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Child Neuropsychology, 12: 165–172, 2006

Copyright © Taylor & Francis Group, LLC


ISSN: 0929-7049 print / 1744-4136 online
DOI: 10.1080/09297040500276836

A COMPARISON OF CHILDREN WITH EPILEPSY


TO AN AGE- AND IQ-MATCHED CONTROL GROUP
ON THE CHILDREN’S MEMORY SCALE

Kristine A. Borden, Thomas G. Burns, and


Stephanie D. O’Leary
Department of Neuropsychology, Children’s Healthcare of Atlanta, Georgia

Past research has found that children with epilepsy exhibit decreased memory skills. In
addition, some studies have found that children with epilepsy obtain significantly lower IQ
scores than controls. In an effort to examine whether children with epilepsy have specific
memory weaknesses versus global cognitive difficulties, the present study compared the
performance of 62 children (age range = 6–16 years). Thirty-one children with epilepsy
were compared to 31 age- and IQ-matched controls on the Children’s Memory Scale (CMS)
to determine whether differences in memory skills persist when IQ is matched. An indepen-
dent t-test comparing index and scaled scores was performed. The results indicated that
with the exception of the Word Pairs subtest (p < .01), children with epilepsy did not differ
significantly on the CMS subtests when IQ was matched. This suggests that list-learning
paradigms may be particularly sensitive to memory impairments in children with epilepsy
and/or that children with epilepsy have more global cognitive impairments.

INTRODUCTION
Past research has found that children with epilepsy exhibit memory difficulties
(Williams & Sharp, 2000). However, research in this area has been inconsistent, with some
studies failing to find a correlation between epilepsy and memory difficulties (Williams
et al., 2001). One factor that may contribute to these contradictory findings is discrepancies
in methods for controlling IQ. For example, some studies have used IQ cutoffs, which do
not ensure that the clinical and control groups have comparable IQs. Therefore, it is diffi-
cult to determine whether children with epilepsy demonstrate memory specific deficits or
global cognitive weaknesses. Because some studies have found that children with epilepsy
obtain lower IQ scores than children who do not have epilepsy (Moore & Baler, 2002;
Smith, Elliott, & Lach, 2002; Williams, Griebel, & Dykman, 1998), it is important to con-
trol for this variable. In addition, Baron (2004) cautions against the use of normative data
from memory tests without considering intellectual level, as memory deficits may be over-
estimated in children with low-average IQs. Therefore, IQ level does seem to have a medi-
ating effect on children’s performances on tests of memory and is important to control.

Address correspondence to Kristine A. Borden, Department of Neuropsychology, Children’s Health-


care of Atlanta at Scottish Rite, 1001 Johnson-Ferry Road, Atlanta, NW 30342, Georgia. Tel: (404) 785-2849.
Fax: (404) 785-2851. E-mail: kristineborden@hotmail.com

165
166 K. A. BORDEN ET AL.

Another variable that may contribute to inconsistent findings in this area is lack of
consistency in standardized tests of memory for children. It is difficult to compare studies
examining memory among children with epilepsy when the various measures used to assess
memory utilize different tasks and modalities. Since 1994, three widely used memory
instruments have been published. These include the California Verbal Learning Test —
Children’s Version (CVLT; Delis, Kramer, Kaplan, & Ober, 1994), the Wide Range Assess-
ment of Memory and Learning — Second Edition (WRAML-2; Adams & Sheslow, 2003),
and the Children’s Memory Scale (CMS; Cohen, 1997). Williams et al. (2001) assessed
memory patterns of children with well-controlled idiopathic or cryptogenic epilepsy using
the CVLT-C, a word-list learning test. The children obtained Verbal IQ scores that were
within the average range (VIQ = 95.6). They found that children with both types of sei-
zures performed relatively similar to the CVLT-C standardization population. Surpris-
ingly, children with epilepsy exhibited significantly higher scores in their accuracy of new
learning and recognition skills while exhibiting less intrusions and perseverations. They
performed similar to the standardization population on the remaining CVLT-C indices.
Williams & Haut (1995) found that children with epilepsy obtained significantly
lower scores than children with substance abuse and psychiatric disturbances on the
WRAML. However, IQ was not specifically controlled in this study and there was no nor-
mative control group included in the analysis.
Very little research examining the performance of children with epilepsy has been
conducted with the CMS. The CMS is a test of visual and verbal memory for children ages
6 to 16 years old. The core test consists of four subtests, two of which assess memory for
visually presented material (Dot Locations and Faces subtests) and two of which assess
memory for auditorily presented material (Stories and Word Pairs subtests). For each sub-
test, the examinee is asked to recall and/or recognize information both immediately after
presentation and after a delay of approximately 30 minutes.
Cohen (1992) conducted a study on a preliminary version of a children’s memory
instrument and found that children with left temporal lobe epilepsy (TLE) performed signi-
ficantly worse on auditorily and verbally presented memory tasks than controls, and children
with right TLE performed significantly worse on visually presented memory tasks. How-
ever, this preliminary version of the CMS has few similarities to the current version of the
test. The 1992 children’s memory instrument consisted of five auditory/verbal memory tasks
(Digit Span, Sentence Repetition, Passage Recall, Verbal Learning, and Auditory-Paired
Associative Learning) and six visual memory tasks (Memory for Designs, Visual Sequential
Memory Test, Sequential Hand Movements, Sequential Touch Test, Visual Paired Associate
Learning, and Delayed Tactile Kinesthetic Recall). The only subtests from this version that
are comparable to the current CMS subtests that factor into the Verbal and/or Visual Indices
are the Passage Recall (similar to Stories), Auditory-Paired Associative Learning (similar to
Word Pairs), and Verbal Learning (similar to Word Lists) subtests. Only two of these tasks
(Passage Recall and Auditory-Paired Associative Learning) are included in core CMS bat-
tery, both of which are auditory/verbal tasks. Therefore, the results of Cohen’s (1992)
research using this preliminary children’s memory instrument may not be applicable or com-
parable to children’s performance on the current version of the CMS.
Beardsworth & Zaidel (1994) studied memory for faces, which is similar to the
Faces subtest of the CMS, in epileptic children before and after surgery. They found that
children with right TLE performed significantly worse on this task than both children with
left TLE and normal controls. However, IQ was not specifically controlled for as children
were included in the study only if they had a WISC-R Full Scale IQ of >70.
PERFORMANCE OF CHILDREN WITH EPILEPSY ON THE CMS 167

A preliminary analysis comparing the performance of children with temporal lobe


epilepsy (TLE) and controls on the current version of the CMS, using an IQ cutoff criteria
of >80, found that children with TLE performed significantly lower on all CMS indices
(Cohen, 1997). Because the average IQs for each group were not provided, it is unknown
whether the clinical and control groups exhibited significantly different IQs. Therefore,
the present study sought to determine whether children with epilepsy continue to exhibit
memory impairments when IQ scores are matched. It is hypothesized that when IQ is
matched, children with epilepsy would obtain significantly lower scores on the CMS than
the control group.

METHOD
Procedure
The clinical group was obtained by performing a computer search of children who
had received a neuropsychological evaluation at a regional medical center in the south-
eastern United States between 2000 and 2003. Children were selected for the study based
on the following inclusionary criteria: (1) they were administered the Wechsler Intelli-
gence Scale for Children — Third Edition (WISC-III; Wechsler, 1991) and obtained a Full
Scale IQ > 70, (2) they were administered the CMS, and (3) they had an EEG that con-
firmed the diagnosis of epilepsy. Exclusionary criteria consisted of the following: (1) they
did not have a comorbid diagnosis of ADHD, learning disability, head injury, or any other
neurological or psychiatric disorder.

Participants
The search initially identified 45 children, 14 of which were excluded based on the
above criteria (4 children had ADHD, 4 children had a head injury, 4 children had a psy-
chiatric disorder, and 2 children had comorbid ADHD/psychiatric disorder). The remain-
ing 31 participants (12 males, 19 females) included in the study ranged in age from 6 to 16
years. Ethnicity was generally representative of the population served by the hospital with
26 Caucasian children (83%), four African-American children (12%), one Hispanic child
(3%), and one child classified as Other (3%). These percentages are somewhat similar to
the 2000 United States Census, which reported that the United States population consists
of 69.13% White individuals, 12.06% Black individuals, and 12.55% Hispanic individuals.
The remainder of the population (6.26%) was identified as “Other.”
The age of seizure onset ranged from 1 to 15 years of age (Mean = 7.0 years). Diag-
noses of epilepsy included simple partial (6%), complex partial (48%), primary generalized
(23%), primary generalized, absence (10%), and undetermined (13%). Because seizure
location was undetermined for some participants, it was not considered for analysis in this
study. At the time of testing, five children were not taking antiepileptic medication, 15
children were taking one antiepileptic medication, and 11 children were receiving two or
more antiepileptic medications. Information regarding seizure frequency and duration was
unavailable for many participants either because parents were unable to report on this
information or the children were evaluated before the initiation of the study and this infor-
mation was not obtained.
Data for the control group was provided, with permission, by The Psychological
Corporation. These children were administered the CMS and WISC-III as part of a study
168 K. A. BORDEN ET AL.

to validate the CMS (Cohen, 1997). This control sample was age- and IQ-matched to the
clinical sample. Within the control group, there were 17 Caucasian children (53%), eight
African-American children (25%), five Hispanic children (17%), and two children were
classified as Other (6%).

Data Analysis
Using SPSS version 12.0 statistics package, independent t-tests were conducted to
compare the WISC-III and CMS performances of children with epilepsy (n = 31) with
controls (n = 31). Comparisons were conducted with all WISC-III IQ and index scores, as
well as all CMS indices and subtests. IQ and index scores have a mean of 100 with a stan-
dard deviation of 15 and scaled scores have a mean of 10 with a standard deviation of
three. P-values of <.05 were considered to be statistically significant. A tendency toward
significance was presumed if a p-value was between 0.05 and 1.0. Experiment-wise error
also was calculated to determine the probability of Type 1 errors.
In an effort to examine differences that may exist within the epilepsy group, an
exploratory analysis using independent t-tests was conducted with the WISC-III and CMS
means for children with complex partial epilepsy (CPS) and children who had seizures
other than CPS. Means were also examined for children with CPS and their matched con-
trols. Finally, within the clinical group, independent t-tests were conducted to examine dif-
ferences between age of onset for the CPS and non-CPS groups. In addition, correlations
between test data and age of onset were obtained.

RESULTS
Intellectual Functioning
The mean Full Scale IQ for the entire sample was 92.19 (SD = 12.39). There were
no significant differences between groups for age, WISC-III Full Scale IQ, Verbal Scale
IQ, Performance Scale IQ, Verbal Comprehension Index, Perceptual Organization Index,
and Freedom from Distractibility Index. Group means, standard deviations, and levels of
t-test significance for WISC-III IQ and index scores are presented in Table 1. The epilepsy
group (Processing Speed Index (PSI) = 90.65; SD = 15.44) performed significantly lower
than the control group (PSI = 99.03; SD = 13.47) on the PSI.
An independent t-test comparing children with CPS to children with seizures other
than CPS did not reveal significant differences on any WISC-III variable examined. In

Table 1 Performance of Epilepsy and Control Groups on the WISC-III

WISC-III Epilepsy Group Control Group T-test

Full Scale IQ 92.13 (12.46) 92.26 (12.52) .968


Verbal Scale IQ 95.13 (12.04) 94.26 (12.90) .784
Performance Scale IQ 90.65 (14.39) 91.71 (12.31) .755
Verbal Comprehension 95.13 (12.29) 94.45 (12.79) .832
Perceptual Organization 92.87 (14.92) 91.55 (13.43) .715
Freedom from Distractibility 98.90 (14.21) 100.67 (11.83) .601
Processing Speed 90.65 (15.44) 99.03 (13.47) .029

*Scores are standard scores (mean = 100; standard deviation = 15).


PERFORMANCE OF CHILDREN WITH EPILEPSY ON THE CMS 169

addition, there were no differences between children with CPS and their matched controls
on WISC-III variables.

Memory Functioning
An independent t-test comparing index and scaled scores on the CMS indicated that
when IQ is matched, there were no significant differences in performance between chil-
dren with epilepsy and normal controls on most indices and subtests. A significant differ-
ence was found on the Learning Index (p < .01), with the epilepsy group obtaining
significantly lower scores than controls. This finding was due to a significantly lower
score on the Word Pairs Learning subtest (p < .01). In addition, children with epilepsy per-
formed significantly lower on the Word Pairs Total scaled score (p < .01). Group means,
standard deviations, and levels of t-test significance for CMS indices and subtest scores
are presented in Tables 2 and 3. A tendency toward significance was found for the Verbal
Immediate (p = .070) and Verbal Delayed (p = .091). There were no other subtests that
approached significance. It is important to note that due to the high number of compari-
sons made, the probability of making a Type 1 error is .642.

Age of Onset
Within the clinical group, independent t-tests examining age of onset between CPS
and non-CPS groups did not reveal any significant differences. Therefore, all children
with epilepsy were considered as a group and correlations between age of onset and
WISC-III and CMS scores indicated a significant relationship between age of onset and
Full Scale IQ, Verbal IQ, Performance IQ, and Perceptual Organization Index. There were
no significant relationships between age of onset and CMS scores.

DISCUSSION
Overall, the mean WISC-III FSIQ of 92.19 (SD = 12.39) is consistent with past
research findings that children with epilepsy tend to obtain IQs in the low end of the aver-
age range (Rodin, Schmaltz, & Twitty, 1986; Aldencamp et al., 1999). While children with
epilepsy obtained similar scores on most WISC-III IQ and index scores, they performed

Table 2 Performance of Epilepsy and Control Groups on the CMS Indices

Epilepsy Group Control Group

Standard Standard
CMS Index Mean Deviation Mean Deviation T-test

Visual Immediate 91.35 18.7 97.71 11.7 .115


Visual Delayed 92.81 17.9 97.65 10.2 .196
Verbal Immediate 83.81 20.0 92.96 14.8 .070
Verbal Delayed 87.16 20.5 95.58 15.5 .091
General Memory 87.32 17.5 94.57 14.7 .114
Attention/Conc. 95.84 20.0 101.16 16.8 .260
Learning 85.42 18.6 97.45 14.2 <.01
Delayed Recognition 89.43 22.4 91.68 17.1 .661

Scores are standard scores (mean = 100; standard deviation = 15).


170 K. A. BORDEN ET AL.

Table 3 Performance of Epilepsy and Control Groups on the CMS Subtests

Epilepsy Group Control Group

Standard Standard
CMS Index Mean Deviation Mean Deviation T-test

Dots Learning 9.52 3.0 10.00 3.0 .529


Dots Total 9.97 3.0 10.10 2.8 .862
Dots Long Delay 9.77 2.4 9.74 2.7 .961
Stories Immediate 9.39 3.6 8.61 2.7 .384
Stories Del. Recall 9.16 4.1 8.73 2.8 .649
Stories Del. Recog. 9.10 4.1 8.35 3.2 .431
Faces Immediate 9.03 4.7 9.16 3.3 .900
Faces Delayed 9.16 4.4 9.48 3.0 .736
Word Pairs Learning 6.84 2.9 9.19 3.3 <.01
Word Pairs Total 6.74 3.3 9.26 3.3 <.01
Word Pairs Long Del. 7.81 3.9 8.94 3.7 .247
Word Prs. Del. Recog 8.94 5.2 9.32 3.8 .737
Numbers Total 9.74 2.8 10.13 3.8 .649
Sequencing Total 10.16 3.1 10.26 2.8 .898

Scores are scaled scores (mean = 10; standard deviation = 3).

significantly lower on the Processing Speed Index. Past research has indicated that antie-
pileptic medications may adversely affect motor speed and mental processing speed (Wil-
liams & Sharp, 2000), which may account for the significantly lower Processing Speed
Index scores in the current study. Also consistent with past research, age of onset corre-
lated with intellectual functioning (Farwell, Dodrill, & Barzel, 1985). Children with ear-
lier ages of onset had lower IQs than children with older ages of onset.
In general, our findings did not support the hypothesis that children with epilepsy
would continue to exhibit memory-specific impairments on the CMS while IQ was matched.
The results of the present study indicated that children with epilepsy did not exhibit signifi-
cant memory impairments on most subtests of the CMS. One possible explanation for these
findings may be that children with epilepsy have more global cognitive impairments, rather
than memory-specific impairments. The lack of memory-specific weaknesses in children
with epilepsy may result from the diffuse cognitive effects of seizures, a more rapid spread
of epileptiform activity between the temporal lobes and other parts of the brain (Williams
et al., 2001), and/or the plasticity of children’s brain structures (Baron, 2004). Plasticity may
account for reorganization and/or less lateralization of cognitive processes. Another explana-
tion may be that children with complex partial epilepsy may have more difficulty with mem-
ory tests. However, children with CPS in this study did not perform significantly different
than their matched controls or children with seizures other than CPS.
Children with epilepsy did, however, obtain significantly lower scores on the Learn-
ing Index than the control group. Their performance on this index was due to difficulties
on the Word Pairs Learning subtest, which measures the child’s ability to process, learn,
and recall a list of paired words over three learning trials. This may suggest that list-learning
paradigms in which children are asked to associate word pairs are particularly sensitive to
the types of memory impairments that children with epilepsy exhibit. One explanation for
our findings may lie in the increased demands necessary for this particular task, such as
more complex strategy use (e.g., learning and recalling the word, as well as remembering
which word pairs go together) in the absence of pertinent contextual information.
PERFORMANCE OF CHILDREN WITH EPILEPSY ON THE CMS 171

This more complex type of memory task seems more similar to the types of tasks chil-
dren are expected to perform at school, particularly at higher levels, and may account for
why children with epilepsy experience difficulties in school despite performing within the
average range on tests of memory during their neuropsychological evaluation. In a social
studies class, for example, a child may be asked to remember a list of explorers, as well as
what lands they discovered and the dates of their discoveries. A child with epilepsy may be
able to remember the explorers and the dates but may have difficulty recalling which explor-
ers go with which dates. This also may be true for children with epilepsy attempting to learn
a foreign language, in which they have to be able to recall the Spanish word, for instance,
and match it to its English counterpart in the absence of pertinent contextual information.
Because children with epilepsy performed similar to controls after a delay, both on free
recall and recognition trials, this suggests that they may need more time for consolidation in order
to accurately retrieve such information. On the CMS, children are told to remember material
because they will be asked to recall it later. Given the extra time during the delay, children may
continue to rehearse information allowing for recall at a rate similar to children without epilepsy.
As our study was a preliminary analysis examining memory while matching for IQ,
there were several limitations. One limitation of the present study was the lack of informa-
tion regarding localization or lateralized EEG findings upon diagnosis of epilepsy. Because
temporal lobe epilepsy has been associated with memory difficulties (Williams & Sharp,
2000), our results may not generalize to this subgroup of children with epilepsy, as only six
children were known to have complex partial epilepsy originating in the temporal lobes.
This may explain the differences between the results of the present study and that of Cohen’s
(1997) preliminary analysis. It may be possible that when compared to IQ-matched controls,
children with temporal lobe epilepsy will exhibit more memory-specific impairments as
measured by the CMS than do children with extratemporal or generalized epilepsy.
Another limitation of this study was the limited investigation into the effect of seizure type
on cognitive functioning. Due to our small sample size, an analysis of seizure type was not optimal.
Past research addressing this issue has resulted in variable findings. For example, Mandelbaum &
Burack (1997) found that prior to the initiation of antiepileptic therapy; children with generalized
nonconvulsive seizures were at greater risk for cognitive impairments than children with either par-
tial or convulsive seizures. Their results were consistent with a previous study examining attention
and visual-spatial, problem-solving, and sequencing skills (Giordani et al., 1985). In contrast,
Williams et al. (2001) did not find any differences among children with complex partial or general-
ized seizures whose epilepsy was well-controlled with monotherapy. Thus, the interaction of level
of seizure control (e.g., medication factors) and seizure type should be examined in future research.
Another limitation is that children with ADHD, learning disabilities, head injuries, and
psychiatric and neurological disorders were excluded. As the goal of the present study was to
determine the effects of epilepsy on memory functioning, our results may not apply to children
with comorbid diagnoses of epilepsy and one of the above mentioned diagnoses. Future studies
may want to compare the effects of ADHD, epilepsy, and ADHD + epilepsy on memory func-
tioning to determine whether differing profiles exist for these three groups.
Other variables that should be explored in future research while controlling for intellect
include duration and severity of seizure disorder and age of onset, as both of these factors can
influence the degree of cognitive deficit (Williams & Sharp, 2000). In addition, antiepilep-
tic medications have been found to have adverse cognitive effects (e.g., difficulty with
attention), which can affect memory performance (Mikati & Rahmeh, 2001). Therefore,
the effects of type and quantity of antiepileptic medications on memory performance also
should be explored while controlling for IQ.
172 K. A. BORDEN ET AL.

ACKNOWLEDGEMENTS
This research was supported by a grant from Children’s Healthcare of Atlanta at Scottish Rite. We
thank Rob K. Merritt, M. A., Director of Clinical Research, Children’s Healthcare of Atlanta, Inc., for
his assistance with this grant. We also thank The Psychological Corporation for providing CMS data.

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