CognCognitive reserve in paediatric traumatic brain injury.pditive Reserve in Paediatric Traumatic Brain Injury

Brain Injury, July 2010; 24(7–8): 995–1002

ORIGINAL ARTICLE

Cognitive reserve in paediatric traumatic brain injury: Relationship
with neuropsychological outcome

AMANDA FUENTES1, CHERISSE MCKAY2, & CHRISTINA HAY2
1

York University, Toronto, Ontario, Canada and 2Bloorview Kids Rehab, Toronto, Ontario, Canada

(Received 2 September 2009; revised 7 April 2010; accepted 26 April 2010)

Abstract
Primary objective: The current study examined the relationship between neuropsychological performance and cognitive
reserve (as measured by word reading and vocabulary tasks) in children with TBI.
Research design: Retrospective records analysis of the neuropsychological test results of 52 participants with medically
documented traumatic brain injuries, ranging from 6–16 years of age.
Main outcome and results: Indicators of cognitive reserve were not correlated with the majority of well-recognized
neuropsychological measures.
Conclusions: Although past research has found that verbal ability is a valid indicator of CR in adult populations, the present
study found evidence against the validity of this traditional reserve proxy when applied to the paediatric population. These
findings suggest one of two conclusions: (1) measures used to indicate CR in adult populations (word reading, vocabulary)
are not valid indicators of cognitive reserve in paediatric populations; and/or (2) the measures themselves are valid, yet there
is simply not a significant relationship between cognitive reserve and short-term (i.e. less than 6 months) neuropsychological
outcome in paediatric TBI.
Keywords: Traumatic brain injury, Pediatric, Cognitive reserve

Introduction
A rising amount of research has explored cognitive
reserve (CR) in individuals with neurological conditions as it has proven to be a significant factor in
estimating the degree of resulting cognitive impairment. Few studies have investigated cognitive
reserve in paediatric populations, despite the high
incidence of traumatic brain injuries (TBIs) in
children and adolescents. Cognitive reserve has
been defined as ‘the discrepancy between the
degree of pathology and the degree of functional
impairment evidenced across individuals with the
same disorder’ ([1], p. 131). This concept is measured indirectly by proxies such as pre-injury cognitive ability, post-injury intellectual and academic
functioning, socioeconomic status, family function
and level of education (in adults) [2]. The hypothesis

that cognitive reserve is a moderator of the effects of
TBI is consistent with the recurring clinical observation that there does not appear to be a direct link
between the degree of brain pathology and level
of resulting cognitive impairment across individuals [3]. Variability in neuropsychological outcome
appears to be related to CR differences stemming
from discrepancies in education, occupation, social
economic status and genetics.
Evidence of reserve can be observed by studying
individuals that have sustained pathological insult,
such as a traumatic brain injury (TBI). Bigler [4]
points out that the functioning of the brain at the time
of injury is a crucial factor in determining the overall
impact of the insult. Essentially, the recovery process
after TBI relies heavily on the brain’s reserve capacity
to endure the insult and then to repair itself [3]. This
notion is supported by the study conducted by

Correspondence: Amanda Fuentes, York University, Toronto, Ontario M3J 1P3, Canada. Tel: 647-293-4255. E-mail: [email protected]
ISSN 0269–9052 print/ISSN 1362–301X online ß 2010 Informa Healthcare Ltd.
DOI: 10.3109/02699052.2010.489791

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A. Fuentes et al.

Kesler et al. [5], which examined pre-injury and postinjury cognitive status of adult TBI survivors. In this
study, scores from standardized academic testing
were used as an index of pre-morbid ability and then
compared to post-injury IQ scores. In conjunction
with the reserve hypothesis, the findings illustrated
that individuals with lower pre-morbid academic
ability showed greater vulnerability to the impact of
the brain injury [5]. The concept of reserve also
comes into play later in the lifespan after TBI, as
survivors have shown an increased risk of developing
psychiatric and neurodegenerative disorders [3, 5].
In this way, brain injury is viewed as a risk factor that
decreases reserve and, as such, increases vulnerability
for the onset of dementia.
Similarly, developmental research has shown that
CR is an important moderator of outcomes following
TBI in children [6, 7]. For example, Fay et al. [6]
investigated post-insult cognitive ability as a proxy of
cognitive reserve to predict outcome after childhood
mild TBI. Fay et al. [6] hypothesized that cognitive
reserve would moderate the occurrence of postconcussive symptoms attributable to mild TBI, such
that outcome would be poorer among children of
lower cognitive ability than higher cognitive ability
(as assessed by a battery of standardized tests
administered within 3 weeks post-injury).
Cognitive ability for each child was represented by
a single overall composite score, which was determined by computing the mean standard score across
a variety of cognitive tests. Post-concussive symptoms were assessed using the Post-concussive
Symptom Interview (PCS-I) and the Health and
Behaviour Inventory (HBI). Hierarchical linear
modelling revealed that children with lower cognitive
reserve capacity and complicated mild TBI showed
greater vulnerability to the development of postconcussive symptoms than children with higher
cognitive reserve capacity. Thus, the results suggested that outcome was moderated jointly by CR
and injury severity. In a study that illustrated the
influence of pre-injury abilities on outcomes following childhood brain insult, Farmer et al. [7] examined memory functioning in children with varying
degrees of brain insult who did or did not have
previously identified learning problems. Children
with prior learning difficulties performed significantly worse on measures of memory functioning
compared to their peers with no prior learning
problems. These results were consistent with the
hypothesis that pre-injury learning problems moderated the effects of TBI. Interestingly, children with
prior learning problems demonstrated more cognitive weaknesses even when severity of injury and age
factors were held constant. Hence, the variability in
neuropsychological outcomes of childhood TBI may
be explained in terms of differences in levels of CR.

Studies of neuropsychological outcome of childhood TBI highlight developmental factors that
interact with pre-injury cognitive ability to define
long-term recovery of brain insult. There is clear
evidence that an earlier age at injury is more
detrimental to outcome than an injury suffered at
an older age. To illustrate, greater vulnerability for
difficulties in language, intelligence and motor skills
are reported in children injured before 5 years of
age [8]. Additionally, younger children with TBI
demonstrate a longer recovery interval [8]. Dennis
et al. [2] suggest that injury to the immature brain
adversely affects the development of cognitive skills.
In this way, earlier age at injury diminishes CR by
preventing the child from acquiring efficient
cognitive strategies that may have otherwise been
recruited to maintain function after brain insult [2].
Clearly, these empirical findings support the theory
that brain injury affects the adult brain differently
than the child brain. The relationship between CR
and neuropsychological outcome would also be
expected to differ since children have had less time
to develop such reserve. As such, it remains unclear
whether the measures used to assess cognitive
reserve in adult populations would be reliable and
valid indicators in a paediatric population.
An accurate estimation of pre-morbid cognitive
functioning is a crucial step in interpreting neuropsychological assessments [9]. In an attempt to
accomplish this goal, many researchers have utilized
past achievement information such as standardized
tests (e.g. IQ tests, aptitudes tests, the Graduate
Record Examination, etc.) [9]. However, this
method of estimation is limited by the lack of
availability of this information. Other variables
thought to represent reserve include indirect achievement information, such as grade point average, level
of educational attainment and occupation [10]. Premorbid ability has also been inferred by examining
measurements of neural activity and brain size [10].
However, Dennis et al. [2] point out that this
methodology is generally not employed with children
because head and brain size change throughout
development. Demographic regression estimation
methodology has also been employed to predict
scores, but has proven to be ineffective in providing
accurate estimates of individuals [11].
Finally, a useful alternative approach of estimation
employs what is referred to as ‘hold’ tests. This
method relies on the assessment of abilities that are
considered to be stable and resistant to brain
damage [11]. It has been suggested that verbal ability
represents a ‘hold’ measure because of its relative
resistance to cerebral insult [12]. Hence, verbal
ability constitutes a measure of crystallized intelligence. Manly et al. [13] support the significance of
literacy level as a means of measuring reserve by

Cognitive reserve in paediatric TBI
affirming that ‘literacy measures educational experience more accurately than years of education, and
thus is a superior assessment of the knowledge,
strategy, and skills needed to perform well on
traditional neuropsychological tasks’ (p. 227). As a
result, various standardized reading tests have been
shown to be valid indicators of pre-injury functioning
and cognitive reserve, including the Wide Range
Achievement Test-Third Edition (WRAT-3) [14]
and the North American Adult Reading Test
(NAART) [15]. The Wechsler Adult Intelligence
Scale (WAIS) and its subsequent revisions (including
the current WAIS-III) have also been viewed as a
hold measure [11]. Vanderploeg et al. [9] reported
that the Information and Vocabulary sub-tests were
the most accurate indicator of reserve. Ruff et al. [16]
also investigated vocabulary as a predictor of functional outcome following head trauma in a severe
group between 12–65 years and found that intact
vocabulary was associated with return to work/
school.
Past studies have documented mixed evidence for
the usefulness of verbal ability as an estimator of
cognitive reserve in children. Chapman and
McKinnon [8] examined 400 children with severe
closed head injuries and found that recovery of basic
language skills, vocabulary and syntactic abilities
occurred during the first 3 months post-injury,
regardless of age at insult. Chapman and
McKinnon [8] suggested that the recovery of
‘higher-order’ language functions (such as semantics, syntax, etc.) may be accomplished through the
brain’s ability to compensate for early injuries using
the recruitment of new nerve cells. Conversely, other
researchers have reported that literacy is particularly
vulnerable following childhood TBI [17].
Specifically, children with early head injuries
(before 6.5 years of age) perform more poorly on
standardized tests of reading than children with
similar injuries suffered at an older age [17]. Barnes
et al. [17] suggested that a head injury sustained
before formal reading instruction constitutes a significant risk factor for difficulties in acquiring basic
reading skills. In this way, age at injury was proposed
to primarily affect the acquisition of new skills [17].
Catroppa et al. [18] investigated the development of
reading skills post-TBI, from time of injury to
7 years post-injury, in a mild-to-severe group injured
between 3–12 years. Their results showed that
reading ability was more compromised in children
injured between 3–7 years of age than in children
injured between 8–12 years. Thus, past research has
identified reading difficulties following TBI in preschool or early primary grades, however, little is
known regarding the resilience of these skills following TBI in older childhood.

997

In summary, past evidence indicates that the
picture of post-injury literacy skills as a proxy of
CR is not straightforward because recovery after
brain injury relies on the developmental stage of the
individual at the time of injury. Within the context of
TBI, both literacy and hold tests have become well
recognized as indicators of pre-morbid functioning
within adult populations. Although past studies have
demonstrated recovery of language functions in
older children, children injured at a younger age
have been reported to have persisting literacy difficulties [8, 17]. At the same time, injury severity does
not account for all variance in cognitive outcome, as
researchers have reported only modest contributions
of traditional indices of severity (such as GCS
ratings) to neuropsychological performance postinjury [2, 3, 8]. Given the importance of identifying
children who are at risk for negative outcomes
following TBI, research must address whether literacy tests are indeed valid estimates of cognitive
reserve in children. Since previous studies have
found that literacy skills in children who have
sustained an injury before 6.5 years are vulnerable
to such injuries, only children 6 years old or older
were used in this study. The overall purpose of this
study is to examine cognitive reserve in paediatric
brain injury and its relation to neuropsychological
outcome. Specifically, it will examine (a) if the
relationship between cognitive and neuropsychological outcome observed in adult TBI translates to
paediatric populations and (b) if well recognized
indicators of cognitive reserve, such as hold tests and
literacy tasks, are valid indicators in paediatric
populations. To determine the possible efficacy of
these hold tests, they will be compared to a wellrecognized injury severity indicator, the Glasgow
Coma Scale (GCS) to see if cognitive reserve relates
to neuropsychological outcome as well, or better
than, injury severity itself.

Method
Participants
The data used in this study consisted of 52 TBI cases
3–6 months post-injury, meeting certain inclusion/
exclusion criteria, referred to the neuropsychology
service of a non-acute paediatric inpatient/daypatient
neurorehabilitation hospital located in a large urban
area in Canada. This hospital serves as the primary
rehabilitation hospital for the province of Ontario
and thus individuals were residents of a wide variety
of urban and rural areas across the province.
Inclusion criteria required a medically documented
history of TBI, age between 6–16, current need for
neuropsychological assessment and conventional
medical signs of brain injury (e.g. loss of

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A. Fuentes et al.
Table I. Demographic characteristics of the TBI
sample (n ¼ 52).

Table II. Injury characteristics of traumatic brain
injury (TBI) participants (n ¼ 52).

Count (%)
Age
Mean (SD)
Range
Gender
Male
Female
Handed dominance
Right
Left
Unknown

11.81 (3.13)
6–16
34 (65)
18 (35)
43 (83)
4 (8)
5 (9)

consciousness and post-traumatic amnesia) documented in the medical record. Exclusion criteria
included history of pre-morbid developmental disability, learning disability, autism spectrum disorder,
attention deficit disorder or any other neurological
impairment or disorder (e.g. seizure disorder, previous TBI, etc.). Data was also excluded for cases in
which English was a second language, if the primary
cognitive reserve measures (see Materials section)
were not administered or when the results of the
assessment were determined to be either invalid or
unreliable by the treating neuropsychologist (as
documented in the neuropsychological report) secondary to inconsistent or questionable motivation
and/or effort.
In terms of demographic variables, the group was
comprised of 34 males and 18 females, with an
average age of 11.81 years (ranging again from
6–16). The large majority of the children were right
handed (83%). A more detailed description of
demographic characteristics of the group is presented in Table I.
Overall, the group consisted of predominantly
moderate-to-severe brain injuries (see Table II).
Specifically, admission Glasgow Coma Scale (GCS)
[14] was indicative of moderate or severe degree of
brain injury (513) in 70% of the cases. Fifty of 52
cases revealed cerebral insult on neuroimaging, even
those rated as mild severity according to the GCS. In
fact, of the 15 cases of mild brain injury (as defined
by a GCS score of 13 or greater), 14 of them had
positive neuroimaging. Diffuse axonal injury was
reported in 27% of cases. In the 50 cases in which
medical records included information regarding
post-injury seizure activity, 42 of them did not
have any documented seizure activity.
Materials
The dependent measures in this study were derived
from a variety of neuropsychological measures.
Cognitive reserve was measured using the Word

Count (%)
Cause of head trauma
MVA (car only)
MVA w/pedestrian or bike
Bike/recreation
Fall
Boating
Other
ER Admission GSC
Severe (3–8)
Moderate (9–12)
Mild (13–15)
Unknown
Neuroimaging
Positive
Negative
Laterality
Left
Right
Bilateral
Unknown
Lobes
Frontal
Multiple
Other
Unknown
Diffuse Axonal Injury
Positive
Negative
Unknown
Seizure
Negative
Positive
Unknown

24
15
5
2
2
4

(46)
(29)
(10)
(4)
(4)
(8)

25
10
15
2

(48)
(19)
(29)
(4)

50 (96)
2 (4)
13
11
21
7

(25)
(21)
(40)
(14)

14
26
6
6

(27)
(50)
(12)
(12)

14 (27)
37 (71)
1 (2)
42 (81)
8 (15)
2 (4)

MVA ¼ Motor vehicle accident; GCS ¼ Glasgow
Coma Scale.

Reading sub-test of the Wechsler Individual
Achievement Test-Second Edition (WIAT-II) [15]
and the Vocabulary sub-test of the Wechsler
Intelligence Scale for Children-Fourth Edition
(WISC-IV) [16]. Although there has not been
any direct research examining the WISC-IV and
WIAT-II as indicators of pre-morbid functioning,
they were chosen based on the aforementioned
literature that used comparable indices of literacy
and vocabulary knowledge (e.g. WRAT-3,
WAIS-III) as indicators of pre-injury functioning in
adult TBI populations [8, 10]. The neuropsychological measures used in this study were those commonly used as part of the neuropsychological battery
assessing the following cognitive domains: sustained
and divided attention (Test of Everyday Attention for
Children (TEA-Ch): Sky Search Attention Scaled
Score (visual scanning and attention), Score
Scaled Score (sustained auditory attention), Sky
Search Dual Task Decrement Scaled Score (multimodal divided attention) and Score Dual Task Score

Cognitive reserve in paediatric TBI

999

Table III. Pearson correlations (r2) between neuropsychological measures and WIAT-II word reading, WISC-IV vocabulary
and GCS (respective sample sizes contained in brackets).

Measure
TEA-Ch
Sky search scaled score
Score scaled score
Sky search DT scaled score
Score DT scaled score
CVLT-C List A Total T-score
RCFT
Immediate T-score
Delay T-score
WISC-IV
PSI
Coding scaled score
Symbol search scaled score
WCST # correct raw score
CCT Total T-score

WIAT-II Word Reading
r2 (n)

0.138
0.108
0.388
0.449
0.225

(36)
(36)
(36)*
(36)**
(41)

WISC-IV Vocabulary
r2 (n)

0.025
0.050
0.053
0.261
0.295

(46)
(46)
(46)
(45)
(48)*

Glasgow Coma Scale (GCS)
r2 (n)

0.124
0.062
0.299
0.497
0.253

(44)
(44)
(44)*
(43)**
(46)

0.138 (33)
0.061 (33)

0.238 (37)
0.220 (37)

0.129 (36)
0.140 (36)

0.261
0.227
0.302
0.093
0.270

0.141
0.140
0.166
0.054
0.229

0.431
0.379
0.418
0.141
0.313

(42)
(42)
(42)
(41)
(40)

(52)
(52)
(52)
(49)
(47)

(50)**
(50)**
(50)**
(47)
(45)*

*p50.05; **p50.0, DT ¼ Dual task/decrement score.

(unimodal divided attention)) [17], visual-motor
processing speed (WISC-IV Processing Speed
Index score, Digit Symbol Coding Scaled Score
and Symbol Search Scaled Score) [16], learning and
memory (California Verbal Learning TestChildren’s version (CVLT-C) List A Total T-score
[18]; Rey Complex Figure Test (RCFT) Immediate
Recall T-score and Delayed Recall T-score) [19] and
executive functioning (Wisconsin Card Sorting Test
(WCST) Total Correct Raw Score [20]; Children’s
Category Test (CCT) Total T-score) [21].

Results
To determine if there was a relationship between
pre-morbid functioning (as measured by the
WIAT-II Word Reading and WISC-IV Vocabulary
scores) and neuropsychological outcome, Pearson
correlations were used. Neither the WIAT-II Word
Reading nor WISC-IV Vocabulary scaled scores
were significantly correlated to the majority of the
neuropsychological measures (see Table III).
In terms of WIAT-II Word Reading performance,
it was only significantly correlated with the divided
attention measures (i.e. Dual Task scores) of the
TEA-Ch. It was not significantly correlated with any
of the measures related to visual-motor processing
speed, memory, basic attention or executive
functioning. Similarly, WISC-IV Vocabulary performance failed to relate to any of the neuropsychological measures, with the exception of verbal learning
and memory (CVLT-C List A Total T-score). Injury
severity, as measured by GCS score, was correlated
with measures of divided attention (TEA-Ch Sky
Search DT and Score DT) and processing speed

(WISC-IV Processing Speed Index, Coding sub-test
and Symbol Search sub-test). Since neither of the
cognitive reserve variables were significantly correlated to the neuropsychological outcome measures,
regressional analyses were not conducted.

Discussion
The objective of the current study was to determine
the utility of reading and vocabulary tests as
measures of pre-morbid ability for children with
TBI. Specifically, two main research questions were
posed: (1) does the relationship between cognitive
and neuropsychological outcome observed in adult
TBI translate to paediatric populations?; and (b) Do
well recognized indicators of cognitive reserve, such
as hold tests and literacy tasks, remain valid indicators in paediatric populations? Overall, the findings
showed that neither reading ability (WIAT-II Word
Reading sub-test score) nor vocabulary skills
(WISC-IV Vocabulary sub-test score) were related
to levels of neurocognitive functioning following
TBI, with the exception of isolated divided attention
tasks. In comparison, moderate correlations were
found between Glasgow Coma Score (GCS) and
neuropsychological measures of divided attention
and processing speed, indicating that severity of
injury still serves as a modestly stronger, yet still
unreliable, predictor of neuropsychological outcome.
Taken together, these findings suggest that the
moderating effect of cognitive ability on neuropsychological outcome in adult TBI may not directly
apply to the paediatric population. Consequently,
the results provide evidence against the validity
of the traditional reserve proxy of reading

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A. Fuentes et al.

ability/vocabulary when applied to the paediatric
population.
The current pattern of findings is inconsistent
with the threshold theory of cognitive reserve
described by Stern [3]. According to the threshold
theory, individuals with higher cognitive reserve are
somewhat protected from the effects of brain pathology, as they must sustain higher levels of pathology
before performance is affected [3]. In this study,
there was no relationship between neuropsychological outcome following TBI and cognitive reserve (as
measured by verbal ability). The lack of association
between pre-morbid cognitive ability and outcomes
following childhood TBI is somewhat surprising,
given that previous research has suggested that lower
CR is a significant risk factor for poorer neuropsychological outcome in both children and adults
[5–7]. The failure of this study to find a relation
between CR in children and neuropsychological
outcome following TBI may be due to the fact that
verbal ability was used as an indicator of CR. To the
authors’ knowledge, the current study is the first to
assess the relationship between pre-morbid verbal
ability and subsequent neuropsychological outcomes
following TBI in children. It may be the case that a
child’s level of CR is not synonymous with their
reading abilities and vocabulary knowledge. In other
words, vocabulary and reading may not be stable,
crystallized measures in children as they are in
adults. This would serve to undermine the effectiveness of reading and vocabulary abilities as
pre-morbid predictors because they would not be
resilient to the adverse effects of TBI. This conclusion is supported by past research describing the
comparability of a pure demographic approach with
the hold test prediction method in children [9]. The
active model [3] of CR is grounded in the notion
that the brain actively attempts to compensate for
the disruption represented by TBI by utilizing preexisting cognitive processing strategies. However, as
previously suggested by others [4], these cognitive
abilities may not be fully developed in children at the
time of cerebral insult. Consequently, children may
lack the cognitive strategies that are necessary to
counter against the damaging effects of TBI. Hence,
developmental factors may exert a significant influence on cognitive functioning after TBI by rendering
the child less capable of responding to the challenge
of TBI. This implication is supported by a number
of studies demonstrating that early age at insult is
associated with more detrimental and persisting
effects in a number of cognitive domains [28–30].
In particular, previous research has documented
clear evidence that childhood TBI represents a risk
factor for difficulties in acquiring basic word decoding skills [17]. This observation is particularly

relevant to the present study, given that the mean
age of participants was 11.8 years (range ¼ 6–16).
Alternatively, it may be the case that the levels of
performance exhibited by children on verbal measures do reflect crystallized abilities (and are therefore
accurate markers of CR), but simply went undetected
in the current study. This explanation is supported by
previous research reporting the resilience of verbal
abilities to the impact of brain pathology in childhood
TBI [8]. For example, the results from this study
differ from the findings of Chapman and McKinnon
[8], who observed good recovery of basic language,
vocabulary and syntactic abilities in children with
severe head injuries 3 months post-injury. The
differing results may be due to the fact that the
Chapman and McKinnon [8] study used a sample of
400 children, whereas the current study examined a
small sample of children (n ¼ 52). The use of a small
sample size may have limited the power of the current
study to detect effects of CR. Finally, it remains
possible that the laterality of the damage from the
head injury may have affected reading and vocabulary
skills (and may have therefore influenced CR). For
example, Barnes et al. [17] observed that poorer
reading was associated with contusions involving the
left side of the brain. Once again, there was an
insufficient number of participants to provide information on the relation between laterality and CR, as
measured by reading and vocabulary.
Several caveats to the present study must be noted.
First, an inherent weakness exists in the task of
developing pre-morbid prediction strategies in clinical samples. Clearly, the best way to determine preinjury functioning is to have completed baseline
neuropsychological testing to which post-injury test
scores can be directly compared. However, accurate
measures of pre-morbid ability (such as standardized
test data) are typically not present and were not
available in the clinical sample of the present study
either. Nevertheless, it remains suggested that only
fluid skills are likely to be impacted by the negative
effects of TBI, while crystallized abilities should be
resistant to these effects [12]. Given that vocabulary
and reading are considered to be crystallized abilities,
they were expected to be minimally affected by brain
pathology and were therefore utilized to estimate
overall levels of pre-morbid cognitive function.
Although a number of past studies have validated
this ‘hold’ test approach in pre-morbid estimation for
adults [9–11], brain damage may have affected
similar verbal hold measures in children, indicating
the influence of developmental factors. A shortcoming of the present study is that it was not possible to
control for important differences in brain recovery
that may have been present among participants due
to the confounding variable of developmental plasticity. For example, past studies have also reported

Cognitive reserve in paediatric TBI
that level of education is predictive of outcome
following TBI [5]. This raises a difficulty for the
current study, as younger participants may have been
more vulnerable to the functional impact of TBI due
to their reduced number of years of education and
less stabilized reserve. Further, it could be argued
that a more accurate and possibly more clinically
meaningful approach to assessing pre-morbid ability
would be to examine the differences in neuropsychological outcomes between high- and low-reserve
groups. However, due to the small number of
participants (n ¼ 52) there was no clear way of
developing cut-off requirements that would serve to
accurately divide participants into clinically meaningful groups. Finally, given the moderating effect of
age at onset of TBI and developmental plasticity, it
could also be argued that a better understanding of
CR in children would have been achieved by dividing
the participants into age groups. Again, this was not
possible due to the small sample size.
In summary, the absence of any significant correlations between the Verbal IQ measures and neuropsychological scores post-injury suggests that these
abilities are not valid indicators of cognitive reserve
in the paediatric TBI population. This finding
emphasizes the importance of developing an integrated approach to studying how the neuropsychological outcome of childhood TBI is mediated by
CR. In turn, this will help to explain the indirect link
that has been reported between severity of insult and
clinical outcome. Developing a more comprehensive
interpretation of the outcome of brain injuries in
children requires teasing apart the components that
underlie the recovery process of TBI in early life.
Given that the current measures may not be valid
indicators of CR, then it is important to determine
which measures are valid indicators in paediatric
populations. Given what is known about the adult
literature, it is possible that socio-economic status
(SES) would be related to recovery and outcome. As
such, it is possible that parental education levels may
be predictive of childhood outcome more so than a
child’s educational abilities like reading and vocabulary [31, 32]. In order to define key areas of family
function that may serve as useful proxies of CR,
future studies should investigate associations
between parental unemployment, parental conflict
and parent mental health and neurocognitive outcomes. To this end, research examining the differential outcomes of high- and low-reserve children
and high- and low-reserve parents will prove to be
useful in determining whether or not children with
similar levels of neuropathology experience similar
levels of impairment. Similarly, in order to gain
further insight regarding the meaning of age at onset
of TBI and the effects for reading and vocabulary
skills, it would be important to investigate

1001

differential outcomes among younger and older
children. Advances in paediatric neuroimaging provide the opportunity to investigate possible differences in neural processing that may exist between
high- and low-reserve children and between younger
and older children. Recent research of cognitive
function in children survivors of TBI has demonstrated that neuropsychological outcome is also
moderated by time since onset of CNS insult [33].
For example, even when severity of head injury is
held constant, younger children have been observed
to show a slower rate of recovery over time [33].
Longitudinal studies of cognitive function of children survivors of TBI may therefore prove useful in
providing a more comprehensive view of development post-injury. The mental health of the child may
also serve to buffer or compromise neuropsychological outcome post-insult. Hence, it would be useful
to explore the association between outcome and preinjury or post-injury psychiatric disorders in children. Ultimately, the findings reported in the present
study support the current conception of CR as a
dynamic process that is modifiable at different stages
of the lifespan [10].

Declaration of interest: The authors report no
conflict of interest. The authors alone are responsible for the content and writing of the paper.

References
1. Bieliaukas LA, Antonucci A. The impact of cognitive reserve
on neuropsychological measures in clinical trials. In: Stern Y,
editor. Cognitive Reserve: Theory and Applications.
New York: Taylor & Francis; 2007. p 131–142.
2. Dennis M, Yeates KO, Taylor HG, Fletcher JM. Brain reserve
capacity, cognitive reserve capacity, and age-based functional
plasticity after congenital and acquired brain injury in children.
In: Stern Y, editor. Cognitive Reserve: Theory and
Applications. New York: Taylor & Francis; 2007. p 53–84.
3. Stern Y. The concept of cognitive reserve: A catalyst for
research. In: Stern Y, editor. Cognitive Reserve: Theory and
Applications. New York: Taylor & Francis; 2007. p 1–4.
4. Bigler ED. Traumatic brain injury and cognitive reserve. In:
Stern Y, editor. Cognitive Reserve: Theory and Applications.
New York: Taylor & Francis; 2007. p 85–116.
5. Kesler SB, Adams HF, Blasey CM, Bigler ED. Premorbid
intellectual functioning, education, and brain size in traumatic
brain injury: An investigation of the cognitive reserve hypothesis. Applied Neuropsychology 2003;10:153–162.
6. Fay TB, Yeates KO, Taylor HG, Bangert B, Dietrich A,
Nuss KE, Rusin J, Wright M. Cognitive reserve as a moderator
of postcuncussive symptoms in children with complicated and
uncomplicated mild traumatic brain injury. Journal of the
International Neuropsychological Society 2010;16:94–105.
7. Farmer JE, Kanne SM, Haut JS, Williams J, Johnstone B,
Kirk K. Memory functioning following traumatic brain injury
in children with premorbid learning problems. Developmental
Neuropsychology 2002;22:455–469.

1002

A. Fuentes et al.

8. Chapman SB, McKinnon L. Discussion of developmental
plasticity: Factors affecting cognitive outcome after pediatric
traumatic brain injury. Journal of Communication Disorders
2000;33:333–344.
9. Vanderploeg RD, Schinka JA, Baum KM, Tremont G,
Mittenberg W. WISC-III premorbid prediction strategies:
Demographic
and
best
performance
approaches.
Psychological Assessment 1998;10:277–284.
10. Richards M, Deary IJ. A life course approach to cognitive
reserve: A model for cognitive aging and development?
American Neurological Association 2005;58:617–622.
11. Vanderploeg RD, Schinka JA, Axelrod BN. Estimation of
WAIS-R premorbid intelligence: Current ability and demographic data used in a best-performance fashion.
Psychological Assessment 1996;8:404–411.
12. Richards M, Sacker A. Lifetime antecedents of cognitive
reserve.
Journal
of
Clinical
and
Experimental
Neuropsychology 2003;25:614–624.
13. Manly JJ, Touradji P, Tang M, Stern Y. Literacy and
memory decline among ethnically diverse elders. Journal of
Clinical and Experimental Neuropsychology 2000;25:
680–690.
14. Orme DR, Johnstone B, Hanks R, Novack T. The WRAT-3
reading subtest as a measure of premorbid intelligence among
persons with brain injury. Rehabilitation Psychology 2004;
49:250–253.
15. Johnstone B, Callahan CD, Kapila CJ, Bouman DE. The
comparability of the WRAT-R reading test and the NAART
as estimates of premorbid intelligence in neurologically
impaired patients. Archives of Clinical Neuropsychology
1996;11:513–520.
16. Ruff RM, Marshall LF, Crouch J, Klauber MR, Levin HS,
Barth J, Kreutzer J, Blunt BA, Foulkes MA, Eisenberg HM,
Jane JA, Marmarou A. Predictors of outcome following severe
head trauma: Follow-up data from the Traumatic Coma
Data Bank. Brain Injury 1993;7:101–111.
17. Barnes MA, Dennis M, Wilkinson M. Reading after closed
head injury in childhood: Effects on accuracy, fluency, and
comprehension. Developmental Neuropsychology 1999;15:
1–24.
18. Catroppa C, Anderson VA, Muscara F, Morse SA,
Haritou F, Rosenfeld JV, Heinrich LM. Educational skills:
Long-term outcome and predictors following paediatric
traumatic brain injury. Neuropsychological Rehabilitation
2009;19:716–732.
19. Yeates KO, Taylor HG, Wade SL, Drotar D, Stancin T,
Minich N. A prospective study on short- and long-term

20.
21.

22.

23.

24.

25.

26.

27.
28.

29.

30.

31.

32.

33.

neuropsychological outcomes after pediatric traumatic brain
injury. Neuropsychology 2002;16:514–523.
Teasdale G, Jennett B. Assessment of coma and impaired
consciousness: A practical scale. Lancet 1974;2:81–84.
Wechsler D. Wechsler Individual Achievement Test
(WIAT-II). 2nd ed. San Antonio, Texas: The Psychological
Corporation; 2001.
Wechsler D. Wechsler Intelligence Scale for Children
(WISC-IV). 4th Edition: American Manual. San Antonio,
Texas: The Psychological Corporation; 2003.
Manly T, Robertson IH, Anderson V, Nimmo-Smith I. The
Test of Everyday Attention for Children. England: Thames
Valley Test Company; 1999.
Fridlund AJ, Delis DC. California Verbal Learning Test:
Children’s Version. Texas, USA: The Psychological
Corporation; 1994.
Meyers JE, Meyers KR. Rey Complex Figure Test and
Recognition Trial. Lutz, Florida: Psychological Assessment
Resources, Inc; 1995.
Heaton RK, Chelune GJ, Talley JL, Kay GG, Curtiss G.
Wisconsin Card Sorting Test. Lutz, Florida: Psychological
Assessment Resources, Inc; 1981.
Boll T. Children’s Category Test. USA: The Psychological
Corporation; 1993.
Anderson V, Moore C. Age at injury as a predictor of
outcome following pediatric head injury: A longitudinal
perspective. Child Neuropsychology 1995;1:187–202.
Anderson VA, Morse SA, Klug G, Catroppa C, Haritou F,
Rosenfield J, Pentland L. Predicting recovery from head
injury in young children: A prospective analysis. Journal of
International Neuropsycholgoical Society 1997;3:568–580.
Dennis M, Barnes MA, Wilkinson M, Humphreys RP. How
children with head injury represent real and deceptive
emotion in short narrartives. Brain and Language 1998;61:
450–483.
Kaplan GA, Turrell G, Lynch JW, Everson SA, Helkala EL,
Salonen J. Childhood socioeconomic position and cognitive
function in adulthood. International Journal of Epidemiology
2001;30:256–263.
Capron D, Petrill SA, Pike A, Price T, Plomin R. Chaos in
the home and socioeconomic status are associated with
cognitive development in early childhood: Environmental
mediators identified in a genetic design. Intelligence 2004;32:
445–460.
Dennis M. Developmental plasticity in children: The role of
biological risk, development, time, and reserve. Journal of
Communication Disorders 2000;33:321–332.

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