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Epilepsy & Behavior 12 (2008) 276–280


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The validity of the Child Behavior Checklist for children with epilepsy
a,*
U. Gleissner , N.E. Fritz a, M. Von Lehe b, R. Sassen a, C.E. Elger a, C. Helmstaedter a

a
Department of Epileptology, University of Bonn, Bonn, Germany
b
Department of Neurosurgery, University of Bonn, Bonn, Germany

Received 14 September 2007; revised 25 October 2007; accepted 25 October 2007


Available online 11 December 2007

Abstract

The validity of the Child Behavior Checklist (CBCL) for patients with epilepsy has been questioned, because several items may reflect
seizure semiology rather than habitual behavior. This study compared a standard version of the CBCL with an adjusted version that
excluded those ambiguous items. Participants were 58 pediatric patients with epilepsy who were assessed preoperatively and 1 year after
successful surgical treatment. Before surgery, the adjusted version indicated significantly lower values for the scales Attention Problems,
Thought Problems, and Total Problems than the standard version. After surgery, the difference between the standard and adjusted ver-
sions and the scores for the ambiguous items were unchanged, although all patients were completely seizure free at that time. Elevated
scores on the ambiguous items thus probably reflect real behavioral problems and are not due to confusion with seizure semiology. The
results support the CBCL as a valid assessment tool in children with epilepsy.
 2007 Elsevier Inc. All rights reserved.

Keywords: Epilepsy; Child Behavior Checklist; Ambiguous items; Validity; Behavioral problems

1. Introduction (for instance, staring blankly, nervous movements or


twitching, wets self, and daydreams). In a review of 46
Children with neurological diseases are at a higher risk studies that included 2434 children with epilepsy, Roden-
for psychopathology than children with nonneurological burg et al. [3] found attention problems, thought problems,
diseases [1]. Therefore, examining possible psychopathol- and social problems to be relatively specific to children with
ogy is a standard component of the diagnostic procedure epilepsy compared with children with other chronic dis-
in children with epilepsy. The Child Behavior Checklist eases. Four of the eleven items that contribute to the Atten-
(CBCL) [2] is the most frequently used instrument for tion Problems scale and two of the seven items that
assessing behavioral adjustment in these patients. In a contribute to the Thought Problems scale are ambiguous.
meta-analysis by Rodenburg et al. [3], 31 of 46 studies Oostrom et al. [5] rescored the seven ambiguous items in
assessed behavioral problems using the CBCL. However, the CBCL as missing values. As a consequence, the per-
the CBCL was not originally designed for use with children centage of patients who exceeded the clinical cutoff score
who have chronic physical conditions, and there are con- for at least one of the scales, to which these items contrib-
cerns about its validity in such patients [4,5]. When applied uted, fell from 46 to 23%. This decrease in psychopathol-
to children with epilepsy, it is possible that several items are ogy ratings occurred only in children with epilepsy, not
rated on the basis of seizure features rather than habitual in healthy controls. The authors concluded that CBCL-
behavior and, hence, render behavioral scores ambiguous derived psychopathology percentages should therefore be
interpreted cautiously.
*
Eliminating critical items increases the risk that poten-
Corresponding author. Address: Department of Epileptology, Univer-
sity of Bonn, Sigmund-Freud Strasse 25, 53105 Bonn, Germany. Fax: +49
tially useful information about psychological functioning
(0)228 287 14486. might be omitted. However, including the critical items
E-mail address: ulrike.gleissner@ukb.uni-bonn.de (U. Gleissner). raises another problem: the frequency and the extent of

1525-5050/$ - see front matter  2007 Elsevier Inc. All rights reserved.
doi:10.1016/j.yebeh.2007.10.013
U. Gleissner et al. / Epilepsy & Behavior 12 (2008) 276–280 277

behavioral problems may be overestimated. The distortion Table 1


takes effect only in one direction (overestimation of prob- Group characteristics
lems), and a result that is below the critical cutoff can be Number of patients 58
regarded as correct. Nevertheless, incorrectly classifying a Gender (male/female) 27/31
Age at presurgical examination (years) 9.8 (3.4)a
child without behavioral problems as being behaviorally Age at onset of epilepsy (years) 4.5 (3.9)a
impaired would be serious and should be avoided. Preoperative IQ 82.8 (16.4) [44–125]b
The reported studies used the old version of the CBCL Side of surgery (left/right) 36/22
(4–18 years) [2]. Yet the same problems also arise for the Site of surgery (number of patients)
new version of the CBCL (6–18 years) [6], because it still Temporal 28
contains all the ambiguous items. The recently developed Frontal 10
preschool version of the CBCL (1.5–5 years) [7] also Parietal/occipital 8
Functional hemispherectomy 7
includes several ambiguous items (daydreams or gets lost
Multilobular resection 5
in his/her thoughts, nervous movements or twitching, fidg- a
ets, and strange behavior). Mean (SD).
b
Mean (SD) [range].
The present study further evaluates the degree of distor-
tion created by the ambiguous items in the CBCL by exam- 2.2. Child Behavior Checklist
ining the pre- and postoperative CBCL results of pediatric
patients who became completely seizure free after epilepsy The CBCL, which yields profiles of children’s problems as observed by
surgery. Because the patients had had their last seizure parents and other caregivers, was used to assess behavioral problems pre-
operatively and 1 year after surgery. It contains descriptions of 118 behav-
more than 1 year before the postoperative assessment, the
ioral and emotional problems. The respondent is asked to rate the child’s
estimates given by the parents should no longer reflect behavior over the previous 6 months on a graded scale: 0 = item is not
the seizures. The postoperative assessment was performed true; 1 = somewhat or sometimes true; 2 = very or often true. The result-
1 year after surgery, and the CBCL asks for behavioral ing profile consists of eight subordinate problem scales (Anxiety/Depres-
problems during a time interval of the previous 6 months. sion, Withdrawal, Somatic Complaints, Aggression, Delinquent
Behaviour, Attention Problems, Thought Problems, and Social Problems)
Thus, the patients have been seizure free for the entire time
that are grouped into superordinate scales: Internalizing Problems (subor-
interval as dictated by the CBCL. Comparing the standard dinate scales: Withdrawal, Somatic Complaints, Anxiety/Depression),
version and the results obtained by an adjusted version, Externalizing Problems (subordinate scales: Delinquent Behavior, Aggres-
which was corrected for the epilepsy-critical items, should sion) and total problems (sum of all items besides two items that assess
result in a smaller deviation after surgery if the ambiguous asthma and allergy). The scores of the items that constitute a scale are
summarized (summed raw scores) and transformed into standardized
items reflect mainly seizure semiology. In this case,
scores (T scores) according to the norms provided in the test manual.
the scores on the ambiguous items should decline According to expert ratings provided in another study [5], there are seven
postoperatively. items in the CBCL that give rise to ambiguity. This is because the wording
Lendt et al. [8] described an early improvement in could reflect aspects of habitual behavior as well as aspects of a seizure:
behavioral problems 3 months after epilepsy surgery in
the CBCL. The behavioral improvements were assumed • Is confused or seems to be in a fog (item 13)
• Has daydreams or gets lost in his/her thoughts (item 17)
to result directly from removal of the epileptic focus,
• Has nervous movements or twitching (item 46)
because they were dependent on seizure outcome. How- • Stares blankly (item 80)
ever, the critical items were included in the CBCL evalua- • Shows strange behavior (item 84)
tion, and therefore, it is not possible to tell whether the • Wets self during the day (item 107)
improvement indeed reflected behavioral improvement or • Wets the bed (item 108)
if it was due to the fact that the seizure symptoms were
These ambiguous items contribute to three subordinate and two super-
no longer incorrectly reported as behavioral problems in
ordinate scales:
seizure-free patients. Therefore, a second purpose of the
present study was to check the degree to which postopera- • Attention Problems (4 of 11 items)
tive improvement is due to a change in the ambiguous • Withdrawal (1 of 9 items)
items and to investigate if postoperative improvement is • Thought Problems (2 of 7 items)
also observed in the adjusted CBCL. • Internalizing Problems (1 of 32 items)
• Total Problems (7 of 118 items).

2. Methods
We used two sets of behavioral scores for these scales: the first set was
obtained according to the manual [9] and is referred to as CBCL. For the sec-
2.1. Patients ond set, the ambiguous items were treated as missing values; that is, they were
not included in the summed raw scores. This set is referred to as CBCLadj..
The neuropsychological database of the Department of Epileptology
at the University of Bonn was retrospectively screened for pediatric
patients (age <17) who were completely seizure free 1 year after a surgical 3. Results
treatment and had a pre- and postoperative assessment with the CBCL.
The search yielded 58 patients ranging between 4 and 17 years in age. Table 2 provides the pre- and postoperative results
Patient characteristics are provided in Table 1. obtained with the standard version and the adjusted
278 U. Gleissner et al. / Epilepsy & Behavior 12 (2008) 276–280

Table 2
Comparison of the standard and adjusted versions of the CBCL
Attention Problems Thought Problems Withdrawal Internalizing Problems Total Problems
Presurgery
CBCL 62.5 (9.3) 57.3 (7.9) 60.2 (9.1) 58.7 (10.1) 59.3 (9.1)
CBCLadj. 59.5 (6.8) 55.1 (6.6) 60.1 (8.7) 58.7 (9.9) 58.6 (8.9)
*** *** ***
T test for paired samples n.s. n.s.
Postsurgery
CBCL 57.1 (7.9) 52.8 (5.4) 56.1 (7.9) 50.9 (11.2) 50.5 (11.1)
CBLCadj. 55.5 (6.5) 52.0 (4.8) 56.5 (8.2) 51.1 (11.3) 49.9 (10.9)
** ** **
T test for paired samples n.s. n.s.
Note. T scores are cutoff scores for clinically significant impairment: T score P 68 for the subordinate scales, T score P 60 for the superordinate scales.
Values are means (SD). CBCL, Child Behavior Checklist; adj., adjusted version; n.s., not significant (P > 0.05).
***
P < 0.001.
**
P < 0.01.

version of the CBCL. A comparison with t tests for paired values was evident only for the item stares blankly,
samples with the standard and adjusted versions indicates, for which the postoperative score was lower than the
for the adjusted version, significantly lower results for the preoperative score (preoperative mean: 0.3, postoperative
scales Attention Problems, Thought Problems, and Total mean: 0.1, F = 6.0, P = 0.015). All other ambiguous items
Problems before surgery (t tests for paired samples, all t showed no significant postoperative changes (F < 3.0 with
> 4.7 with P < 0.001) as well as after surgery (all t > 2.9 P > 0.09).
with P < 0.007). For the superordinate scales, we compared A discordant classification means that a child is classi-
the number of patients scoring above the critical cutoff fied as impaired only in the standard CBCL and not in
score (T score P 60) for the standard and adjusted CBCL the adjusted version (T score P 68 for the subordinate
(Fig. 1) by computing Cohen j coefficients. The results scales, T score P 60 for the superordinate scales). The dis-
show a high congruence pre- and postoperatively for the cordant classification percentages are reported in Table 3.
scales Total Problems and Internalizing Problems (Cohen They were observed mainly in the subordinate scales, but
j coefficients before surgery > 0.93, after surgery > 0.91, rarely in the superordinate scales. After surgery, the per-
a coefficient of 1 indicates maximal congruence). centage of discordant classifications tended to be higher
T tests for paired samples with the pre- and postopera- for Attention Problems and lower for the Withdrawal
tive group average scores as pairs indicated significant scale. For the other scales, the percentage of discordant
improvements for all scales independent of whether the classifications remained largely unchanged.
standard CBCL or the adjusted CBCL was used (CBCL: Elevated levels of behavior problems have been reported
all t > 3.8 with P < 0.001; CBCLadj.: all t > 2.7 with in children with low IQ [10,11], and our sample included
P < 0.01). Postoperative changes in the ambiguous items many patients with intellectual disability or borderline
were evaluated by univariate analyses of variance, with intelligence (21% of patients had an IQ < 70, 35% of
the time of examination (pre- and postoperative) as an patients had an IQ between 70 and 85). Correlational anal-
independent variable and the items as dependent variables. yses, however, indicated no significant associations
A significant difference between the pre- and postoperative between IQ and the superordinate scales of the CBCL in
our sample (r < 0.11 with P > 0.4). A group comparison

60 Table 3
Before surgery After surgery
% behavioural problems

Discordant classifications
50
Percentage of discordant classifications
40 Before surgery After surgery
Attention Problems 40 (6/15) 62 (5/8)
30
Thought Problems 57 (4/7) 50 (1/2)
Withdrawal 25 (3/12) 0 (0/4)
20
Internalizing Problems 4 (1/27) 7 (1/15)
Total Problems 3 (1 of 29) 12 (2/17)
10
Total Internalizing Total Internalizing Note. In a discordant classification, a child is classified as impaired
problems problems problems problems (T score P 68 for the subordinate scales, T score P 60 for the superor-
Standard CBCL Adjusted CBCL dinate scales) in the standard version, but not in the adjusted version. For
instance, on the Attention Problems scale, 15 children were preoperatively
Fig. 1. Percentage of patients with problem scores above the cutoff. A classified as being impaired in the standard version, and of those 15
comparison of the standard and adjusted versions of the CBCL before and children, only 6 (=40%) were still classified as impaired when the adjusted
after surgery is illustrated. version was used.
U. Gleissner et al. / Epilepsy & Behavior 12 (2008) 276–280 279

between patients with intellectual disability (IQ < 70), vs 62%). Several studies have described Attention Problems
borderline intelligence (IQ between 70 and 85), and average as frequent behavioral problems in patients with epilepsy.
or above-average intelligence (IQ > 85) indicated no Dunn et al. [12] reported that 25% of the adolescents with
differences in the superordinate scales of the CBCL preop- epilepsy and 37% of the children with epilepsy had scores
eratively (ANOVAs, F < 0.2 with P > 0.8) and postopera- above the clinical cutoff for the CBCL Attention Problems
tively (ANOVAs, F < 2.2 with P > 0.1). Hence, it can be scale. Davies et al. [13] found that 12% of children with
assumed that our results are not significantly influenced uncomplicated epilepsy had attention-deficit/hyperactivity
by elevated levels of behavior problems in patients with disorder according to the DSM-IV (Diagnostic and Statis-
low IQ. tical Manual of Mental Disorders, Fourth Edition). By
using the Attention Deficit Disorder Evaluation Scale—
4. Discussion Home Version (ADDES-HV), Williams et al. [14] found
that children with epilepsy were at an increased risk for
Our findings support the validity of the CBCL for the inattentiveness and hyperactivity. They investigated 42
assessment of behavioral adjustment in paediatric patients newly diagnosed children with epilepsy at the time of diag-
with epilepsy. Less psychopathology was indicated by nosis and again when they were seizure free for at least 3
using the adjusted version versus the standard version. months under medical treatment. The frequency of inatten-
However, this was still true after surgery when the patients tive and hyperactive–impulsive symptoms remained largely
had been free of seizures for the 12 months prior to the unchanged, although the children were seizure free. In our
postoperative evaluation. It is therefore unlikely that the study, the absolute number of patients with attention prob-
ratings of the parents led to false classifications by merely lems decreased after surgery, but the rate of discordant
reflecting seizure semiology. This is supported by the find- classification did not. We therefore suggest that diagnosing
ing that the ratings of the ambiguous items remained attention problems with the standard version of the CBCL
largely unchanged after surgery. Discordant classifications can be regarded as valid and does not appear to be due to
(i.e., a child was classified as impaired only in the standard confusion with seizure semiology.
version but not in the adjusted version) were very rare for When the CBCL is used in a clinical context, the exam-
the superordinate scales. In a carefully designed study, iner has, in principle, the opportunity to clarify and to
Oostrom et al. [5] evaluated the CBCL in children with interpret the meaning of the critical items. To be on the safe
recently diagnosed epilepsy. As in our study, the difference side, it is possible to inform the caregiver that seizure symp-
between the standard and adjusted scores was evident toms should not be included in the rating. Austin et al. [15]
mainly for the narrowband scales (Attention Problems, instructed the parents not to include any behavior that
Withdrawal, and Thought Problems), but negligible for might belong to seizure semiology or relate to seizures.
the broadband scales (Internalizing Problems and Total Nevertheless, in their study, newly diagnosed children with
Problems). Their study and ours differ with respect to the epilepsy had higher levels of psychopathology than those
date of examination. At the time of preoperative examina- children from a general population.
tion, our patients had had epilepsy for several years, All in all, our results demonstrate that valid results can be
whereas Oostrom and colleagues’ patients were newly diag- obtained using the CBCL in children with epilepsy, at least
nosed. Directly after diagnosis, the effect of ambiguity was for those children who have had epilepsy over a longer per-
prominent in that study and decreased over time. The iod. The number of ambiguous items is small, and the bias
authors explained that this was due to: (1) the relatively caused by item ambiguity seems to be negligible. The super-
high frequency of seizures (antiepileptic drug treatment ordinate scales are only marginally influenced by the ambig-
had not yet begun) and (2) the increasing knowledge of uous items. Most discordant are the results obtained with an
parents, which, over time, helped them to differentiate adjusted version for the subscales Attention Problems and
between epilepsy symptoms and habitual behavior. In our Thought Problems. However, elevated scores on the Atten-
study, more than 50% of patients had intellectual disability tion Problems scale probably reflect real attention problems
or borderline intelligence. Elevated levels of behavior prob- and are not due mainly to confusion with seizures. The scale
lems have been reported in children with low IQ in the lit- Thought Problems should be interpreted with caution any-
erature [10,11]. In our sample, however, behavior problems way because of its low reliability [9]. The postoperative
were equally frequent in patients with average intelligence improvement in behavioral problems that has been reported
and patients with low IQ. Therefore, it can be regarded in previous studies (see, for instance, [8]) seems to be real. In
unlikely that our results are significantly influenced by most patients it is not due to disappearance of seizure-related
the low IQ of our patients. behavior after complete seizure relief.
Discordant classifications were found in our study, par-
ticularly for the Attention Problems and Thought Prob-
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