , Mirkka Kyntaja , PirkkoNieminen & Raija KorpelaPublished online: 08 Jun 2010.

To cite this article: Silja Pirila , Jaap van der Meere , Paivi Korhonen , PirjoRuusu-Niemi , Mirkka Kyntaja , Pirkko Nieminen & Raija Korpela (2004) ARetrospective Neurocognitive Study in Children With Spastic Diplegia, DevelopmentalNeuropsychology, 26:3, 679-690, DOI: 10.1207/s15326942dn2603_2

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A Retrospective NeurocognitiveStudy in Children

With Spastic Diplegia

Silja PirilaPaediatric Research Centre

Tampere University Hospital, TAUH, Finland

Department of Psychology

Tampere University, Finland

Jaap van der MeereDepartment of Developmental and Experimental Clinical Psychology

University of Groningen, The Netherlands

Paivi Korhonen and Pirjo Ruusu-NiemiPaediatric Research Centre

Tampere University Hospital, TAUH, Finland

Mirkka Kyntaja and Pirkko NieminenDepartment of Psychology

Tampere University, Finland

Raija KorpelaPaediatric Research Centre

Tampere University Hospital, TAUH, Finland

The study presents the results on neonatal cranial ultrasonography (US) and later in-

telligence (Wechsler Intelligence Scale–Third Edition and Wechsler Preschool and

Primary Scale of Intelligence–Revised) and Neuropsychological assessments of 15

children with spastic diplegia. The assessments were undertaken when the children

were 5 to 12 years of age. The children’s IQ scores were, as a group, at the lower end

DEVELOPMENTAL NEUROPSYCHOLOGY, 26(3), 679–690Copyright © 2004, Lawrence Erlbaum Associates, Inc.

Requests for reprints should be sent to Silja Pirila, Paediatric Research Centre, Tampere University

Hospital, TAUH, P.O. Box 2000, FIN–33521, Tampere, Finland. E-mail: silja.pirila@pshp.fi

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of the normal distribution. The neuropsychological assessment indicated that deficits

in visuomotor and visuospatial processing were characteristic of the children. No as-

sociation was found between the neonatal cranial US findings and the IQ and

neurocognitive scores. However, the cranial US findings strongly predicted func-

tional motor limitations of the children.

Cerebral palsy (CP) refers to a heterogeneous group of impairments character-

ized by a persistent disorder of movement and posture caused by

nonprogressive pathological processes in the immature brain (Albright, 1996).

Although the neuropathophysiology of CP is not yet comprehensively under-

stood, its associated physiological disturbances have been provided by the re-

search in developmental neurobiology and neuroscience. In the great majority

of cases, either hemorrhage or periventricular leukomalacia (PVL) reflecting

necrosis of the periventricular white matter are the primary causes most likely

to produce the definite brain cell damage (Filloux, 1996). Overall, CP has been

observed to occur in 1.2 to 2.5 children per 1,000 by early school age. Con-

sidering the life-long effects of the handicap, children with CP deserve our re-

search attention. Unfortunately, children with major handicapping conditions,

including CP, are excluded in longitudinal risk studies most of the time, as re-

viewed by Ornstein, Ohlsson, Edmonds, and Asztalos already in 1991. Since

then, little has changed. Whereas follow-up studies focused on CP have limited

themselves to the motor part of the disability, ignoring the cognitive develop-

ment that is considered one of the main factors determining the quality of life

the child will enjoy (Nelson, Swaiman, & Russman, 1994). At best, such stud-

ies report the IQ/DQ (intelligence or developmental quotient) index. For in-

stance, in the recent study of Nordmark, Hagglund, and Lagergren (2001), the

clinical features and gross motor functions were analyzed in a large sample of

167 children (age range 6 to 9.7 years) suffering from CP. Using the Gross Mo-

tor Function classification System (GMFCS), 85% of the children with normal

or borderline IQ were classified into Levels I or II indicating mild motor dis-

ability, and 44% of the children with mental retardation were severely motor

disabled and classified into the Levels IV and V. Consequently, the Nordmark

et al. study revealed that severe motor impairment is often, but not necessarily,

combined with associated impairments such as mental retardation.

Interesting as the finding is, one may have doubts about whether an IQ index

is enough to describe the cognitive functioning of motor handicapped children,

especially when they reach school age and beyond. By that age, it is assumed

that the more subtle long-term morbidities in areas of learning, visuomotor inte-

gration, and language performance become more detectable because these diffi-

culties usually do not manifest themselves much in infancy. Within this perspec-

tive, the study of Olsen et al. (1998) is of importance. In addition to IQ, the

researchers used a neuropsychological test (NEPSY) to investigate attention,

680 PIRILA ET AL.

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verbal abilities, perceptual-motor skills, and memory in 41 preterm children with

a mean age of 8 years. Thirteen children had PVL and out of them, 4 had devel-

oped CP (2 suffered from spastic diplegia, the other 2 suffered from spastic

hemiplegia and dystonic tetraplegia). As a group, the children performed poorly

in tasks requiring spatial and visuo-perceptual abilities that were associated with

the finding of PVL in MRI, especially with posterior ventricular enlargement.

Surprisingly, the children with CP performed as good as the clinically healthy

preterm children. However, as the authors themselves admitted, the small num-

ber of children with CP made it difficult to make any strong conclusions con-

cerning their cognitive functioning.

This study elaborated on the issue of CP and neurocognitive functioning using

the NEPSY test. Because CP is an umbrella term and heterogeneity hinders the in-

terpretation of research outcome, the study confined itself to children who had

spastic diplegia due mainly to PVL detected by neonatal cranial ultrasound. The

pathology of diplegia involves areas located along the external angle of the lateral

ventricles, thus damaging the fibers from the internal aspects of the hemisphere

that include the motor fibers to the lower limbs. Motor fibers from the mesial cor-

tex (leg area) are preferentially involved, the leukomalacic area interrupting leg fi-

bers or stretching them around the dilated ventricle. As a result, the intelligence

level is relatively intact in patients suffering from spastic diplegia (Holling &

Leviton, 1999). The location of leukomalacia along the posterior part of the lateral

ventricles, interrupting the optic radiations, is responsible for visual difficulties

and strabismus. Witelson (1987) reviewed experimental outcome focused on the

effects of prenatal damage on the cognitive and neuropsychological development.

She underlined that the development of language functions take precedence at the

expense of visuospatial functions. Because PVL lesions involve the periventricular

white matter through which the corticospinal tract descends, we expect in our sam-

ple the most pronounced cognitive deficits in the perceptual-motor domain

whereas verbal and memory functions will be relatively intact. In addition, the as-

sociation between the neonatal cranial US results and neurocognitive findings will

be examined.

With respect to the association between the neonatal cranial US findings and

later outcome, the following may be said. First, the association between the neu-

roanatomical lesions and the clinical features is far from perfect. Cystic leuko-

malacia usually results in severe diplegia. However, diplegia can occur without

any detectable lesion in the newborn period, and noncavitated echogenic areas

may disappear without sequelae (Olsen et al., 1997). Nevertheless, neonatal cra-

nial serial US abnormalities predict impairments in perceptual-motor (de Vries,

Eken, Groenendaal, van Haastert, & Meiners, 1993; Mercuri et al., 1999; van

Wezel-Meijler et al., 1999) and mental functions (Biagioni, Bartalena, Boldrini,

Pieri, & Cioni, 2000; de Vries et al., 1998; Ringelberg & van de Bor, 1993). The

majority of these studies investigated children when they were younger than 2 to

SPASTIC DIPLEGIA 681

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3 years of age, well before more complex cognitive skills and higher motor func-

tioning could be tested. The current design made it possible to evaluate the de-

gree of association between cranial US abnormalities detected early in life and

IQ, as well as neuropsychological functioning when the children achieved the el-

ementary school age with the following hypothesis. Holling and Leviton (1999)

concluded that especially an IQ level below 70 is directly proportional to the

size and extent of the US defined white matter echolucencies, on the basis of 15

studies that satisfied the following criteria: details about the size, extent or loca-

tion of the cerebral white-matter echolucencies seen on cranial US scans, fol-

low-up assessments related to echolucency characteristics, and a sample size of

at least 10 infants. (Unfortunately, authors did not provide in their review spe-

cific information about the range of the IQs.) Given that diplegia is not generally

associated with mental retardation, no correlation between IQ level and US find-

ings was expected in our sample. However, a high correlation was expected be-

tween the cranial US and limitations concerning the lower extremities (walking)

and upper extremities (fine motor functionality).

METHOD

Participants

Fifteen children (9 boys, 6 girls) were randomly selected out of a total sample of 27

children suffering from spastic diplegia in the age range of 5 to 12 years living in

the region of Tampere University Hospital. This hospital serves about 450,000 in-

habitants in the south west of Finland. As infants, they were treated in the neonatal

intensive care unit and followed-up later in the Department of Pediatric Neurology.

Cranial Ultrasound

During the first hospitalization, infants were examined at the neonatal ward by cra-

nial US at least at the ages of 2 and 3 days, and at 1 to 2 weeks intervals afterwards,

using an Aloka SSD-900 mechanical sector scanner (Aloka, Co., Japan) with a

multifrequency transducer (7.5 MHz crystals). After first discharge, US follow-up

was planned individually depending on the clinical status and US findings of the

child. As a result, the range of observations with US after Days 2 to 3 varied from 3

to 10. The 7.5 MHz probe was used to ensure the best possible resolution. PVL was

classified according to de Vries et al. (1993) as I (mild), II (moderate), and III (se-

vere). Grade I is periventricular areas of increased echogenicity present for 7 days

or more or mild structural anomaly. Grade II is loss of brain tissue from any cause,

including small localized fronto-parietal cysts or irregular enlargement of the ven-

tricular system. Grade III is periventricular areas of increased echogenicity evolv-

682 PIRILA ET AL.

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ing into extensive periventricular cystic lesions involving occipital and fronto-pari-

etal periventricular white matter or generalized atrophy of the brain from any

cause. Intraventricular hemorrhage (IVH) grading was performed according to

Papile, Burstein, Burstein, and Koffler (1978). A neonatologist and a pediatric

neurologist were independently performing the US classification in the year 2003.

Both were not aware of the neurocognitive findings of the children, thus improving

the reliability of the US grading. Inconsistencies between the two raters regarding

the presence or the severity of PVL did not take place.

Assessment of Motor Limitations

In the age range of 5 to 12, Autti-Ramo’s (1996) Scale (ARS) was used to measure

the amount of assistance needed in gross motor functioning. The scale classifies

the amount of assistance needed in gross motor functioning as mild (I), moderate

(II) or severe (III) according to the following criteria:

1. Mild disability: the child is able to learn to walk without any assistance, al-

though with spastic gait.

2. Moderate disability: the child may learn to walk assisted.

3. Severe disability: the child is unable to learn to walk or to use functionally

the handicapped part of the body. Instead, he/she may be able to learn to

manage a standard electric wheelchair.

It is to be noted that Level I (mild) of the ARS is comparable to the Levels I and

II of the GMFCS (Nordmark et al., 2001), Level II of the ARS (moderate) equals

Level III of the GMFCS, whereas Level III of the ARS is equivalent with Levels IV

and V of the GMFCS.

The functionality of the upper extremities was classified according to a

three-grade scale ranging from 1 (normal), 2 (immature), to 3 (deviant) concern-

ing muscle tonus, symmetrical use of the hands, and fine motor manipulation.

IQ and Neuropsychological Assessment

When the children were 5 to 12 years of age, two assessments (4 hr duration) were

carried out either in the day care centre or in the child’s school. The cognitive level

was assessed with the aid of the Finnish standardized version of the Wechsler Intel-

ligence Scale for Children-Third edition (the WISC-III). Two children were 5

years of age. To estimate their IQ level the WPPSI-R was used. The neurocognitive

assessment was made using the NEPSY: A Developmental Neuropsychological

Assessment (Korkman, Kirk, & Kemp, 1998). The measure consists of 30 tests

that tap various aspects of attention, language, sensorimotor and visuospatial func-

SPASTIC DIPLEGIA 683

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tions, memory, and learning. Because of the disabilities of the target group and

time constrains, this study limits itself to 14 tests, presented in the results section.

Statistics

Statistical analyses were made by using nonparametric methods (The Statistical

Package for Social Sciences, 10.1) becauseof thedifficulties inmakinganyassump-

tions concerning the normality of the sample distribution. Spearman rho correlation

coefficient was used to explore the linkage between the perinatal predictors and the

outcome. Mann-WhitneyU test was used to measure subgroup differences concern-

ing the NEPSY. Wilcoxon Signed Ranks test was used with repeated measures. P

values less than .05 were considered to be statistically significant.

RESULTS

Table 1 shows per subject the gestational age, birthweight, Apgar scores in 1 and 5

min, de Vries ultrasound classification of PVL (US), the neonatal and additional

problems, the gross motor functionality tapped by the ARS scale, the functionality

of the upper extremities and the IQ scores.

Table 1 shows that the group functioned at or just below the lower boundary of

the normal variation (FIQ: M = 81, range = 64 to 107, SD = 12). The children

showed relatively intact verbal abilities (VIQ: M = 97, range = 76 to 125, SD = 14)

compared to the performance IQ (PIQ: M = 65, range = 36 to 93, SD = 17). The dis-

crepancy between the verbal and performance IQ was significant (Wilcoxon

Signed Ranks test, Z = –3.41, p < .001).

The Spearman correlation between the US results and the FIQ, VIQ, and PIQ

were respectively –.21 (ns), .29 (ns), and –.43 (ns). The Spearman correlation be-

tween the US grading (mild, moderate, severe) and the ARS and the sum score of

the functionality of the upper extremities were respectively .84 (p < .000) and .36

(ns). The findings altogether suggest that the US findings predicted the gross mo-

tor outcome of the children but not the functionality of the upper extremities.

The neuropsychological scores of the NEPSY are depicted in Figure 1.

Figure 1 shows that only 3 of the 5 neuropsychological domains were affected.

As expected, clear deficits were found within the Sensorimotor functions and

Visuospatial processing but Language and Memory or Learning functions were at

or very close to norms, with the exception of the speeded naming task. In addition,

deficits were found in the Attention and Executive Function domain, including the

tower test and visual attention and auditory attention tasks.

Several statistical analyses were carried out to investigate whether functional im-

pairments of the lower and upper extremities or visual limitations were relevant for

the performance on the NEPSY. The ARS scale (tapping the severity of the impair-

684 PIRILA ET AL.

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TAB

LE1

Neo

nata

lSta

tus,

Fun

ctio

nalit

yof

Gro

ssM

otor

and

Fin

eM

otor

Abi

litie

san

dIQ

per

Par

ticip

ant

GA

Wee

ks

Apgar

1/5

min

Low

er

Ext

rem

itie

s

(AR

S)

Hands

Fin

e

Moto

rB

WU

SG

rN

eonata

lP

roble

ms

Addit

ional

Pro

ble

ms

Tonus

Sym

met

ryF

IQV

IQP

IQ

1.

31

1,5

80

7/8

IB

il.per

iven

tric

ula

r

echogen

icit

y,P,

O

11

11

83

92

74

2.

37

2,6

60

1/3

IA

sphyxia

,bil

.

per

iven

tric

ula

r

echogen

icit

yP,

T

Str

abis

mus

ambly

opia

11

11

81

88

75

3.

38

4,5

00

8/9

IH

ypogly

chae

mia

,bil

.

per

iven

tric

ula

r

echogen

icit

y,O

,

ven

tric

lean

dple

xus

chori

oid

us

asym

met

ry

Str

abis

mus

ambly

opia

11

11

67

76

58

4.

26

950

2/5

IA

sphyxia

,bil

.

per

iven

tric

ula

r

echogen

icit

y,F,P,

O,

bil

.ven

tric

ula

r

dil

atat

ion

11

22

97

101

93

5.

28

1,1

75

8/9

IH

ypogly

chae

mia

,bil

.

per

iven

tric

ula

r

echogen

icit

y,O

,bil

.

ven

tric

ula

rdil

atat

ion

IVH

(II)

stra

bis

mus

ambly

opia

12

22

92

93

90

6.

28

1,2

80

6/8

IIP

VL

,unil

.cy

sts,

P(s

),

right

ven

tric

ula

r

dil

atat

ion

IVH

(I)

21

11

79

89

69

(conti

nued

)

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TAB

LE1

(Con

tinue

d)

GA

Wee

ks

Apgar

1/5

min

Low

er

Ext

rem

itie

s

(AR

S)

Hands

Fin

e

Moto

rB

WU

SG

rN

eonata

lP

roble

ms

Addit

ional

Pro

ble

ms

Tonus

Sym

met

ryF

IQV

IQP

IQ

7.

31

1,3

15

1/7

IIP

VL

,bil

.cy

stP,

O(L

),

bil

.ven

tric

ula

r

dil

atat

ion

IVH

(II)

33

33

107

125

88

8.

32

1,6

90

8/8

IIP

VL

,bil

at.cy

sts

P,O

(S),

left

ven

tric

ula

r

dil

atat

ion

Str

abis

mus

32

22

70

103

36

9.

28

1,1

15

8/8

IIP

VL

,bil

.cy

sts

P,O

,(S

),

ger

min

alm

atri

x

deg

ener

atio

n,bil

.

ven

tric

ula

rdil

atat

ion

Str

abis

mus

asti

gm

atis

mus

renal

hyper

tensi

on

31

11

69

87

50

10.

31

1,7

70

4/6

IIP

VL

,unil

.cy

stO

,(S

)S

trab

ism

us

23

33

82

105

61

11.

27

960

6/8

IIP

VL

,unil

.cy

sts

P,O

(S),

bil

.ven

tric

ula

r

dil

atat

ion

Str

abis

mus

myopia

23

33

83

111

53

12.

31

1,7

00

6/7

IIP

VL

,unil

.cy

sts

P,O

(S)

Str

abis

mus

12

22

80

93

49

13.

33

1,5

70

8/8

III

PV

L,bil

.cy

sts

P,O

(L),

right

pore

nkep

hal

y,P,

O,b

il.ven

tric

ula

r

dil

atat

ion

IVH

(III

)st

rabis

mus

abduce

ns

par

esis

31

21

99

112

85

14.

28

1,3

20

7/8

III

PV

L,bil

.cy

sts

P,O

(L),

bil

.ven

tric

ula

r

dil

atat

ion

Str

abis

mus

31

12

70

88

52

15.

32

1,9

70

7/8

III

PV

L,bil

.cy

sts

F,P,

O

(L),

pore

nkep

hal

yF,P,

O,ri

ght

ven

tric

ula

r

dil

atat

ion

IVH

(III

)ep

ilep

sy3

33

364

93

49

No

te.

GA

=ges

tati

on

age;

BW

=bir

thw

eight;

US

Gr

=ult

raso

und

gra

de;

AR

S=

Autt

i-R

amo’s

scal

e;T

onus

=m

usc

leto

nus;

Sym

met

ry=

sym

met

rica

luse

of

upper

extr

em-

itie

s;F

ine

moto

r=

fine

moto

rm

anip

ula

tion;U

nil

.=u

nil

ater

al;B

il.=

bil

ater

al;P

=p

arie

tal;

T=

tem

pora

l;O

=occ

ipit

al;F

=fr

onta

l;L

=la

rge;

S=

smal

l;IV

H=

intr

aven

tric

ula

r

hem

orr

hag

e.

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ment of the lower extremities) correlated only with the block construction subtest of

the NEPSY (ρ = –.52, p < .05), whereas the functionalityof the upper extremities did

not correlate significantly with any of the subtest scores of the NEPSY. A series of

Mann-Whitney U tests showed that children with visual limitations (n = 10, see Ta-

ble 1) scored significantly lower than the children without such difficulties (n = 5) on

the subtests of visual attention (p < .002) and design copying (p < .02).

No significant correlations were found between the cranial US results and the

NEPSY scores.

DISCUSSION

The aim of this study was to investigate the IQ level and neurocognitive profile of

children suffering from spastic diplegia and their relation between brain abnormal-

ity according to neonatal cranial ultrasonography. The children formed a relatively

homogeneous group with respect to cranial US: All had periventricular findings

and posterior cortical abnormality, some unilateral and some bilateral. The find-

ings were as follows:

SPASTIC DIPLEGIA 687

FIGURE 1 Mean scores of the 14 subtests of the NEPSY (a developmental

neuropsychological assessment).

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First, children scored at the lower end of the normal distribution of overall intel-

lectual function, but with normative or near-normative verbal abilities. Better ver-

bal than nonverbal cognitive functioning in CP has also been reported by others

(Carlsson et al., 1994; Fazzi et al., 1994). As expected, children had low scores on

the performance-based IQ scores. This finding was confirmed by the neuro-

psychological investigation (NEPSY) where clear deficits were noticed in the ar-

eas of visuomotor and visuospatial processing, together with relatively intact lan-

guage and memory or learning functions. These findings fit well with the earlier

discussed study of Olsen et al. (1998). This study and the study by Olsen et al.

showed cognitive correlates with posterior cortical damage. However, our sample

of prematurely born children was more affected than theirs with cystic forms of

PVL in parietal, parietal-occipital, or frontal-parietal-occipital areas in 9 out of the

15 children. As a result, our sample demonstrated severe problems in the domains

of visuomotor and visuospatial processing whereas their sample of premature born

children performed poorly in the same domains but in the normal range.

The majority of the children showed severe problems with the lower extremi-

ties: 6 children were unable to learn to walk, and 3 were able to walk assisted.

Given the severe motor limitations of the children one may question to what ex-

tent the performance on NEPSY could be explained by impairments of the upper

extremities as found in 10 children. However, no significant correlations were

found between the fine motor abilities (e.g., ability to manipulate objects) and

the NEPSY. In addition, 10 children showed visual problems. The performance

in the subtests of visual attention and design copying were associated with these

limitations.

The second finding was that there was no relation between the PVL as stated

with ultrasound after birth and later cognitive outcome. No significant correlations

were found between the ultrasound gradings (mild, moderate, severe) and the IQ

scores and neuropsychological functioning. However, a high correlation was

found between the ultrasound findings and the gross motor limitations of the chil-

dren expressed by the ARS.

One may argue that the small number of children who participated in the

study (n = 15) may have prevented a significant correlation between ultrasound

abnormalities and cognitive outcome when they grew older. This argument

seems unlikely. First, the sample size was large enough to demonstrate a clear

correlation between the ultrasound findings and the gross motor impairment.

Second, when reviewing 15 studies that satisfied the criteria of a sample size of

at least 10 infants, Holling and Leviton (1999) concluded that cognitive dysfunc-

tion, especially with an IQ less than 70 was directly proportional to the size and

extent of the ultrasonographically defined white-matter echolucencies. It is to be

noted that about all participants in this study scored in the normal range of ver-

bal abilities. In addition, the nonsignificant correlations between the US finding

and the neurocognitive deficits as indexed by NEPSY, are in accord with the re-

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mark of Levene (1990) that it is unreasonable to expect early neonatal US find-

ings to predict minor impairments that are only detectable after the age of 5

years or more. An additional possible explanation is that cranial US scans are

simply not sensitive enough to reveal subtle injuries as compared with the use of

structural magnetic resonance imaging, which provides superior soft tissue con-

trast and spatial resolution compared to ultrasonography, might be a more appro-

priate methodology to predict neuropsychological disabilities (Olsen et al.,

1998). This said, we acknowledge that these findings are based on a small sam-

ple of children and the results might best be seen as a preliminary and descrip-

tive study with clues about what to look for in new research. As far as our

knowledge goes, correlates to posterior cortical damage have so far not been

looked for and even less found, with the exception of the study by Olsen et al.

(1998). These results suggest that posterior cortical findings are associated with

deficits on visuospatial and visuomotor tasks in addition to deficits in attention

and executive function and speeded naming.

ACKNOWLEDGMENTS

This research has been made possible by Grants 7012 and 9501 of the Tampere

University Foundation and Medical Research Fund of Tampere University

Hospital.

We thank Matti Koivikko for his critical review of earlier drafts of the manu-

script.

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