Child Neuropsychology

A Journal on Normal and Abnormal Development in Childhood and

Adolescence

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Cognitive outcomes of pediatric stroke

Isabella Jacomb, Melanie Porter, Ruth Brunsdon, Anna Mandalis & Louise
Parry

To cite this article: Isabella Jacomb, Melanie Porter, Ruth Brunsdon, Anna Mandalis &
Louise Parry (2016): Cognitive outcomes of pediatric stroke, Child Neuropsychology, DOI:
10.1080/09297049.2016.1265102

To link to this article: http://dx.doi.org/10.1080/09297049.2016.1265102

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CHILD NEUROPSYCHOLOGY, 2016
http://dx.doi.org/10.1080/09297049.2016.1265102

Cognitive outcomes of pediatric stroke

Isabella Jacomba, Melanie Portera, Ruth Brunsdonb, Anna Mandalisc and Louise Parryc
a
Department of Psychology, Macquarie University, North Ryde, Australia; bChildren’s Hospital at
Westmead, Australia; cSydney Children’s Hospital, Randwick, Australia

ABSTRACT ARTICLE HISTORY

A limited number of longitudinal studies have investigated long- Received 1 July 2016
term neuropsychological development in the pediatric stroke Accepted 20 November
2016
population. This study retrospectively examines cognitive out-
comes in 41 children with a history of stroke, with reference to KEYWORDS
age at stroke, laterality, region and mechanism of stroke. In the Neuropsychology; Pediatric;
course of recovery, neuropsychological measures of intellectual Childhood; Stroke; Outcome
functioning and memory were administered at two time points,
whilst executive functioning, attention and academic skills were
administered at one time point. As predicted, children with stroke
performed significantly worse compared to normative expecta-
tions on all neuropsychological measures. Up to two thirds of
children scored in the borderline impaired and impaired ranges
on at least one domain of cognition. Performance on intellectual
and memory assessment remained relatively stable over time.
Younger age at stroke was found to be associated with poorer
intellectual functioning. No effects of laterality of stroke on neu-
ropsychological performance over time were found. Children with
subcortical stroke demonstrated a greater improvement in
immediate memory over time than children with cortical stroke.
These findings reveal that children with stroke display long-term
cognitive difficulties that typically remain stable over time.
Attention and academic skills are particularly vulnerable to impair-
ment. Further evidence that age at stroke is a significant factor in
terms of cognitive outcome is provided, in support of the “early
vulnerability” position.

Pediatric stroke has an estimated incidence of between 0.6 and 13 cases per 100,000
children (Hartel, Schilling, Sperner, & Thyen, 2004). Available studies have demon-
strated that stroke in childhood is associated with a range of poor outcomes, including
seizures (Cnossen et al., 2010; deVeber, MacGregor, Curtis, & Mayank, 2000), paresis
(Galvin, Hewish, Rice, & Mackay, 2011; Steinlin, Roellin, & Schroth, 2004), behavioral
difficulties (Trauner, Nass, & Ballantyne, 2001); psychiatric disorders (Max et al., 2002,
2003), and poorer quality of life (O’Keeffe, Ganesan, King, & Murphy, 2012).
Neuropsychological studies that are available have shown that children with stroke
often display reductions in many cognitive domains compared to controls and norma-
tive expectations, including intellectual functioning (Hogan, Kirkham, & Isaacs, 2000),

CONTACT Isabella Jacomb ijacomb@bigpond.com

The supplemental data for this article can be accessed here
© 2016 Informa UK Limited, trading as Taylor & Francis Group
2 I. JACOMB ET AL.

attention (Max et al., 2004), processing speed (Block, Nanson, & Lowry, 1999), language
(Ballantyne, Spilkin, & Trauner, 2007; Funnell & Pitchford, 2010), visuospatial abilities
(Schatz, Craft, Koby, & DeBaun, 2004), learning and memory (Lansing et al., 2004) and
executive functioning (Anderson et al., 2010; Long et al., 2011). The extent of these
deficits varies, with neuropsychological performance ranging from impaired to low
average (i.e., from 0.7 to > 2 SDs below normative expectations; Anderson et al.,
2010; Everts et al., 2008). Moreover, one study reported ongoing cognitive impairments
in approximately 75% of children 2 years post-stroke (Pavlovic et al., 2006).
There are a number of factors that may affect the impact of childhood stroke on
neuropsychological performance, including age at stroke, and laterality, region, and
mechanism of stroke. A recent paper by Fuentes, Deotto, Desrocher, deVeber, and
Westmacott (2016) reviews the literature findings on the role that these factors may
have on cognitive outcomes in childhood stroke. Evidence consistently indicates that
younger age at stroke is a risk factor for less favorable cognitive outcomes (Anderson
et al., 2010; Block et al., 1999; Lansing et al., 2004; Max, Bruce, Keatley, & Delis, 2010).
However, a non-linear model of age at lesion effects has also been proposed, with
findings suggesting that stroke in middle childhood may lead to a better outcome on a
range of neuropsychological measures compared with stroke occurring in very early or
late childhood (Allman & Scott, 2013; Everts et al., 2008; Jacobs, Harvey, & Anderson,
2007). Several studies have not found any effect of laterality on cognitive outcomes such
as intellectual functioning (Ballantyne et al., 2007; Everts et al., 2008) and memory
(Lansing et al., 2004) following pediatric stroke, and it appears that factors such as age
at stroke, age at assessment, and the specific cognitive domain being assessed are likely
to be moderating influences (Fuentes et al., 2016). In regard to region of stroke, it has
consistently been found that combined cortical and subcortical lesions (compared to
cortical or subcortical) have proved to be the most detrimental in terms of cognitive
outcome, whilst cortical stroke has a poorer cognitive outcome than subcortical stroke
(Steinlin et al., 2004). The potential role of mechanism of stroke (ischemic vs. hemor-
rhagic) on long-term cognitive outcomes has not been examined.

Change in Neuropsychological Performance over Time in Pediatric Stroke

Time may bring no change in cognitive status; alternatively, time may reveal new deficits,
exacerbate old deficits, or change the rate of development. (Dennis, 2000)

Based on the literature, there are two competing hypotheses regarding longitudinal
cognitive outcomes in children with early brain damage. Children’s cognitive functions
may either remain stable over time or, alternatively, children may fail to make age-
appropriate developmental gains or “grow into” seemingly new deficits (Anderson,
Northam, Hendy, & Wrennall, 2001).
To date, very few longitudinal studies have been conducted on neuropsychological
development in children following stroke. Of the longitudinal studies that have been
conducted, the majority have only examined change over time in children who experi-
enced a stroke in the perinatal or neonatal period (Ballantyne, Spilkin, Hesselink, &
Trauner, 2008; Westmacott, MacGregor, Askalan, & deVeber, 2009). Overall, these
studies have produced conflicting results. For instance, some studies have concluded
 CHILD NEUROPSYCHOLOGY 3

that performance on neuropsychological measures remains stable over time (Ballantyne

et al., 2008; Muter, Taylor, & Vargha-Khadem, 1997), perhaps consistent with the
plasticity hypothesis, whilst other studies have reported greater deficits in performance
over time (Levine, Kraus, Alexander, Suriyakaham, & Huttenlocher, 2005; Westmacott
et al., 2009), more in line with the vulnerability account.
Thus far, only one study has investigated cognitive and intellectual outcomes over
time in children who sustained a stroke within a broad age range. In this study, Aram
and Eisele (1994) reported overall stability in the intellectual performance of children
with stroke over a mean time period of 4 years and 2 months, with age at stroke ranging
from prenatal to 16 years. The results suggest that earlier age at stroke, particularly
prenatally or during the first few years of life, may be more detrimental to intellectual
development than injury sustained later in childhood.
As such, the literature on change over time in children with stroke is very limited,
and mostly restricted to early onset stroke data and intellectual functioning. Multiple
factors may have led to inconsistent and unreliable findings, including the use of a small
cohort size, numerous different assessment measures and a short test–retest interval
(Ballantyne et al., 2008). These mixed results suggest that further research into the
longitudinal effects of neuropsychological performance in children with stroke is
required (Fuentes et al., 2016).

The Current Study

In light of the above, the current retrospective study aims to investigate cognitive
outcomes following pediatric stroke in a relatively large retrospective clinical sample
of children followed-up over time. Particular reference is paid to the influence of age at
stroke and the laterality, region and mechanism of stroke in determining cognitive
outcomes. Compared to previous longitudinal studies, which have predominantly
examined change over time in perinatal and neonatal stroke, the current study exam-
ines a broader age range of children (i.e., 0 to 17 years at age of stroke). The current
study specifically focuses on intellectual functioning (full-scale, verbal and nonverbal),
verbal memory (immediate, delayed and recognition), executive functioning, attention,
and academic skills. The domains of intellectual functioning and memory are the only
cognitive areas studied at both time points.
The aims of the study are as follows: (1) To investigate whether children who
suffer a stroke perform more poorly on neuropsychological tests (intellectual func-
tioning, memory, executive functioning, attention, and academic skills) relative to
standardized norms; (2) to examine whether there are any significant changes in
performance in measures of intellectual functioning and memory over time; and (3)
to explore whether there are effects of age at stroke, laterality of stroke (i.e., left,
right, bilateral), region of stroke (cortical, subcortical) and mechanism of stroke
(ischemic, hemorrhagic) on change in intellectual functioning and memory perfor-
mance over time.
4 I. JACOMB ET AL.

Method
Participants
The participants consist of pediatric stroke patients who underwent at least two
neuropsychological assessments during the time period of 2000 to 2014 at the
Children’s Hospital at Westmead and the Sydney Children’s Hospital at Randwick,
both in Sydney, Australia. Eligible children were identified from database searches
within the Brain Injury Rehabilitation Program across sites.
The inclusion criteria are as follows: (1) aged 0 to 17 years at time of stroke; (2)
evidence of stroke on magnetic resonance imaging (MRI) brain scan; and (3) at least two
neuropsychological assessments. Exclusion criteria are: (1) history of pre-injury develop-
mental delay or intellectual disability or learning disability; (2) stroke secondary to brain
tumor resection; (3) stroke secondary to neurological impairment such as traumatic brain
injury, hypoxia; (4) moya moya disease; and (5) a history of seizures. A total of 14
children were excluded based on the above criteria, which left a cohort of 41 children (24
males). The age range of the sample at time of their stroke was 0.00 to 16.64 years
(M = 6.96, SD = 4.92). Table 1 provides demographic information on the sample.

Materials
Socioeconomic status (SES)
Area of residency for each family (using postal codes) was used as a measure of each
child’s SES based on the Index of Relative Socio-Economic Disadvantage (IRSD;
Australian Bureau of Statistics, 2011), with a range from 0 to 100. The IRSD is a
general socioeconomic index that summarizes a range of information about the eco-
nomic and social conditions of people and households within an area. A lower index
score reflects relatively greater disadvantage (lower SES), whilst a higher index score
reflects a relative lack of disadvantage in general (higher SES).

Coding Protocol
A standard coding protocol (modified from Leventer et al., 1999) was employed to rate
brain insult characteristics: (a) Age of stroke was determined via MRI brain findings and
medical records (clinical history, medical investigations); (b) Mechanism of stroke was
coded as “ischemic” or “hemorrhagic”; (c) Region of stroke was coded as: “cortical”,
“subcortical”, “cortical & subcortical” or “intraventricular”; and (d) Laterality was

Table 1. Participant Demographics (n = 41).

M (SD) Range
Sex (number M/F) 24/17 -
Socioeconomic status (SES) 58.61 (27.93) 6.00–100.00
Age at stroke (years) 6.96 (4.92) 0.00–16.64
Age at initial assessment (years) 8.46 (3.70) 4.58–17.16
Age at final assessment (years) 12.51 (3.30) 6.79–18.55
Time since stroke at initial assessment (years) 1.51 (2.07) 0.12–7.81
Time since stroke at final assessment (years) 5.55 (3.59) 1.14–13.30
Time between initial and final assessment (years) 4.04 (2.64) 0.79–11.14
Note. SES measured by the Index of Relative Socio-Economic Disadvantage (IRSD).
 CHILD NEUROPSYCHOLOGY 5

Table 2. Participant Stroke Characteristics (n = 41).

n
Laterality
Left 8
Right 8
Bilateral 7
Region
Cortical 23
Subcortical 10
Cortical & Subcortical 6
Intraventricular 2
Stroke Mechanism
Ischemic 13
Hemorrhagic 28

coded as: “left”, “right”, or “bilateral” (only cortical strokes were coded for laterality).
These characteristics were determined from neuroimaging records that had been
reviewed and determined by independent qualified neurologists. Table 2 provides
details of stroke characteristics for the current research cohort. See Supplementary
Material A for information on cause of stroke.

Neuropsychological Measures
A comprehensive clinical neuropsychological test battery was undertaken at each time
point. However, the retrospective nature of the study across different clinical sites and the
lengthy period of time over which the data was viewed means that a number of different test
batteries were used. Some neuropsychological measures were therefore combined pragma-
tically to provide a summary measure of the relevant cognitive domain (see Supplementary
Material B for the full list of all measures used across all cognitive domains).

Longitudinal Analyses
The following cognitive domains were assessed at two time points and included in the
analyses to provide an indication of change over time.

Intellectual Functioning
A number of measures of intellectual functioning were utilized. All measures of intellectual
functioning are highly correlated in terms of validity (Elliott, 1990, 2007; Wechsler, 1989;
Wechsler, 1997a, 2004, 2005b, 2008) and, therefore, are considered suitable for providing
an overall index of intellectual functioning. Index measures were obtained for the following:
Verbal IQ (VIQ), Nonverbal IQ (NVIQ), and Full-Scale IQ (FSIQ).

Memory
Several measures of verbal memory were utilized. All measures of verbal memory are
highly related in terms of validity (Adams & Sheslow, 2003; M. Cohen, 1997; Wechsler,
1997b, 2009) and provide an overall index of memory. Index measures were obtained
for Immediate Memory, Delayed Memory, and Recognition Memory.
6 I. JACOMB ET AL.

Cross-sectional Analyses
The following cognitive domains were assessed at only one time point (final assess-
ment) and were included in the analysis.

Executive Functioning in Everyday Life

The Behavior Rating Inventory of Executive Function (BRIEF; Gioia, Isquith, Guy, &
Kenworthy, 2000) provides an index of executive abilities in everyday life. The BRIEF
comprises 8 clinical scales (Inhibition, Shift, Executive Control, Initiate, Working Memory,
Plan/Organize, Organization of Materials, and Monitor) that form two broader indices
(Metacognition and Behavioral Regulation). A Global Executive Composite (GEC) can also
be calculated. A t-score greater than 65 indicates clinically significant executive impairment.

Attention
The Test of Everyday Attention for Children (TEA-Ch; Manly, Robertson, Anderson, &
Nimmo-Smith, 1999) was used to measure attention. The subtests Sky Search, Score
and Sky Search DT provide measures of selective attention, sustained attention and
divided attention, respectively.

Academic Skills
The Wechsler Individual Achievement Test – Second Edition (WIAT-II; Wechsler,
2005) provides measures of academic functioning. The subtests of interest are Word
Reading, Spelling, and Numerical Operations.

Procedure
This study was approved by the Human Research Ethics Committee of the Sydney
Children’s Hospital Network, Sydney, Australia. Eligible children were identified via
medical records. Children had been assessed individually by a clinical neuropsycholo-
gist employed at either the Children’s Hospital at Westmead or the Sydney Children’s
Hospital at Randwick, both in Sydney, Australia.

Statistical Methods
Some children did not complete some measures due to the retrospective nature of the
study. Missing data are not recoded.
Quantitative analyses were conducted using SPSS v18.0. Initial analyses (chi-squared tests
and analyses of variance [ANOVAs]) focused on determining the presence of any group
differences on descriptive demographics (gender, SES, age at assessments) and lesion variables
(age at stroke, time since stroke, and laterality, mechanism and region of stroke) that might
contribute to group differences on neuropsychological measures. To determine whether
children with stroke performed more poorly than expected across cognitive domains, the
subsample of the individuals who undertook neuropsychological assessment at two time
points was compared to the published test norms using independent sample t-tests, and effect
sizes were calculated using Cohen’s d (J. Cohen, 1988). Reliable change index (RCI) measures
were calculated using the Jacobson–Truax method (Jacobson & Truax, 1991), using the
 CHILD NEUROPSYCHOLOGY 7

reliability values from the current sample’s performance on neuropsychological measures. An

RCI of 1.96 or greater was used to assess whether the mean difference between performance at
initial and final assessment is a clinically reliable change. Individual participants who meet the
RCI criteria are considered to have “reliable change”, and either “reliable improvement” or
“reliable decline” in their intellectual functioning and memory from the initial to final
assessment time point. Participants’ initial assessment scores were subtracted from their
final assessment scores to provide change scores. Pearson correlations and univariate
ANOVAs were subsequently used to investigate the effects of age at stroke, and laterality,
region and mechanism of stroke that may impact on performance change over time.

Results
Sample Demographics
To evaluate any baseline differences between demographic and lesion variables, chi-
squared tests and ANOVAs were conducted.
There is a similar number of males and females in regard to laterality and region of
stroke (p > .05). A prevalence of 24.4% of males with ischemic stroke was found
compared to 7.3% of females. There are no statistically significant main effects of
gender on age at stroke, time since stroke at initial assessment, time since stroke at
final assessment and time elapsed between initial and final assessment (p > .05).
No significant main effects of age were found in terms of laterality, mechanism, or
region of stroke at initial assessment or at final assessment.

Comparing Stroke Patients to Normative Expectations

Patient assessment results were compared to the normative results published in technical
manuals for each assessment measure. As illustrated in Table 3, as a group, the overall mean
of children with stroke was lower than the normal population on all intellectual functioning
measures at both the initial and final assessments (p < .05). Cohen’s d effect sizes are

Table 3. Differences between the Clinical Sample and Test Means for Intellectual Functioning and
Memory.
n M SD t p Cohen’s d Borderline Impaired (%) Impaired (%)
Initial FSIQ 31 87.06a 15.25 −4.72 <.001** 0.86 9.68 9.68
Final FSIQ 31 88.00a 17.96 −3.72 .001** 0.73 6.45 12.90
Initial VIQ 39 89.23a 13.60 −4.94 <.001** 0.75 7.69 7.69
Final VIQ 39 91.38a 15.03 −3.58 .001** 0.57 7.69 10.26
Initial NVIQ 38 90.11a 17.61 −3.46 .001** 0.60 18.42 10.53
Final NVIQ 38 90.26a 19.12 −3.14 .003** 0.57 7.89 18.42
Initial Immediate Memory 23 8.26b 3.77 −2.21 .038* 0.51 4.34 21.74
Final Immediate Memory 23 9.26b 4.03 −0.88 .388 0.21 8.70 26.09
Initial Delayed Memory 18 8.17b 4.01 −1.94 .070 0.52 5.56 27.78
Final Delayed Memory 18 9.28b 4.62 −0.66 .517 0.18 5.56 27.78
Initial Recognition Memory 12 10.08b 4.54 0.64 .950 0.02 8.33 16.67
Final Recognition Memory 12 9.50b 3.40 −0.51 .620 0.16 8.33 16.67
Note. *p < .05; **p < .01; astandard score where M = 100 and SD = 15 in a normative sample; bscaled score where
M = 10 and SD = 3 in a normative sample. FSIQ = Full-scale IQ; NVIQ = Nonverbal IQ; VIQ = Verbal IQ. Borderline
Impaired = standard scores between 71 and 79 or scaled scores of 6 (i.e., 1.3 to 2 SDs below the mean);
Impaired = standard scores ≤ 70 or scaled scores ≤ 5 (i.e., > 2 SDs below the mean).
8 I. JACOMB ET AL.

medium to large. The overall mean for the immediate memory measure was lower than the
normal population at the initial assessment (p < .05) but not at the final assessment. There
were no significant differences between children with stroke and the normative sample on
delayed memory and recognition memory measures at either time point (p > .05). A
significant proportion of participants (15.38% to 34.79%) had borderline impaired or
impaired scores (i.e., a clinically significant impairment) on all measures of intellectual
functioning and memory.
Table 4 shows that children with stroke achieved higher t-scores than the normative
sample on nearly all BRIEF measures at the final assessment (p < .05). Within the stroke
group, 25.93% achieved a GEC t-score greater than 65, indicating clinically significant
levels of executive functioning impairment. Effect sizes are small to large. The only
measure on which children with stroke did not differ significantly from the normative
sample is Organization of Materials in the BRIEF (p > .05; see Table 4).
As shown in Table 4, children with stroke scored significantly lower on the selective
attention and divided attention measures (Sky Search and Sky Search DT) administered
at the final assessment (p < .05), with medium to large effect sizes. Mean scaled scores
are in the impaired range for divided attention (Sky Search DT). There is a statistical
trend toward children with stroke performing lower on a sustained attention measure
(Score!). Similarly, children scored significantly lower on all academic measures
(p < .05), with large effect sizes. Overall, 29.16% to 66.67% of participants performed
in the borderline impaired and impaired range on all attention measures. The mean
group performance on Numerical Operations (mathematical calculations) falls within

Table 4. Differences between the Clinical Sample and Normative Means for Executive Functioning,
Attention and Academic Functioning at Final Assessment.
n M SD t p Cohen’s d Borderline Impaired (%) Impaired (%)
BRIEF
Inhibition 27 54.37a 10.12 2.24 .034* 0.43 22.22
Shift 27 55.67a 11.46 2.57 .016* 0.53 22.22
Executive Control 27 56.04a 10.16 3.09 .005** 0.60 14.81
Initiate 27 56.48a 10.70 3.15 .004** 0.63 25.93
Working Memory 27 61.93a 9.89 6.27 <.001** 1.20 44.44
Plan/Organize 27 57.63a 10.55 3.76 .001** 0.74 22.22
Organization of Materials 27 53.26a 11.80 1.44 .163 0.30 22.22
Monitoring 27 58.33a 9.73 4.45 <.001** 0.84 25.93
Behavior Regulation 27 57.15a 8.70 4.19 <.001** 0.76 14.81
Metacognition 27 59.31a 10.10 4.70 <.001** 0.93 25.93
GEC 27 59.04a 9.15 5.04 <.001** 0.94 25.93
TEA-Ch
Sky Search 24 7.42b 2.64 −4.80 <.001** 0.91 8.33 20.83
Score! 24 8.46b 3.79 −1.99 .058 0.45 4.17 29.17
Sky Search DT 24 5.29b 3.87 −5.96 <.001** 1.36 20.83 45.83
WIAT
Numerical Operations 17 77.94c 25.40 −3.58 .002** 1.06 - 53.85
Word Reading 17 86.41c 9.16 −2.92 .010** 1.09 11.76 23.53
Spelling 13 88.38c 16.09 −2.60 .023* 0.75 7.69 15.38
Note. *p < .05; **p < .01; at-score where M = 50 and SD = 10 in a normative sample. bscaled score where M = 10 and
SD = 3 in a normative sample; cstandard score where M = 100 and SD = 15 in a normative sample. BRIEF = Behavior
Rating Inventory of Executive Functioning; GEC = Global Executive Composite; TEA-Ch = Test of Everyday Attention
for Children; WIAT = Wechsler Individual Achievement Test – Second Edition. Borderline Impaired = standard scores
between 71 and 79 or scaled scores of 6 (i.e., 1.3 to 2 SDs below the mean); Impaired = t-scores ≥65, standard scores
≤70, scaled scores ≤ 5 (i.e., > 2 SDs below the mean). Bold font indicates mean scores that fall into the Borderline
Impaired range.
 CHILD NEUROPSYCHOLOGY 9

Table 5. Difference in Performance on Intellectual Functioning and Memory Tests over Time.
Initial Final M Reliable Reliable Reliable
n M M difference RCI change (%) improvement (%) decline (%)
FSIQ 31 87.06a 88.00 0.94 15.82 16.13 12.90 3.23
VIQ 39 89.23a 91.38 2.15 15.99 12.82 7.69 5.13
NVIQ 38 90.11a 90.23 0.12 16.91 18.42 7.89 10.53
Immediate Memory 23 8.26b 9.26 1.00 4.05 26.09 17.39 8.70
Delayed Memory 18 8.17b 9.28 1.11 4.16 11.11 11.11 0.00
Recognition Memory 12 10.08b 9.50 −0.58 6.89 16.67 0.00 16.67
Note. astandard score where M = 100 and SD = 15 in a normative sample; bscaled score where M = 10 and SD = 3 in a
normative sample. FSIQ = Full-scale IQ; NVIQ = Nonverbal IQ; RCI = Reliable Change Index; VIQ = Verbal IQ.

the borderline impaired range. The Word Reading and Spelling mean scaled scores fall
within lower average levels, significantly lower than the normative sample. Overall,
23.07% to 53.85% of participants’ scores fall at borderline impaired and impaired levels
on academic measures.

Intellectual Functioning and Memory Change over Time

Table 5 presents RCI values for each of the IQ and memory measures which show that
none of the mean difference scores meet the RCI criteria. Table 5 also shows that there
is only a small percentage of individuals who displayed either a reliable improvement or
a reliable decline in their performance on the measures.

Effects of Age at Stroke on Change over Time

As shown in Table 6, there are significant correlations between age at stroke and change
in FSIQ and NVIQ over time, p < .05. That is, younger age at stroke is significantly
associated with greater change in intellectual functioning over time and overall poorer
intellectual outcome. The effect sizes are medium. There is also a statistical trend
toward an association between age at stroke and change in VIQ. There are no sig-
nificant correlations between age at stroke and change on any of the memory measures
over time, p > .05.

Effects of Laterality on Change over Time

There are no significant main effects of laterality on FSIQ change, F(2, 14) = 2.32,
p > .05, VIQ change, F(2, 19) = 1.14, p > .05, or NVIQ change, F(2, 19) = 2.11, p > .05.

Table 6. Correlations between Age at Stroke and Change in Neuropsychological Measures.

n Age at stroke, M (SD) M difference (SD) r p
Change in FSIQ 31 6.96 (4.92) 0.94 (11.70) .36 .049*
Change in VIQ 39 6.96 (4.92) 2.15 (11.04) .29 .079
Change in NVIQ 38 6.96 (4.92) 0.16 (11.29) .44 .006**
Change in Immediate Memory 23 6.96 (4.92) 1.00 (2.75) −.05 .811
Change in Delayed Memory 18 6.96 (4.92) 1.11 (3.08) −.16 .538
Change in Recognition Memory 12 6.96 (4.92) −0.58 (3.80) .09 .782
Note. *p < .05; **p < .01. FSIQ = Full-scale IQ; NVIQ = Nonverbal IQ; VIQ = Verbal IQ.
10 I. JACOMB ET AL.

There are also no significant main effects of laterality in terms of immediate memory
change, F(2, 10) = 0.63, p > .05, delayed memory change, F(2, 7) = 0.24, p > .05, or
recognition memory change, F(2, 5) = 0.33, p > .05.

Effects of Region of Stroke on Change over Time

There are no significant main effects of region of stroke on FSIQ change, F(1,
23) = 0.23, p > .05, VIQ change, F(1, 30) = 0.52, p > .05, or NVIQ change, F(1,
30) = 0.09, p > 0.5.1 There is a significant main effect of region on immediate memory
change, F(2, 18) = 6.80, p = .02, with subcortical stroke resulting in a greater change in
immediate memory (M = 2.71, SD = 2.14) than cortical stroke (M = −0.15, SD = 2.44).
There are no significant main effects of region on delayed memory change, F(1,
14) = 2.29, p > .05, or recognition memory change, F(1, 9) = 0.48, p > .05.

Effects of Mechanism of Stroke on Change over Time

There are no significant main effects of mechanism of stroke on FSIQ change, F(1,
29) = 0.03, p > .05, VIQ change, F(1, 37) = 0.30, p > .05, or NVIQ change, F(1,
36) = 0.08, p > .05. There are also no significant main effects of stroke mechanism on
immediate memory change, F(1, 21) = 1.26, p > .05, delayed memory change, F(1,
16) = 0.10, p > .05, or recognition memory change, F(1, 10) = 3.46, p > .05.

Discussion
The current study retrospectively examines cognitive outcomes at two assessment time
points in children who sustained a stroke between the ages of 0 and 17 years, providing
a mean follow-up period of 5.55 years at the second time point. Specifically, it
investigates whether children with stroke perform significantly worse compared to
normative expectations on a range of neuropsychological measures at both the initial
and final assessment time points. It also examines whether performance on intellectual
functioning and memory measures improved or deteriorated across the two time
points. An analysis of whether factors such as age at stroke, and laterality, region and
mechanism of stroke impacted the change in cognitive outcomes was also undertaken.
Overall, as predicted, children with stroke were found to be at increased risk of poor
cognitive outcomes compared to healthy children at both initial and final assessment
times. In particular, when compared to normative expectations, children who suffered a
stroke performed significantly worse on neuropsychological measures of intellectual
functioning at both assessment time points, in line with findings from previous cross-
sectional studies (Allman & Scott, 2013; Anderson et al., 2010; Long et al., 2011). Of
note, however, is that mean scores on intellectual and memory functioning measures at
both time points remained within normal limits, in the low average to average range,
also consistent with previous literature (Everts et al., 2008; Hogan et al., 2000).
However, 15.38% to 34.79% of participants’ scores on measures are reflective of border-
line impaired or impaired intellectual functioning and memory.
The assessment of attention, executive functioning and academic functioning was
only consistently undertaken at the final assessment point. A review of these data shows
 CHILD NEUROPSYCHOLOGY 11

a significant difference on mean scores on executive functioning, attention and aca-

demic functioning compared to the normative sample and, whilst the majority of mean
scores fall in the low average to average range, 14.81% to 66.67% of children performed
at borderline impaired or impaired levels on these measures. The measure of divided
attention falls into the impaired range, consistent with the findings of Anderson et al.
(2010). The current study also found that the mean scores on arithmetic calculation fall
into the borderline impaired range, whereas previous cross-sectional studies have
reported less compromised arithmetic abilities (Max, 2004; Max et al., 2010). Overall,
these findings suggest that attention and academic functioning may be particular areas
of cognitive weakness for children following stroke.
In support of the second hypothesis, there was no clinically reliable change in
participants’ performance on neuropsychological measures of intellectual functioning
or memory between the initial and final assessment time points. These relatively
stable results across time are consistent with Aram and Eisele’s (1994) longitudinal
study, which also includes children who sustained a stroke in the perinatal to late
childhood period. The findings are also consistent with Ballantyne et al.’s (2008)
longitudinal study, which is restricted to children with perinatal stroke. Despite the
current findings, it is possible that children with a history of pediatric stroke may
display cognitive or intellectual impairments that increase or even emerge over time
(Anderson et al., 2001).
Consistent with the third hypothesis, however, age at stroke had a significant impact
on outcome on two measures of intellectual functioning (VIQ and FSIQ). There is a
statistical trend toward age at stroke impacting on outcome in NIQ. There is a linear
influence of age effects, with a younger age being associated with greater change in
intellectual functioning over time (i.e., failure to make appropriate gains) and overall
poorer outcome in terms of intellectual functioning. This finding is in line with
previous cross-sectional studies (Anderson et al., 2010; Studer et al., 2014). Overall,
the association between age at stroke and change in intellectual functioning over time is
consistent with the “early vulnerability” position of brain development, which proposes
that earlier age at brain insult may result in greater impairments in cognitive
functioning.
Interestingly, however, there is no significant effect of age at stroke and change in
verbal memory measures over time, contrary to predictions. This result is also divergent
from Lansing et al.’s (2004) cross-sectional study which found that early age at stroke is
associated with greater verbal learning and memory impairment compared to older age
at stroke. To the best of the authors’ knowledge, the current study is the first to examine
longitudinal change in memory scores over time. The current results may, therefore,
suggest that age at stroke does not have such an important impact on change in
memory over time, compared to intellectual functioning.
As predicted, there is no significant effect of laterality on change in intellectual
functioning or memory over time, consistent with previous cross-sectional studies
(Everts et al., 2008; Max, 2004) and with Ballantyne et al.’s (2008) longitudinal study
investigating intellectual outcomes following perinatal stroke. As such, the current
findings support the proposal that, as opposed to the striking lateralized deficits seen
in adults with stroke (Ballantyne et al., 2007), patients with a history of pediatric stroke
display more “generalized” deficits over time in several cognitive domains (Max, 2004).
12 I. JACOMB ET AL.

There is some support for the prediction that the region of stroke would have a
significant effect on change in performance on intellectual and memory measures over
time. Specifically, children with subcortical stroke show significantly greater change in
immediate memory over time than children with cortical stroke. This finding is con-
sistent with previous cross-sectional studies which have shown that cortical stroke is
associated with poorer cognitive outcomes than subcortical stroke (Steinlin et al., 2004).
However, it is of note that the current sample has relatively small group sizes in terms
of region of stroke compared to these previous studies. It was also not possible to
analyze the effect of intraventricular or combined cortical and subcortical stroke on
cognitive outcome due to the small group sizes. Future studies with larger group sizes
are warranted to further investigate the results of the current study.
Lastly, there is no support for the hypothesis that mechanism of stroke has a
significant effect on change in performance on neuropsychological measures over time.

Strengths of the Research

This is one of only a few longitudinal studies investigating cognitive outcomes in
children following stroke. A major advantage of the present study is the inclusion of a
relatively large number of children aged 0 to 17 years at time of stroke, especially
given that pediatric stroke is described as rare in the literature. The exclusion of
children with documented premorbid intellectual disability, developmental delay or
learning disability eliminates the possibility of confounding the current results.
Furthermore, by excluding children with brain lesions of diverse neurological
causes—such as traumatic brain injury, brain tumors, and comorbid seizure disor-
ders—it was possible to study a relatively pure sample of individuals with pediatric
stroke. In this way, potential limiting factors such as more diffuse damage or the
effects of a chronic, evolving lesion were avoided.
Another strength of the current study is its use of standardized neuropsychological
measures to assess performance in the different cognitive domains. Furthermore, whilst
it can be argued that using well-matched control groups as a comparison is the best
approach, the utilization of normative data does have an advantage over the use of the
kind of small, unrepresentative control samples commonly reported in this field that
can increase the risk of the inaccurate characterization of study results.

Limitations of the Research

When interpreting the current study findings, a number of potential limitations should
be considered. Firstly, as a retrospective study conducted over many years, there are
inevitably missing data and changes in assessment protocols that took place over time
which require compromises on methodology and statistical analysis. Specifically, parti-
cipants were assessed on different measures of intellectual functioning and memory.
However, correlations between the intelligence indices and memory indices are high
and, therefore, inherent differences in scores due to varying test protocols should be
minimized.
Future research should also include analysis of other important cognitive domains
over time, such as language, visuospatial skills, working memory, visual memory and
 CHILD NEUROPSYCHOLOGY 13

processing speed, which could not be investigated in the present study due to its
retrospective nature and the fact that these tests were not administered to a large
proportion of the current sample. Assessment of executive functioning, attention and
academic functioning at two time points would also be optimal in order to provide
information on any change in outcomes over time in these domains.

Clinical Implications
Despite the above limitations, this study has widespread clinical applications. Firstly, it
provides additional evidence that children with stroke demonstrate lowered perfor-
mance, relative to normative populations, on neuropsychological measures of intellec-
tual functioning, memory, executive functioning, attention, and academic functioning,
compared to normative expectations. A substantial proportion of children (up to two
thirds in this study) are at risk of a borderline impaired or impaired cognitive outcome,
particularly in the domains of divided attention and academic arithmetic skills. Based
on current cognitive rehabilitation research, a focus on remediating these skills in a
child who has sustained a stroke might cause change and prevent long-term impair-
ment (Anderson & Catroppa, 2006; King, DeBaun, & White, 2008; Rabipour & Raz,
2012).
The current study also provides important information about prognosis in children
with stroke over time, and reveals that children with stroke present with very little
improvement or decline in their intellectual and verbal memory abilities. A greater
understanding of how children with pediatric stroke fare over time is particularly
important, as it will benefit parents, clinicians and teachers in generating appropriate
expectations and realistic goals (as well as making it easier to plan for rehabilitation and
educational support needs over the long term).
The results also show that young age is a risk factor for a poor cognitive outcome in
childhood stroke, which suggests that children with early stroke onset have an obvious
need for neuropsychological follow-up after stroke, because this identifies as early as
possible which children will require additional educational interventions to support
their learning. Furthermore, whilst older age at stroke appears to result in better
cognitive outcomes, these children should still receive follow-up neuropsychological
assessments over time, particularly in relation to their attention and academic skills.

Conclusion
The current study is one of very few longitudinal studies that investigates long-term
cognitive outcomes in children with stroke across two assessment time points.
Overall, the current findings contribute to the literature by revealing that children
with stroke display long-term cognitive weaknesses, with no significant improvement
or decline in their abilities occurring over time. Attention and academic skills may
be particularly vulnerable to long-term impairment. Further evidence that age at
stroke is a significant factor in terms of cognitive outcome is provided, in support of
the “early vulnerability” position. There is also some support for subcortical stroke to
be related to better cognitive outcomes than cortical stroke. The current study is one
of the first longitudinal studies to reveal that there appear to be minimal effects of
14 I. JACOMB ET AL.

laterality and mechanism of stroke on cognitive outcome change over time.

Implications for clinical practice are important, as follow-up neuropsychological
assessments are necessary to target future rehabilitation and intervention of cognitive
deficits in children with stroke.

Note
1. On account of the small group size, intraventricular strokes (n = 2) and combined cortical &
subcortical strokes (n = 6) were not included in the region of stroke analysis.

Disclosure statement
No potential conflict of interest was reported by the authors.

References
Adams, W., & Sheslow, D. (2003). Wide Range Assessment of Memory and Learning (2nd ed.).
Lutz, FL: Psychological Assessment Resources.
Allman, C., & Scott, R. B. (2013). Neuropsychological sequelae following pediatric stroke: A
nonlinear model of age at lesion effects. Child Neuropsychology, 19(1), 97–107. doi:10.1080/
09297049.2011.639756
Anderson, V., & Catroppa, C. (2006). Advances in postacute rehabilitation after childhood-
acquired brain injury: A focus on cognitive, behavioral and social domains. American Journal
of Physical Medicine & Rehabilitation, 85, 767–778. doi:10.1097/01.phm.0000233176.08480.22
Anderson, V., Catroppa, C., Morse, S., Haritou, F., & Rosenfeld, J. (2005). Functional plasticity or
vulnerability after early brain injury? Pediatrics, 116, 1374–1382. doi:10.1542/peds.2004-1728
Anderson, V., Northam, E., Hendy, J., & Wrennall, J. (2001). Developmental neuropsychology: A
clinical approach. Hove: Psychological Press.
Anderson, V., Spencer-Smith, M., Coleman, L., Anderson, P., Williams, J., Greenham, M., . . .
Jacobs, R. (2010). Children’s executive functions: Are they poorer after very early brain insult.
Neuropsychologia, 48(7), 2041–2050. doi:10.1016/j.neuropsychologia.2010.03.025
Aram, D. M., & Ekelman, B. L. (1986). Cognitive profiles of children with early onset of
unilateral lesions. Developmental Neuropsychology, 2(3), 155–172. doi:10.1080/
87565648609540339
Aram, D. M., & Eisele, J. A. (1994). Intellectual stability in children with unilateral brain lesions.
Neuropsychologia, 32, 85–95. doi:10.1016/0028-3932(94)90071-X
Australian Bureau of Statistics. (2011). Census of population and housing: Socio-economic indexes
for areas (SEIFA), Australia. Cat. No. 2033.0.55.001.
Ballantyne, A. O., Scarvie, K. M., & Trauner, D. A. (1994). Verbal and performance IQ patterns
in children after perinatal stroke. Developmental Neuropsychology, 10, 39–50. doi:10.1080/
87565649409540565
Ballantyne, A. O., Spilkin, A. M., Hesselink, J., & Trauner, D. A. (2008). Plasticity in the
developing brain: Intellectual, language and academic functions in children with ischaemic
perinatal stroke. Brain, 131, 2975–2985. doi:10.1093/brain/awn176
Ballantyne, A. O., Spilkin, A. M., & Trauner, D. A. (2007). Language outcome after perinatal
stroke: Does side matter? Child Neuropsychology, 13, 494–509. doi:10.1080/
09297040601114878
Banich, M. T., Levine, S. C., Kim, H., & Huttenlocher, P. (1990). The effects of developmental
factors on IQ in hemiplegic children. Neuropsychologia, 28, 35–47. doi:10.1016/0028-3932(90)
90084-2
 CHILD NEUROPSYCHOLOGY 15

Block, G. W., Nanson, J. L., & Lowry, N. J. (1999). Attention, memory, and language after
pediatric ischemic stroke. Child Neuropsychology, 5(2), 81–91. doi:10.1076/chin.5.2.81.3169
Casey, B., Giedd, J., & Thomas, K. (2000). Structural and functional brain development and its
relation to cognitive development. Biological Psychology, 54, 241–257. doi:10.1016/S0301-0511
(00)00058-2
Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2nd ed.). NJ: Laurence
Erlbaum.
Cohen, M. (1997). Children’s Memory Scale. San Antonio, TX: Psychological Corporation.
Cnossen, M., Aarsen, F. K., Van den Akker, S. L. J., Danen, R., Appell, I. M., Steyerberg, E. W., &
Catsman-Berrevoets, C. E. (2010). Paediatric arterial ischaemic stroke: Functional outcome
and risk factors. Developmental Medicine & Child Neurology, 52, 394–399. doi:10.1111/j.1469-
8749.2009.03580.x
Dennis, M. (2000). Developmental plasticity in children: The role of biological risk, development,
time, and reserve. Journal of Communication Disorders, 33, 321–332. doi:10.1016/S0021-9924
(00)00028-9
Dennis, M., Francis, D., Cirino, P., Schachar, R., Barnes, M. A., & Fletcher, J. M. (2009). Why IQ
is not a covariate in cognitive studies of neurodevelopmental disorders. Journal of the
International Neuropsychological Society, 15, 1–13. doi:10.1017/S1355617709090481
deVeber, G., MacGregor, D., Curtis, R., & Mayank, S. (2000). Neurologic outcome in survivors of
childhood arterial ischemic stroke and sinovenous thrombosis. Journal of Child Neurology, 15
(5), 316–324. doi:10.1177/088307380001500508
Elliott, C. D. (1990). Differential Ability Scales. San Antonio, TX: Psychological Corporation.
Elliott, C. D. (2007). Differential Ability Scales – Second Edition (DAS-II). San Antonio, TX:
Psychological Corporation.
Everts, R., Pavlovic, J., Kaufmann, F., Uhlenberg, B., Seidel, U., Nedeltchev, K., . . . Steinlin, M.
(2008). Cognitive functioning, behavior, and quality of life after stroke in childhood. Child
Neuropsychology, 14, 323–338. doi:10.1080/09297040701792383
Ewing-Cobbs, L., Miner, M. E., Fletcher, J. M., & Levin, H. S. (1989). Intellectual, motor, and
language sequelae following closed head injury in infants and preschoolers. Journal of
Pediatric Psychology, 14, 531–547. doi:10.1093/jpepsy/14.4.531
Fuentes, A., Deotto, A., Desrocher, M., deVeber, G., & Westmacott, R. (2016). Determinants of
cognitive outcomes of perinatal and childhood stroke: A review. Child Neuropsychology, 22(1),
1–38. doi:10.1080/09297049.2014.969694
Funnell, E., & Pitchford, N. J. (2010). Reading disorders and weak verbal IQ following left
hemisphere stroke in children: No evidence of compensation. Cortex, 46, 1248–1258.
doi:10.1016/j.cortex.2010.06.013
Galvin, J., Hewish, S., Rice, J., & Mackay, M. T. (2011). Functional outcome following paediatric
stroke. Developmental Neurorehabilitation, 14(2), 67–71. doi:10.3109/17518423.2010.547241
Gioia, G. A., Isquith, P. K., Guy, S. C., & Kenworthy, L. (2000). Behavior Rating Inventory of
Executive Functioning (BRIEF). Odessa, FL: Psychological Assessment Resources.
Hartel, C., Schilling, S., Sperner, J., & Thyen, U. (2004). The clinical outcomes of neonatal and
childhood stroke: Review of the literature and implications for future research. European
Journal of Neurology, 11, 431–438. doi:10.1111/ene.2004.11.issue-7
Hogan, A., Kirkham, F., & Isaacs, E. (2000). Intelligence after stroke in childhood: Review of the
literature and suggestions for future research. Journal of Child Neurology, 15, 325–332.
doi:10.1177/088307380001500509
Jacobson, N. S., & Truax, P. (1991). Clinical significance: A statistical approach to defining
meaningful change in psychotherapy research. Journal of Consulting and Clinical Psychology,
59, 12–19. doi:10.1037/0022-006X.59.1.12
Jacobs, R., Harvey, A. S., & Anderson, V. (2007). Executive function following focal frontal lobe
lesions: Impact of timing of lesion on outcome. Cortex, 43, 792–805. doi:10.1016/S0010-9452
(08)70507-0
Kennard, M. A. (1936). Age and other factors in motor recovery from precentral lesions in
monkeys. American Journal of Physiology, 115, 138–146.
16 I. JACOMB ET AL.

King, A. A., DeBaun, M. R., & White, D. A. (2008). Need for cognitive rehabilitation for children
with sickle cell disease and strokes. Expert Review of Neurotherapeutics, 8(2), 291–296.
doi:10.1586/14737175.8.2.291
Kolb, B., & Whishaw, I. (1996). Fundamentals of human neuropsychology (4th ed.). New York,
NY: W.H. Freeman and Company.
Lansing, A., Max, J. E., Delis, D. C., Fox, P. T., Lancaster, J., Manes, F. F., & Schatz, A. (2004).
Verbal learning and memory after childhood stroke. Journal of the International
Neuropsychological Society, 10(5), 742–752. doi:10.1017/S1355617704105122
Lanthier, S., Carmant, L., Larbrisseau, A., & deVeber, G. (2000). Stroke in children: The
coexistence of multiple risk factors predicts poor outcome. Neurology, 54, 371–378.
doi:10.1212/WNL.54.2.371
Leventer, R., Phelan, E. M., Coleman, L. T., Kean, M. J., Jackson, G. D., & Harvey, A. S. (1999).
Clinical and imaging features of cortical malformations in childhood. Neurology, 53(4), 715–
722. doi:10.1212/WNL.53.4.715
Levine, S. C., Kraus, R., Alexander, E., Suriyakaham, L. W., & Huttenlocher, P. R. (2005). IQ
decline following early unilateral brain injury: A longitudinal study. Brain and Cognition, 59,
114–123. doi:10.1016/j.bandc.2005.05.008
Long, B., Anderson, V., Jacobs, R., Mackay, M., Leventer, R., Barnes, C., & Spencer-Smith, M.
(2011). Executive function following child stroke: The impact of lesion size. Developmental
Neuropsychology, 36(8), 971–987. doi:10.1080/87565641.2011.581537
Manly, T., Robertson, I., Anderson, V., & Nimmo-Smith, I. (1999). Test of Everyday Attention for
Children. Cambridge: Thames Valley Test Company.
Max, J. E. (2004). Effect of side of lesion on neuropsychological performance in childhood stroke.
Journal of the International Neuropsychological Society, 10(5), 698–708. doi:10.1017/
S1355617704105092
Max, J. E., Bruce, M., Keatley, E., & Delis, D. (2010). Pediatric stroke: Plasticity, vulnerability, and
age of lesion onset. The Journal of Neuropsychiatry and Clinical Neurosciences, 22(1), 30–39.
doi:10.1176/jnp.2010.22.1.30
Max, J. E., Manes, F. F., Robertson, B., Mathews, K., Fox, P. T., & Lancaster, J. L. (2005).
Prefrontal and executive attention network lesions and the development of attention-deficit/
hyperactivity symptomatology. Journal of the American Academy of Child & Adolescent
Psychiatry, 44(5), 443–450. doi:10.1097/01.chi.0000156661.38576.0f
Max, J. E., Mathews, K., Lansing, A., Robertson, B., Fox, P. T., Lancaster, J. L., . . . Smith, J.
(2002). Psychiatric disorders after childhood stroke. Journal of the American Academy of Child
& Adolescent Psychiatry, 41(5), 555–562. doi:10.1097/00004583-200205000-00013
Max, J. E., Mathews, K., Manes, F. F., Robertson, B., Fox, P. T., Lancaster, J. L., . . . Collings, N.
(2003). Attention deficity hyperactivity disorder and neurocognitive correlates after childhood
stroke. Journal of the International Neuropsychological Society, 9, 815–829. doi:10.1017/
S1355617703960012
Max, J. E., Robin, D. A., Taylor, H. G., Yeates, K. O., Fox, P. T., Lancaster, J. L., . . . Austermann,
S. (2004). Attention function after childhood stroke. Journal of the International
Neuropsychological Society, 10(7), 976–986. doi:10.1017/S1355617704107066
Mosch, S. C., Max, J. E., & Tranel, D. (2005). A matched lesion analysis of childhood versus
adult-onset brain injury due to unilateral stroke: Another perspective on neural plasticity and
recovery of social functioning. Cognitive and Behavioral Neurology, 18(1), 5–17. doi:10.1097/
01.wnn.0000152207.80819.3c
Muter, V., Taylor, S., & Vargha-Khadem, F. (1997). A longitudinal study of early intellectual
development in hemiplegic children. Neuropsychologia, 35, 289–298. doi:10.1016/S0028-3932
(96)00079-6
O’Keeffe, F., Ganesan, V., King, J., & Murphy, T. (2012). Quality-of-life and psychosocial out-
come following childhood arterial ischaemic stroke. Brain Injury, 26(9), 1072–1083.
doi:10.3109/02699052.2012.661117
 CHILD NEUROPSYCHOLOGY 17

Pavlovic, J., Kaufmann, F., Boltshauser, E., Capone Mori, A., Gubser Mercati, D., Haenggeli, C.,
. . . Ramelli, G. (2006). Neuropsychological problems after paediatric stroke: Two year follow-
up of Swiss children. Neuropediatrics, 37(1), 13–19. doi:10.1055/s-2006-923932
Rabipour, S., & Raz, A. (2012). Training the brain: Fact and fad in cognitive and behavioral
remediation. Brain & Cognition, 79, 159–179. doi:10.1016/j.bandc.2012.02.006
Roach, S. E. (2000). Etiology of stroke in children. Seminars in Pediatric Neurology, 7(4), 244–
260. doi:10.1053/spen.2000.20078
Schatz, J., Craft, S., Koby, M., & DeBaun, M. R. (2004). Asymmetries in visual-spatial
processing following childhood stroke. Neuropsychology, 18(2), 340–352. doi:10.1037/
0894-4105.18.2.340
Schatz, J., Craft, S., Koby, M., Siegel, M. J., Resar, L., Lee, R. R., . . . DeBaun, M. R. (1999).
Neuropsychologic deficits in children with sickle cell disease and cerebral infarction: Role of
lesion site and volume. Child Neuropsychology, 5(2), 92–103. doi:10.1076/chin.5.2.92.3170
Steinlin, M., Roellin, K., & Schroth, G. (2004). Long-term follow-up after stroke in childhood.
European Journal of Pediatrics, 163, 245–250. doi:10.1007/s00431-003-1357-x
Studer, M., Bolsthauser, E., Capone Mori, A., Datta, A., Fluss, J., Mercati, D., . . . Steinlin, M.
(2014). Factors affecting cognitive outcome in early pediatric stroke. Neurology, 82(9), 784–
792. doi:10.1212/WNL.0000000000000162
Trauner, D. A., Chase, C., Walker, P., & Wulfeck, B. (1993). Neurologic profiles of infants and
children after perinatal stroke. Pediatric Neurology, 9, 383–386. doi:10.1016/0887-8994(93)
90107-N
Trauner, D. A., Nass, R., & Ballantyne, A. O. (2001). Behavioural profiles of children and
adolescents after pre- or perinatal unilateral brain damage. Brain, 124, 995–1002.
doi:10.1093/brain/124.5.995
Warrington, E. K., James, M., & Maciejewski, C. (1986). The WAIS as a lateralizing and
localizing diagnostic instrument: A study of 656 patients with unilateral cerebral lesions.
Neuropsychologia, 24, 223–239. doi:10.1016/0028-3932(86)90055-2
Wechsler, D. (1989). Wechsler Preschool and Primary Scale of Intelligence – Revised (WPPSI-R).
San Antonio, TX: Psychological Corporation.
Wechsler, D. (1997a). Wechsler Adult Intelligence Scale – Third Edition (WAIS-III). San Antonio,
TX: Psychological Corporation.
Wechsler, D. (1997b). Wechsler Memory Scale – Third Edition (WMS-III). San Antonio, TX:
Psychological Corporation.
Wechsler, D. (2004). Wechsler Preschool and Primary Scale of Intelligence – Third Edition
(WPPSI-III). San Antonio, TX: Psychological Corporation.
Wechsler, D. (2005a). Wechsler Individual Achievement Test – Second Edition (WIAT-II). San
Antonio, TX: Psychological Corporation.
Wechsler, D. (2005b). Wechsler Intelligence Scale for Children – Fourth Edition (WISC-IV). San
Antonio, TX: Psychological Corporation.
Wechsler, D. (2008). Wechsler Adult Intelligence Scale – Fourth Edition (WAIS-IV). San Antonio,
TX: Psychological Corporation.
Wechsler, D. (2009). Wechsler Memory Scale – Fourth Edition (WMS-IV). San Antonio, TX:
Psychological Corporation.
Westmacott, R., Askalan, R., MacGregor, D., Anderson, P., & deVeber, G. (2010). Cognitive
outcome following unilateral arterial ischaemic stroke in childhood: Effects of age at stroke
and lesion location. Developmental Medicine & Child Neurology, 52(4), 386–393. doi:10.1111/
dmcn.2010.52.issue-4
Westmacott, R., MacGregor, D., Askalan, R., & deVeber, G. (2009). Late emergence of cognitive
deficits after unilateral neonatal stroke. Stroke, 40(6), 2012–2019. doi:10.1161/
STROKEAHA.108.533976