Journal http://jcn.sagepub.com/ of Child Neurology
Temporal Lobe Epilepsy in Childhood: Comprehensive Neuropsychological Assessment Catarina A. Guimarães, Li M. Li, Patrícia Rzezak, Daniel Fuentes, Renata C. Franzon, Maria Augusta Montenegro, Fernando Cendes, Sigride Thomé-Souza, Kette Valente and Marilisa M. Guerreiro J Child Neurol 2007 22: 836 DOI: 10.1177/0883073807304701 The online version of this article can be found at: http://jcn.sagepub.com/content/22/7/836
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Original Article
Temporal Lobe Epilepsy in Childhood: Comprehensive Neuropsychological Assessment
Journal of Child Neurology Volume 22 Number 7 July 2007 836-840 © 2007 Sage Publications 10.1177/0883073807304701 http://jcn.sagepub.com hosted at http://online.sagepub.com
Catarina A. Guimarães, PhD, Li M. Li, MD, PhD, Patrícia Rzezak, BSc, Daniel Fuentes, PhD, Renata C. Franzon, MD, PhD, Maria Augusta Montenegro, MD, PhD, Fernando Cendes, MD, PhD, Sigride Thomé-Souza, MD, Kette Valente, MD, PhD, and Marilisa M. Guerreiro, MD, PhD
The neuropsychological features of children with temporal lobe epilepsy are not yet well defined. The aim of this study was to identify the neuropsychological deficits in children with temporal lobe epilepsy. We evaluated 25 patients and compared them with 25 normal children. All children underwent a comprehensive neuropsychological assessment. We found a significant difference in favor of the control group in the following measures: IQ; forward digit; Trail Making Test for Children B; Wisconsin Card Sorting Test; block design; Boston naming test, verbal fluency; and Wide Range Assessment of Memory and Learning
verbal learning, visual learning, verbal memory, visual memory, delayed recall of verbal learning, delayed recall of stories, and recognition of stories. Our findings show that children with temporal lobe epilepsy present with several neuropsychological deficits, despite normal IQ. These findings point to a dysfunction of cerebral areas other than temporal lobe, particularly the frontal lobes.
A
between the localization of the lesion and performance on memory tests is also not well established.18,19 Spectroscopy appears to provide a good correlation between unilateral temporal injury and specific cognitive verbal and nonverbal dysfunction.20 When compared with normal controls, children with temporal lobe epilepsy can show specific memory deficits according to the hemispheric specialization.21-24 This finding means that verbal memory is impaired in children with left temporal lobe epilepsy and visual memory is impaired in children with right temporal lobe epilepsy—a classic finding of memory dysfunction. Other studies, however, found a poor visual memory performance when patients with right mesial temporal sclerosis were assessed, and no difference was detected when verbal tests were used on patients with left mesial temporal sclerosis.25,26 These findings are not in keeping with recent studies in adults, as higher sensitivity is found in verbal memory tests that usually assess left temporal lobe injury.2-4,10-12,27,28 Nevertheless, other studies found no deficit in specific memory.18,29-33 Language disturbance, IQ lower than controls, and deficits in executive functions have also been found in children with temporal lobe epilepsy.18,34,35 Considering the lack of clear-cut data about the neuropsychological profile of children with temporal lobe epilepsy, our aim was to identify the neuropsychological deficits in this population.
dults with temporal lobe epilepsy often present with cognitive deficits of memory and language.1,2 The classic model of material-specific memory supposes that a lesion in, or resection of, the hippocampus of the language-dominant hemisphere usually suggests a verbal memory disturbance,3,4 while damage of the nondominant hemisphere hippocampus may result in visual memory disturbance.5-9 More recent studies, however, have shown that memory deficits seem to be a common finding in patients with temporal lobe epilepsy, especially if the left temporal lobe or both temporal lobes are damaged.2-4,10-13 Those patients may also present with naming problems.1,2 In addition to memory and language deficits, executive dysfunction may be found in patients with temporal lobe epilepsy.4,14-16 Temporal lobe epilepsy in childhood has a wide range of clinical-electroencephalographic presentation.17 In addition, the neuropsychological features in childhood temporal lobe epilepsy are not yet well defined. The relationship From the Department of Neurology, State University of Campinas, São Paulo (CAG, LML, RCF, MAM, FC, MMG), and Institute of Psychiatry, University of São Paulo (PR, DF, ST-S, KV), Brazil. Address correspondence to: Marilisa M. Guerreiro, MD, PhD, Department of Neurology–FCM–UNICAMP, PO Box 6111, 13083-970 Campinas, SP, Brazil; e-mail:
[email protected]. Guimarães CA, Li LM, Rzezak P, et al. Temporal lobe epilepsy in childhood: comprehensive neuropsychological assessment. J Child Neurol. 2007;22:836-840.
Keywords: neuropsychology; epilepsy; temporal lobe epilepsy; memory; executive functions
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Temporal Lobe Epilepsy in Childhood / Guimarães et al
Methods
837
Statistical Analysis
Patients We evaluated 25 children with temporal lobe epilepsy. Inclusion criteria were diagnosis of temporal lobe epilepsy based on clinical, electroencephalogram (EEG), and magnetic resonance imaging (MRI) findings with hippocampal atrophy or temporal cortical lesions; age from 7 to 15 years and 11 months; normal neurological examination results including brief visual and auditory ability; estimate IQ ≥ 70; and signature of informed consent. Exclusion criteria were normal MRI results, MRI showing extratemporal lesion, signs or symptoms of antiepileptic intoxication, children who had never attended regular school, and severe behavior disorder. Considering that there are no normative data for the Brazilian population, the data collected from the patients were compared with that collected from a control group. Control Group Twenty-five normal children were compared with the subjects. Inclusion criteria were similar age, gender, socioeconomic and educational level, and signature of informed consent. Most children of the control group were schoolmates of our patients. Exclusion criteria were children who were relatives of the index patients; estimate IQ lower than 70; use of medication with an effect on the central nervous system; children who never attended school; past history of neurological injury, such as trauma and meningitis; abnormal neurological examination results; and history of pervasive disorders. Therefore, the control group was composed of normal children from a similar sociocultural level as our patients and whose parents allowed them to participate in the study. The assessment included (1) neurological evaluation: medical history, neurological examination, serial EEGs, and video EEG; (2) neuroimaging investigation: MRI was performed using a 2-Tesla scanner (Elscint Prestige) with T1and T2-weighted acquisitions in 3 orthogonal planes or a 1.5-Tesla scanner (GE–Horizon LX 8.3, Medical Systems, Milwaukee, Wis); and (3) neuropsychological examination to assess intellectual level, attention, visual perception, handedness, executive function, visuoconstructive praxis, language, and memory (verbal, visual, and learning). The tests used were (1) Edinburgh Handedness Inventory36 and dichotic listening tests37 to determine hemispheric dominance for language; (2) Wechsler Intelligence Scale for Children, Third Edition (WISC-III)38,39: subtests of block design and vocabulary to estimate IQ; (3) Perception of shapes and colors37; (4) Wisconsin Card Sorting Test40; (5) Trail Making Test for Children A and B37; (6) Digit span (subtest of WISC-III)38; (7) Wide Range Assessment of Memory and Learning41; (8) Block design (subtest of WISCIII)38; (9) Verbal Fluency Test (category: foods)37; and (10) Boston Naming Test.37,39,42
A general descriptive demographic analysis of the data was carried out. The χ2 and Fisher exact tests were used to compare proportions and assess significance of associations among the variables, and the Mann-Whitney test was applied to assess rank difference of data distribution between the 2 groups. The level of significance was set at P < .05.
Results The mean age of epilepsy onset in the patients was 4.6 years (SD, 2.9), and mean age of duration of epilepsy was 8.0 years (SD, 4.0). There were 6 children (24%) who had their seizures controlled for more than 1 year, 8 (32%) had 1 seizure per month, 9 (36%) had 2 to 10 seizures per month, and 2 (8%) had more than 10 seizures per month. A total of 14 children (56%) were using monotherapy and 11 (44%) polytherapy. A history of febrile seizure was found in 14 children (56%). Status epilepticus occurred in 16 children (64%). The MRI findings showed 16 children (64%) had hippocampal atrophy and 9 (36%) had temporal cortical lesions. A total of 14 children (56%) had their lesions on the right temporal lobe, 9 (36%) on the left, and 2 (8%) had bilateral lesions. Both the patient and control groups showed homogeneous characteristics in gender (P = .77, χ2 test), age (P = .86, Mann-Whitney test), schooling (P = .21, MannWhitney test), handedness (P = 1.00, Fisher exact test), and dichotic listening test (P = .86, Fisher exact test). None of the subjects in either group had mistakes in shape and color perception tests. Table 1 presents a descriptive analysis (mean, standard deviation) of the neuropsychological tests and the comparison between them in both groups (P value, Mann-Whitney test). We found a significant difference in favor of the control group in the following measures: IQ; forward digit (WISC-III); Trail Making Test for Children B (time); Wisconsin Card Sorting Test rights, errors, perseverative errors, perseverative responses, number of categories; block design (WISC-III); Boston naming test, verbal fluency (foods); and Wide Range Assessment of Memory and Learning verbal learning, visual learning, verbal memory, visual memory, delayed recall of verbal learning, delayed recall of stories (verbal), and recognition of stories (verbal). The group made no mistakes in the Trail Making Test for Children A, so the item errors of the Trail Making Test for Children A could not be calculated.
Discussion Our findings showed that children with temporal lobe epilepsy present with several neuropsychological deficits.
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Journal of Child Neurology / Vol. 22, No. 7, July 2007
Table 1.
Performance on the Neuropsychological Assessment by Patients With Temporal Lobe Epilepsy (n = 25) and Controlsa (n = 25) Patients, Mean (SD)
Estimated IQ (WISC-III) Forward Digit (WISC-III) Backward Digit (WISC-III) Digit total (WISC-III) TMT A time TMT A errors TMT B time TMT B errors WCST rights WCST errorsa WCST categories WCST perseverative errorsa WCST nonperseverative errorsa WCST perseverative responsesa WCST failures to maintain seta Block Design (WISC-III) Boston naming test Verbal fluency test (foods) Verbal learning (WRAML) Visual learning (WRAML) Verbal memory (WRAML) Visual memory (WRAML) Delayed recall of verbal learning (WRAML)a Delayed recall for stories (WRAML)a Delayed recall of visual learning (WRAML)a Recognition of stories (WRAML)a
96.4 6.8 4.4 11.2 53.8 0.6 111.1 1.2 74.5 53.5 3.9 33.0 20.4 39.6 1.2 31.4 40.6 10.9 37.1 24.3 46.8 70.6 1.8
(13.3) (1.9) (2.0) (3.3) (63.6) (1.0) (159.8) (1.8) (20.4) (20.4) (2.6) (23.4) (13.4) (32.5) (1.1) (18.3) (8.8) (3.2) (7.9) (10.0) (16.2) (13.6) (1.7)
4.6 (3.1) 0.2 (1.6) 9.2 (3.2)
Controls, Mean (SD) 109.7 7.9 5.2 13.1 27.1 0 45.8 0.4 94.2 33.8 7.0 17.7 16.1 20.0 1.3 41.6 48.8 14.1 42.4 31.4 69.7 87.0 0.6
(11.7) (1.9) (1.5) (2.8) (13.0) (0) (24.9) (0.6) (15.2) (15.2) (2.3) (8.0) (8.7) (9.1) (1.1) (16.5) (7.0) (3.1) (6.0) (9.9) (11.7) (9.8) (1.0)
2.8 (3.2) 0.3 (1.1) 12.6 (1.4)
P Value (Mann-Whitney) .0013 .0386 .1503 .0645 .0546 – .0133 .0552 .0008 .0008 .0002 .0020 .2103 .0046 .9435 .0396 .0012 .0020 .0053 .0254 < .0001 < .0001 .0033 .0060 .9840
