Seizure 18 (2009) 639–643
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Seizure
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Preoperative IQ predicts seizure outcomes after anterior temporal lobectomy
Hsiang-Yu Yu a, Yang-Hsin Shih b, Tung-Ping Su c, Ker-Nen Lin a, Chun-Hin Yiu a, Yung-Yang Lin a,
Shang- Yeong Kwan a, Chien Chen a, Der-Jen Yen a,*
a
Department of Neurology, Taipei Veterans General Hospital, National Yang-Ming University, Taiwan
Department of Neurosurgery, Taipei Veterans General Hospital, National Yang-Ming University, Taiwan
c
Department of Psychiatry, Taipei Veterans General Hospital, National Yang-Ming University, Taiwan
b
A R T I C L E I N F O
A B S T R A C T
Article history:
Received 9 April 2009
Received in revised form 5 July 2009
Accepted 30 July 2009
Purpose: IQ tests are frequently used in the preoperative neuropsychological assessment of candidates
for anterior temporal lobectomy (ATL). We reviewed IQ test results and surgery outcomes to evaluate the
roles of IQ tests in the preoperative work-up.
Methods: A total of 205 adult patients who had undergone ATL and whose seizure outcomes were
followed for 2 years after surgery were included. The short form WAIS-R was used to estimate
intelligence. Multiple linear regression and logistic regression analyses were used to examine the
variables for IQ and seizure outcomes.
Results: Education, duration of epilepsy and gender were factors that accounted for 24.6% of the variance
in the full-scale IQ (FSIQ) scores. The verbal IQ and performance IQ discrepancies at various magnitudes
could not lateralize the seizure foci. Freedom of seizure was noted in 128 (62.4%) of the patients. Seizure
outcomes, however, correlated with the preoperative FSIQ. After adjustment for variables that affect
seizure outcomes, the FSIQ was an independent predictor of postoperative seizure outcomes (OR 1.04,
95% CI 1.01–1.06, p = 0.003). Of patients who had FSIQ lower than 70, 50% became free from seizures by 2
years after surgery.
Conclusions: In our study, IQ tests were unable to lateralize seizure foci but may serve as an independent
predictor of postoperative seizure outcomes. Since a longer duration of epilepsy had deleterious effects
on intelligence, earlier surgical intervention might better preserve neuropsychological function and,
consequently, allow better seizure control after ATL. Nonetheless, patients with lower IQ scores could
still benefit from ATL.
ß 2009 British Epilepsy Association. Published by Elsevier Ltd. All rights reserved.
Keywords:
Anterior temporal lobectomy
IQ
Seizure outcome
Temporal lobe epilepsy
1. Introduction
Comprehensive neuropsychological assessments of candidates
for epilepsy surgery are routinely administered at most centers
that specialize in treating epilepsy.1 These tests can facilitate the
evaluation of the integrity of cognition before surgery, the
identification of cognitive sequelae resulting from resection
surgery, the refinement of surgical parameters, and appreciation
of the overall impact of cognitive change following epilepsy
surgery.2 Patients with chronic temporal lobe epilepsy (TLE) have
widespread cognitive morbidity. For patients with TLE, intelligence
assessment is a frequently tested preoperative parameter,
although greater attention is given to the material-specific
* Corresponding author at: Department of Neurology, Taipei Veterans General
Hospital, No. 201, Sec. 2 Shih-Pai Rd, Taipei, Taiwan. Tel.: +886 2 28757578;
fax: +886 2 28757579.
E-mail address: [email protected] (D.-J. Yen).
memory deficits. Comparison of the results from various cognitive
measures between patients with TLE and normal subjects
demonstrated negative impacts of epilepsy on memory, naming,
motor dexterity and intelligence.3,4 The application of neuropsychological tests in lateralizing seizure focus has been of great
interest for researchers. Verbal–performance IQ (V–P IQ) discrepancies related to the side of the hemispheric lesion have been
reported in a large sample of neurological patients tested with
different versions of IQ tests.5,6 A logical hypothesis suggests that
the V–P IQ discrepancies may be able to lateralize the epileptogenic foci. A large number of patients tested following the surgical
removal of the affected temporal lobe have shown either
performance IQs about 6 points higher than verbal IQs (in patients
undergoing left anterior temporal lobectomy (ATL)), or verbal IQs
2.5 points higher than performance IQs (in patients undergoing
right ATL).6 The results, however, were not the same for
lateralizing the epileptogenic side using V–P IQ discrepancies
before surgery. Although a few studies have demonstrated some
degree of lateralizing value for IQ tests under certain conditions,7,8
1059-1311/$ – see front matter ß 2009 British Epilepsy Association. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.seizure.2009.07.009
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H.-Y. Yu et al. / Seizure 18 (2009) 639–643
most studies that attempted to evaluate the role of IQ tests in the
lateralization of epileptogenic foci before surgery failed to
demonstrate promising results.1,9 Another application of preoperative IQ performance has been the prediction of seizure
outcome after ATL. The results were consistent among previous
studies of adult patients: the seizure outcomes of patients with
lower preoperative intelligence performance were not as good as
those of patients with IQs above average.10–12 The most frequently
used IQ tests, Wechsler Adult Intelligence Scale-revised (WAIS-R)
or WAIS-III, require much time and effort to administer and score.
The assessment of global intelligence by various short forms has
been proven to be reasonable with respect to time and as effective
as the full form.1,9 We retrospectively evaluated the roles of IQ
tests using a short form of the WAIS-R for our patients who
underwent ATL. The impact of epilepsy on intelligence, lateralization values with respect to the side of TLE and prediction of
postoperative outcomes were examined in this study.
2. Methods
2.1. Subjects
A total of 205 Chinese-speaking patients who had undergone
ATL for intractable seizures at the Taipei Veterans General
Hospital between 1987 and 2002 were enrolled in this study.
All subjects were older than 16 years of age, and their preoperative
IQ scores and postoperative seizure outcome data were available.
Our preoperative evaluation included long-term video-electroencephalography (video-EEG) telemetry with sphenoidal electrodes, brain magnetic resonance imaging (MRI), magnetic
resonance spectroscopy (MRS since 1995), magnetoencephalography (since 2000), interictal and postictal single-photon
emission computed tomography (SPECT), fluoro-D-glucose positron emission tomography (PET), psychiatric consultation, neuropsychological assessment, and intracarotid amobarbital
procedures (IAPs). The study results were discussed at the
multidisciplinary seizure conference and, in each case, the side
of the temporal lobectomy was determined by concordance of the
above measurements. According to the video-EEG recording
interictal spikes were categorized as unifocal (spikes only in the
temporal region ipsilateral to the side of resection or no spikes) or
non-unifocal (spikes in extratemporal regions or contralateral
temporal spikes with an occurrence of more than 10% of the total
amount of spikes). The interictal EEG was sampled for a 2-min
duration every 30 min during the video-EEG recording. In order to
examine the lateralization values based on preoperative IQ, only
patients with left hemisphere speech dominance as determined
by IAP were included. The seizure outcomes were categorized by
Engel’s classification.13 In this study, freedom from seizures refers
to complete freedom from disabling seizures with or without
auras (Engel’s IA and IB) for 2 years after ATL.
2.3. Statistical analyses
Student’s t, chi-square, and Mann–Whitney U tests were used to
examine the differences in demographic characteristics between
left and right TLE. Simple linear regression analysis was used to
evaluate possible clinical variables, including age, gender, onset,
duration of epilepsy, side of TLE, and pathology of lesions other
than gliosis that could affect IQ. Variables that significantly
correlated with IQ in the simple regression analysis were then
submitted to multiple linear regression analyses. The model
included only variables for which p < 0.05. When examining the
lateralization value of IQ scores, the scores of the VIQ minus PIQ
were categorized as greater than 10 (suggesting right TLE),
intermediate, or less than
10 (suggesting left TLE). The
lateralization results were then compared with the side of the
ATL. To evaluate the relationship between postoperative seizure
outcome and IQ, logistic regression analysis was used. Seizure
outcomes were compared in patients whose FSIQ values were
higher than 87 and lower than 87. The IQ cut-off was determined
by the median FSIQ (87.0) of the 205 patients in this study.
Adjusted variables in the multiple logistic regression models
included age at onset, age at surgery, resection type (ATL with or
without hippocampectomy), histopathological diagnosis (gliosis or
other lesion), and structural abnormality upon MRI (yes or no). A pvalue less than 0.05 was considered to be statistically significant.
All statistical analyses were performed using SPSS version 15.0 for
Windows.
3. Results
The demographic characteristics for both left and right TLE
patients are shown in Table 1. The mean group age at the time of
testing was higher for left TLE patients than right TLE patients
(p = 0.031).
3.1. Factors related to intelligence
The duration of epilepsy and years of education were related to
the IQ scores, according to the linear regression analysis. Patient
age at testing and gender were also statistically significant in
predicting FSIQ and VIQ (Table 2). The age at onset and duration of
epilepsy showed high-grade co-linearity in this study. We then
decided to exclude the age at onset from the multiple regression
analysis because the duration of epilepsy demonstrated a stronger
correlation with the dependent variable of IQ. Patients with
unifocal interictal spikes or no interictal spikes demonstrated a
better FSIQ and PIQ.
In the multiple regression models, education, duration of
epilepsy, and gender accounted for 24.6% and 25.3% of the variance
in the FSIQ and VIQ scores respectively. Education and duration of
epilepsy accounted for 16.7% of the variance in the PIQ scores.
2.2. IQ tests
3.2. Lateralization based on IQ scores
IQ tests were performed by the neuropsychologists. Three
versions of IQ tests including WAIS-R, a short form of the WAIS-R
(Digit span, Arithmetic, Similarities, Block design, Objects assembly and Digit symbol),14 and WAIS-III, have been used in our
epilepsy center over the past 20 years. The correlation between the
short form and full form WAIS-R was examined in a subgroup of 30
patients. Correlations between the short form and full form WAISR in estimating the VIQ, PIQ and FSIQ (Spearman r = 0.76, 0.81, 0.80
for VIQ, PIQ and FSIQ) were significant and robust. The majority of
our cases were assessed by the short form of the WAIS-R. In the
present study, we enrolled only those patients for whom short
form of WAIS-R was used.
The group IQ showed no difference with respect to the side of
TLE (Table 1). The group difference in V–P IQ discrepancies was not
statistically significant (Mann–Whitney U, p = 0.311).
V–P IQ discrepancies greater than 10 points were noted in 56 of
the 205 patients (27.3%), and those less than 10 were present in
16 of the 205 patients (7.8%). Correct lateralization for V–P IQ
discrepancies greater than 10 was 37.5% for left TLE and 57.1% for
right TLE patients. Different magnitudes of V–P IQ discrepancies
did not produce better lateralization values (Table 3). When
patients with pathology diagnoses of gliosis or secondary TLE due
to a tumor or some other structural lesions were analyzed
separately, correct lateralization occurred in a similar fraction to
H.-Y. Yu et al. / Seizure 18 (2009) 639–643
Table 1
Demographics and seizure-related characteristics of left and right temporal lobe
epilepsy patients.
Left TLE
(n = 98)
Right TLE
(n = 107)
p value
Gender (M/F)
Age at onset
Age at IQ test
Duration
Education years
(>9 years/9 years)
Pathology MTS/non-MTS
56/42
15.2 (8.9)
31.6 (8.6)
16.4 (10.0)
60/38
59/48
13.7 (8.9)
29.0 (8.4)
15.3 (7.8)
78/29
0.77
0.24
0.03
0.37
0.08
65/33
61/46
0.17
FSIQ
VIQ
PIQ
VIQ–PIQ
Freedom from seizures
(SF/NSF)
87.0 (15.4)
89.5 (15.9)
85.4 (15.0)
4.1 (10.0)
65/33
89.7 (14.6)
92.6 (14.6)
87.1 (15.6)
5.5 (12.3)
63/44
0.19
0.15
0.43
0.31
0.27
MTS: mesial temporal sclerosis, SF: seizure-free, NSF: not seizure-free, (): standard
deviation.
that obtained when all subjects were analyzed together (left TLE
51.4% and right TLE 36.4% for the gliosis group; left TLE 68.4% and
right TLE 40.0% for the ‘‘other lesion’’ group). Analyses of seizurefree patients and patients with unilateral temporal spikes revealed
similar results (Table 3).
3.3. Seizure outcome
Seizure freedom for 2 years after ATL was observed in 128 of 205
(62.4%) patients. The mean FSIQ in patients with seizure freedom
was higher than that in patients who continued to have disabling
seizures (91.5 15.1 vs. 83.2 13.5, p < 0.001). In a logistic regression
analysis, FSIQ scores were shown to be an independent predictor of
seizure outcome in both the unadjusted model (OR 1.04, 95% CI 1.02–
1.07, p < 0.001) and model adjusted for age at onset, age at surgery,
resection type, histopathological diagnosis, presence of abnormality
upon MRI, and interictal unifocal spikes (OR 1.04, 95% CI 1.01–1.06,
p = 0.003). The FSIQ score category was related to the seizure outcome
(OR 2.80, 95% CI 1.56–5.03, p = 0.001). After adjusting for the
aforementioned variables, patients with FSIQs 87 displayed an odds
ratio for seizure freedom of 2.67 as compared to those with FSIQ <87
(95% CI 1.39–5.13, p = 0.003). There were 20 patients with FSIQs lower
than 70 in our group. Ten patients remained seizure-free at 2 years after
ATL. Among these 20 patients, the postoperative IQ was followed in 9 (5
seizure-free and 4 not seizure-free). None of these patients displayed an
IQ decrement of more than 2 points (Table 4). In contrast, three patients
(33.3%) showed a postoperative scores increment of more than 5 points
in the FSIQ. Two patients (22.2%) gained more than 5 points in the VIQ
and four patients (44.4%) gained more than 5 points in the PIQ after
surgery.
641
4. Discussion
4.1. Factors related to IQ scores
In the present study, level of education attained, gender, and
duration of epilepsy were predictive factors for IQ in medically
intractable TLE. Gender and educational attainment are known
background variables that predict performance on IQ tests.6 The
level of education attained has also been shown to be an important
non-neurological social factor for IQ in patients with epilepsy.3,15
In the present study, males outperformed females on the IQ tests.
Gender differences in the processing of neuropsychological tests
have been demonstrated in normal subjects and patients with
neurological disorders.16–19 Males also showed substantially
better performance than female on the Wechsler’s arithmetic
subsets starting from ages 16.18 Among our subjects, the major
demographic factors predicting performance on the IQ tests were
as same as those observed for normal subjects. With regard to the
epilepsy-related variables, duration was an important factor in our
subjects. The association of the duration of epilepsy and cognition
has been investigated in many cross-sectional studies.3,20,21
Longitudinal studies have also shown that cognitive comorbidity
in patients with epilepsy worsens with time.21–23 Although
memory is the anticipated deficit in patients with TLE, comprehensive neuropsychological tests detected more diffuse and
generalized cognitive impairment in all domains of cognitive
function, including intelligence.3,4 Other potential epilepsy-related
variables e.g., severity and frequency of seizures and types of
antiepileptic drugs (AEDs) were not analyzed in this study.
However, the duration of epilepsy is best viewed as a composite
factor that probably reflects the influence of several factors (e.g.,
repeated seizures,24 toxic effects of AEDs25 and onset of epilepsy at
young age26) that further facilitate neuronal damage. Earlier
surgical intervention in selected cases may reduce the adverse
effect on intelligence caused by the above mentioned factors.
Furthermore, memory decline may be stopped by successful
epilepsy surgery, as demonstrated in a previous well-controlled
study.23
4.2. Lateralization based on IQ scores
Preoperative neuropsychological tests were considered helpful
for determining the lateralization of the seizure focus.1 Review of
the literature suggests that obtaining a correct lateralization value
from neuropsychological tests is not as efficient as video-EEG, MRI,
IAP, or functional neuroimaging in TLE.27–31 There was no
consistent difference in measures of V–P IQ discrepancies or
verbal–visual memory score discrepancies observed between
candidates resected in the left versus right hemispheres.9,30,32–34
A well-designed study investigated the lateralization value of
Table 2
Potential factors affecting the IQ scores.
FSIQ
Univariate b
Age at onset of epilepsy
Age at test
Duration of epilepsy
Male
Left TLE
Education 9 years
Pathology of gliosis
Interictal EEG spikes, unilateral
0.21
0.26
0.45
5.02
2.74
14.32
1.81
4.36
VIQ
p value
0.08
0.03
<0.001
0.02
0.19
<0.001
0.40
0.05
Multiple regression models:
FSIQ = 76.87 0.29 duration + 12.84 education 3.74 gender, p < 0.001, R2 = 0.246.
VIQ = 76.90 0.24 duration + 13.89 education 3.67 gender, p < 0.001, R2 = 0.253.
PIQ = 74.96 0.36 duration + 10.12 education, p < 0.001, R2 = 0.167.
Univariate b
0.15
0.28
0.41
4.95
3.05
15.15
1.34
3.10
PIQ
p value
0.22
0.02
0.001
0.02
0.15
<0.001
0.54
0.16
Univariate b
0.28
0.20
0.47
4.28
1.71
11.57
2.04
4.94
p value
0.02
0.10
0.001
0.02
0.15
<0.001
0.54
0.03
H.-Y. Yu et al. / Seizure 18 (2009) 639–643
642
Table 3
Relationship between VIQ–PIQ discrepancies at different magnitudes and correct TLE lateralization for each side of hemisphere.
V–P discrepancies
10
12
15
Whole group (n = 205)
Patients with freedom from seizures (n = 128)
Proportion of
patients with
discrepancy %
Correct lateralization
n (%)
Left TLE
Right TLE
35.0
27.0
18.0
6 (37.5)
5 (38.5)
2 (33.3)
32 (57.1)
28 (65.1)
20 (62.5)
Proportion
of patients with
discrepancy %
Correct lateralization
n (%)
Left TLE
Right TLE
38.0
32.0
22.0
5 (38.5)
4 (36.4)
2 (33.3)
20 (55.6)
19 (63.3)
13 (56.5)
Patients with freedom from seizures and
unitemporal spikes (n = 90)
Proportion of
patients with
discrepancy %
Correct lateralization
n (%)
Left TLE
Right TLE
36.0
30.0
20.0
3 (30.0)
2 (25.0)
1 (20.0)
12 (52.2)
11 (57.9)
6 (46.2)
TLE: temporal lobe epilepsy.
comprehensive neuropsychological assessment in TLE and found
that only 66% of the patients were correctly lateralized.31 Akanuma
et al. found that neuropsychological tests permitted lateralization
when evaluated in conjunction with Wada tests. Without Wada
tests, however, verbal IQ alone correctly lateralized 58% of the TLE.7
Studies that evaluate the lateralization value of IQ tests commonly
employ the discrepancies associated with the VIQ and PIQ.
Lateralization of seizure foci by V–P IQ discrepancies alone showed
lower sensitivity and, moreover, that certain conditions were
necessary for lateralization.8,9,34 We were not able to lateralize the
side of TLE at different magnitudes for V–P IQ discrepancies. The
lateralization was correct in 57.1% of the right TLE patients, a
percentage not much better than chance. For the left TLE patients,
incorrect lateralization was more frequent than correct lateralization. Although the scores on the short form were correlated with
the scores on the full form in our study, there might have been bias
in the value obtained for V–P IQ discrepancies. The WAIS-R subsets
selected in the evaluation of IQ of our patients were not the same as
the widely used dyad or tetrad of Silverstein’s short form,35 or
Kaufman’s two- , three- or four-subset short form of the WAIS-R.36
Subset selection was initially made according to clinical convenience, and the short form was administered for most of our
patients entering the pre-surgical program. In this retrospective
study we only enrolled patients whose IQs were assessed by the
short form to reduce the variability among subjects. However,
Hermann et al.9 found that there was no lateralization effect for V–
P IQ discrepancies of various magnitudes using a full form of the
WAIS-R. Although a recent study found that IQ tests could
lateralize TLE due to mesial temporal sclerosis in patients with
unilateral temporal spikes,8 this application was still limited.
Among the 82 cases investigated in that study, only 29 displayed IQ
discrepancies greater than 10 points. Such discrepancies occurred
in less than 40% of all patients who took the IQ tests. For the
remaining 60% of patients, the results of the IQ tests did not appear
to be useful for lateralization: the sensitivity of this method for
predicting the side of seizure onset was therefore low. Lateralization based on IQ tests and V–P IQ discrepancies is of limited value.
Previous studies evaluating the lateralization values of neuropsychological tests enrolled only patients with good seizure outcomes.8,34 In the present study, exclusion of patients who were not
free from disabling seizures after ATL or patients with extratemporal spikes or bilateral temporal spikes did not produce better
results in terms of using IQ tests for determination of lateralization.
Table 4
IQ changes after ATL in patients with FSIQs <70 (n = 9).
IQ change
FSIQ
VIQ
PIQ
2–0
0–5
>5
1 (11.1%)
5 (55.6%)
3 (33.3%)
1 (11.1%)
6 (66.7%)
2 (22.2%)
2 (22.2%)
3 (33.3%)
4 (44.4%)
IQ change: postoperative IQ
preoperative IQ.
4.3. Preoperative IQ and seizure outcome
In this study, preoperative IQ was an independent predictor of
postoperative seizure outcome in ATL patients. Patients with lower
preoperative FSIQs tended to have recurrent seizures after ATL.
This observation is concordant with previous studies.10–12,37
Chelune et al. studied on a large group of 1034 adult patients
with ATL and found that patients who continued to have seizure
after surgery had statistically lower preoperative IQs than those
who were seizure-free.10 Malmgren et al. recently included a
relatively large group of pediatric and adult patients with IQs lower
than 70 and demonstrated that IQ was an independent predictor
for postoperative seizure outcome.11 The results in study of
exclusive pediatric patients, however, have shown that preoperative not a good predictors of the postoperative seizure outcome.38,39 The relationship between IQ scores and postoperative
seizure outcomes in the developing brain seems to be different
from that in the developed brain. However, some difficulties
existed in the studies of pediatric patients, and these may be
responsible for the differences from results observed in adult
patients. For example, the different tests used in assessment of IQ
in children (especially across different ages) and the inclusion of
patients undergoing different types of resective surgery might
reduce the homogeneity of these study groups. In this study, we
only enrolled left hemisphere-dominant adult patients of ATL
evaluated by the same IQ test to reduce the heterogeneity of the
study subjects.
A low IQ might be associated with diffuse and generalized
cerebral dysfunction and possibly, a more widespread irritating
area in the brain. Consequently, this may lead to a lower seizurefree rate after ATL. In this study, the patients with unifocal
interictal spikes demonstrated better IQ performance than did
patients with more widespread interictal spikes. Lieb et al. also
showed that bilateral synchronous spikes were associated with
negative IQ performance.37 Lee et al. found that the association
between lower FSIQ and left medial TLE patients was only
significant in patients with bitemporal interictal spikes.8 Widespread irritating features could lead to a lower seizure-free
rate.40,41 After controlling for the interictal spike variable,
however, we determined that preoperative IQ remained an
independent predictor of postoperative outcome in this study.
Other factors contributing to the association between IQ and
postoperative seizure outcome merit further investigation.
Although better IQ performance was associated with a better
seizure outcome, many low IQ patients could benefit from surgery.
Freedom from seizures after ATL was found for 52–64% of adult
patients.10–12,42 With regard to the cognition outcome, no
significant change was noted in low IQ patients after resection
surgery.12,38 In our study, 50% of the patients who had FSIQs lower
than 70 attained freedom from seizures. IQ decrement after ATL
might be a concern for patients with lower IQs; however, the
postoperative IQs did not show a decrement of more than 2 points
H.-Y. Yu et al. / Seizure 18 (2009) 639–643
in our patients. In stead, 33.3% of patients displayed FSIQ
improvements of more than 5 points. Preoperative IQ may provide
additional information for preoperative consultation, but a lower
IQ was not a contraindication for epilepsy surgery. In our cases
with lower preoperative IQ, epilepsy surgery did not have a
negative impact on intelligence.
In summary, preoperative intelligence assessment provided
information regarding the impact of chronic epilepsy on cognition,
and predicted the seizure outcome after ATL in adult patients with
medically intractable TLE. However, the value of V–P IQ
discrepancies for lateralizing the TLE was limited. Since longer
epilepsy duration had deleterious effects on intelligence, earlier
surgical intervention might better preserve neuropsychological
function and, consequently, permit better seizure control after ATL.
Nonetheless, patients with lower IQ scores could still benefit from
ATL.
Acknowledgements
We thank Professor CW Lai and Dr. John Wang for their advice
and Miss WY Sheng for statistical assistance.
This study was supported in part by a grant from the National
Science Council of Taiwan (97-2314-B-075-010).
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
the online version, at doi:10.1016/j.seizure.2009.07.009.
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