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Neurocognitive evaluation in children with occipital lobe epilepsy

Open ArchivePublished:January 20, 2012DOI:https://doi.org/10.1016/j.seizure.2011.12.015

      Abstract

      Purpose

      This study aimed to explore cognitive functions in patients with childhood epilepsy with occipital paroxysms (CEOP) and to compare the performance of these patients with that of patients with symptomatic occipital epilepsy (SOE) and healthy control subjects.

      Method

      Twenty-eight patients with epilepsy (17 CEOP, 11 SOE) were enrolled. The control group had similar demographical characteristics. Cognitive functions evaluated with Wechsler Intelligence Scale for Children-revised edition (WISC-R), The Visual Aural Digit Span (VADS) and Bender Visual Motor Gestalt Test (BVMG).

      Results

      The WISC-R showed lower performance IQ with WISC-R in patients with occipital epilepsy than in healthy controls. The VADS test only showed lower scores in children with symptomatic occipital epilepsy. Mean BVMG test scores were significantly abnormal in both subgroups of childhood epilepsy with occipital paroxysms (early-onset CEOP/late-onset CEOP) and the group with SOE.

      Conclusion

      Patients with CEOP, especially the late-onset form, have significant problems in the domains of visuomotor coordination, memory and attention. The academic performance of these patients should be monitored carefully in follow-up and appropriate educational support should be given as necessary.

      Keywords

      1. Introduction

      Childhood epilepsy with occipital paroxysms (CEOP) accounts for 20–28% of all cases of idiopathic partial epilepsy. The International League Against Epilepsy (ILAE) has recently divided childhood occipital epilepsies into early-onset benign childhood epilepsy (Panayiotopoulos type) and late-onset childhood occipital epilepsy (Gastaut type).
      • Engel J.J.
      International League Against Epilepsy (ILAE). A proposed diagnostic scheme for people with epileptic seizure and with epilepsy: report of the ILAE task force on classification and terminology.
      Early-onset benign childhood occipital epilepsy (Panayiotopoulos type) is characterized by non-visual symptoms including tonic head and eye deviation, ictal vomiting and seizures with or without partial status epilepticus.
      • Ferrie C.D.
      • Beaumanoir A.
      • Guerrini R.
      • Kivity S.
      • Vigevano F.
      • Takaishi Y.
      • et al.
      Early onset benign occipital seizure susceptibility syndrome.
      • Panayiotopoulos C.P.
      Early-onset benign childhood occipital seizure susceptibility syndrome: a syndrome to recognize.
      Seizure onset is between 1 and 12 years of age with a consistent median age of 5 years. Seizures can vary in duration from a few minutes to hours. The frequency of seizures is often low, with an average of 2–3 seizures.
      • Panayiotopoulos C.P.
      Benign childhood epilepsy with occipital paroxysms: a 15-year prospective study.
      • Caraballo R.H.
      • Cersosimo R.O.
      • Medina C.S.
      Idiophatic partial epilepsy with occipital paroxisms.
      Late-onset benign childhood occipital epilepsy (Gastaut type) is characterized by brief seizures with mainly visual symptoms, such as elementary visual hallucinations, illusions, or amaurosis, followed by hemiclonic seizures while awake. Ictal or postictal headaches occur in half of the patients, and the mean age at onset is 8.9 years. Interictal electroencephalograms (EEGs) reveal spikes or sharp and slow wave paroxysms on occipital regions that disappear with the opening of the eyes.
      • Gastaut H.
      A new type of epilepsy: benign partial epilepsy of childhood with occipital spikes-waves.
      • Gastaut H.
      • Roger J.
      • Bureau M.
      Benign epilepsy of childhood with occipital paroxysms up-date.
      The word “benign” is used because epileptic seizures spontaneously resolve by the end of adolescence and rarely reoccur. The absence of neurological and neuropsychological deficits was considered a pre-requisite for the diagnosis of benign partial epilepsies in childhood (CEOP, Rolandic epilepsy). However, recent studies report that neuropsychological problems may accompany these subgroup of epilepsy. Although there are numerous studies describing neurocognitive profiles in Rolandic epilepsy, similar studies in patients with CEOP are limited.
      • Gulgonen S.
      • Demirbilek V.
      • Korkmaz B.
      • Dervent A.
      • Townes B.D.
      Neuropsychological functions in idiopathic occipital lobe epilepsy.
      • Germanò E.
      • Gagliano A.
      • Magazù A.
      • Sferro C.
      • Calarese T.
      • Mannarino E.
      • et al.
      Benign childhood epilepsy with occipital paroxysms: neuropsychological findings.
      In this cross-sectional study we aimed to evaluate cognitive functions in children with CEOP.

      2. Materials and methods

      Seventeen patients with CEOP followed by the Ege University Hospital, Pediatrics Department, Division of Child Neurology (Izmir, Turkey) were enrolled in this study. They were diagnosed according to criteria defined by the International Classification of Epilepsy and Epileptic Syndromes.
      • Hauser W.A.
      • Annegers J.F.
      • Kurland L.T.
      Incidence of epilepsy and unprovoked seizure in Rochester, Minnesota:1935–1984.
      Patients with the following characteristics were selected:
      • Age over 6 years
      • Seizure-free for at least one month
      • Use of a single antiepileptic drug for treatment
      • Normal neurological examination
      • No use of medication except antiepileptic drugs
      • Presence of occipital or parieto-occipital sharp wave or sharp and slow wave activity on EEGs
      • Normal cranial MRI
      Ten patients (Group I) had findings compatible with early-onset CEOP, and seven patients (Group II) had late-onset CEOP. Eleven patients (Group III) with epileptic seizures who also had parieto-occipital focus and abnormal cranial radiological findings were considered to have symptomatic occipital epilepsy. The symptomatic group consisted of nine patients with hypoxic ischemic encephalopathy and two patients with cerebrovascular disease.
      Seventeen healthy school children (9 males and 8 females) were recruited as a healthy control group. The control group had similar demographical characteristics such as age, sex, and sociocultural levels.
      Routine waking and sleep EEGs were obtained from all patients. An international 10–20 electrode placement system was used. Data were recorded with reference electrodes placed on the earlobes. Hyperventilation and intermittent photic stimulation (IPS) were used as standard activation methods. IPS was performed with the strobe lamp placed 30 cm away from the patient's closed eyes. A range of 3–33 Hz was used. The duration of sleep EEGs varied between 45 and 60 min. Only stage I and II non-rapid eye movement sleep was recorded.
      Cranial MRIs were obtained from all patients using a Siemens 1.5 Tesla Magnetom Vision™ MRI Scanner (Erlangen, Germany). Spin-echo T1-weighted images (TR/TF/FA:630/14/70 ms) in the axial, sagittal and coronal planes, spin-echo T2-weighted images (TR/TE/T1/FA:11.52/60/400/180) in the axial plane, and FLAIR (fluid attenuated inversion recovery) (TR/TE/T1/FA:8000/110/2500/180) images were obtained.

      2.1 Neuropsychological tests

      Cognitive tests regarding visuospatial perception, memory, learning difficulties, and attention deficits were conducted. Performance subtests (matrix reasoning, picture completion, block design, and coding) of the Wechsler Intelligence Scale for Children Revised (WISC-R) were applied to all groups.
      • Wechsler D.
      Wechsler intelligance scale for children revised.
      • Savaşır I.
      • Şahin N.
      Wechsler Çocuklar İçin Zeka Ölçeği (WISC-R) El Kitabı.
      Visuomotor abilities were assessed with the Bender Visual Motor Gestalt Test.
      • Bender L.A.
      A visual motor gestalt test and its clinical use.
      All patients and controls received WISC-R performance subtests (picture completion, block design, matrix reasoning and coding). The Intelligence Quotient (IQ) was calculated according to these subtests.
      The Bender Gestalt Test, or the Bender Visual Motor Gestalt Test, is a psychological assessment instrument used to evaluate visual-motor functioning and visual perception skills in both children and adults. Scores on the test are used to identify possible organic brain damage and the degree maturation of the nervous system (“organicity”). The adult type Bender-Gestalt test was applied to patients who were older than 12 years of age. The number of patients given adult tests in Groups I, II, and III were 1, 2, and 3, respectively. The others received the Children's Bender–Gestalt test. The Visual Aural Digit Span Test (VADS) was used for the evaluation of verbal short-term memory function.
      • Karakaş S.
      • Yalın A.
      Görsel işitsel sayı dizileri testi B formu.
      The first subtest required oral repetition of orally presented digits. In the second subtest, subjects had to orally repeat digits presented visually. In the third subtest, the subjects wrote down digits that were presented orally. The fourth subtest involved writing digits that were presented visually.
      Parental informed consent and approval from the Ethics Committee were obtained for the study.

      2.1.1 Statistical analysis

      The Statistical Package for the Social Sciences software (SPSS 13.0 for Windows, SPSS, Inc., Chicago, IL) was used for statistical analyses. The data obtained were evaluated with the Chi-squared test, Kruskal Wallis test, Mann–Whitney U test. p < 0.05 was accepted as statistically significant. We did not carry out any procedures to reduce the risk of type I error due to multiple testing. The statistical tests were used in an explorative way. We applied pair-wise testing only post hoc, that is the test the significance of differences observed between the groups studied.

      3. Results

      The study included 10 patients with early-onset CEOP (aged between 6 and 13.5 years), seven patients with late-onset CEOP (aged between 9 and 16.5 years), and 11 patients with symptomatic occipital epilepsy (aged between 8 and 16.5 years). Demographic characteristics are shown in Table 1.
      Table 1Demographic findings of the patients.
      Group I (n = 10)Group II (n = 7)Group III (n = 11)
      The age of neurocognitive tests (year)8.39 SD ± 2.412.6 SD ± 2.910.8 SD ± 3
      The onset of seizures (year)5.03 SD ± 2.57.9 SD ± 25.4 SD ± 2.5
      Sex (F/M)6/44/36/5
      History of febrile seizures3 (30%)1 (14.3%)0
      Epilepsy history in the family1 (10%)01
      The total number of seizures
       6–20247
       2–6834
      The duration of seizures
       <5 min241
       5–30 min738
       >30 min102
      Semiology of seizures
       Visual hallucination066
       Ictal blindness022
       Deviation of the eyes827
       Otonomic symptoms611
       Ictal vomitting504
       Ictal behavioural changes451
       POSTICTAL headache110
       Impairment of consciousness834
       Hemi/generalized convulsions529
      Antiepileptic drugs
       Carbamazepine755
       Valproic acid321
       Polytherapy5
      Group I, Early-onset childhood occipital paroxysm; Group II, late-onset childhood occipital epilepsy; Group III, symptomatic occipital epilepsy; SD, Standard deviation.
      Age at seizure was significantly earlier in the early-onset group compared to the late-onset CEOP group (mean ± SD: 5.03 ± 2.5 years vs 7.9 ± 2 years, p = 0.009). A significant difference in the average age at diagnosis was observed between patients with early-onset CEOP and other groups (p = 0.006 and p = 0.023, respectively).
      All patients with occipital epilepsy had partial onset seizures. Simple partial, complex partial and secondarily generalized tonic–clonic seizures were described. Ictal vomiting was observed in 50% of patients with early-onset CEOP vs none of the patients with late-onset CEOP. Eye deviation was identified in 80% of cases with early-onset CEOP vs 28% of cases with late-onset CEOP. Temporary blindness, elementary visual hallucinations, and visual field defects were reported by in 85% of patients in both the late-onset CEOP group and the symptomatic group. Headaches were reported in 14.5% of patients with CEOP.
      Hemiclonic and secondary generalized tonic clonic seizures were detected more frequently (73%) in the symptomatic epilepsy group than the CEOP group. In the symptomatic epilepsy group, the duration of seizures and the ratio of non-responsiveness to treatment were also higher than in CEOP patients (p < 0.05).
      Carbamazepine or valproic acid were started as the first antiepileptic drug in all patients with CEOP. Antiepileptic drug treatment was still in use in 3 out of 10 patients with early-onset CEOP and 5 out of 7 patients with late-onset CEOP. In patients with symptomatic occipital epilepsy, carbamazepine and valproic acid were used together with other antiepileptic drugs such as topiramate, oxcarbazepine, and phenobarbital.
      EEG abnormalities of the patients with CEOP and symptomatic occipital epilepsy are shown in Table 2. Detected abnormalities were recurrent, of high amplitude (150–200 mV), and displayed sharp and slow wave series in the occipital regions. In early-onset CEOP cases, the presence of an extra parieto-occipital focus was significantly more frequent than in the late-onset CEOP and symptomatic epilepsy groups (p < 0.05).
      Table 2EEG findings of the patients.
      Occipital focusExtra-occipital focus
      UnilateralBilateral
      Group I (n = 10)824
      Group II (n = 7)521
      Group III (n = 11)743
      Group I, early-onset childhood occipital epilepsy; Group II, late-onset childhood occipital epilepsy; Group III, symptomatic occipital epilepsy.

      3.1 WISC-R performance subscores

      Although the mean IQ score of the late-onset CEOP (86 ± 14.8) group was lower than the mean IQ score of the early-onset CEOP group (98.9 ± 22.1), the difference was not statistically significant (p = 0.13). There was no significant difference between the late-onset CEOP group (86 ± 14.8) and the symptomatic group in terms of mean IQ scores (70 ± 20.8) (p = 0.56). Both the late-onset group and the symptomatic group had significantly lower IQ scores compared to the control group (103.1 ± 13.3) (p = 0.019 and p = 0.001, respectively). On the WISC-R, all of the CEOP patients had lower scores than the control group.

      3.2 Visual aural digit span test-revised (VADS-R)

      There was no significant difference between the subgroups of CEOP and healthy controls in terms of the results of the VADS-R (p > 0.05, Table 3). The VADS-R test showed lower scores only in children with symptomatic occipital epilepsy (p < 0.05).
      Table 3Comparison of Visual Aural Digit Span Test-Revised between the groups.
      Auditory visualAuditory writtenVisual auditoryVisual written
      Group I4.8 ± 1.165 ± 1.264.5 ± 0.85.1 ± 2
      Group II5.1 ± 1.065.2 ± 0.955.28 ± 1.15.85 ± 0.89
      Group (I + II)5 ± 15.1 ± 14.9 ± 15.5 ± 1.5
      Group III4.1 ± 14.4 ± 0.724.2 ± 0.974.66 ± 2
      Healthy controls5.47 ± 0.945.58 ± 0.875.17 ± 1.185.76 ± 1.25
      Group III-Healthy controls p< 0.05. Group I, early-onset childhood occipital paroxysm; Group II, late-onset childhood occipital epilepsy; Group III, symptomatic occipital epilepsy; SD, standard deviation.

      3.3 Bender gestalt test

      The mean value of the Bender–Gestalt test results of the patients and the control group are shown in Table 4. Both the early-onset and late-onset groups had significantly lower scores of Bender–Gestalts test compared to the control group (p > 0.05). As expected, when comparing the symptomatic group with the control group, the symptomatic group had lower scores of Bender–Gestalt which might be indicative of “organicity” (p = 0.001). However, there were no significant differences between the late-onset group and the symptomatic group in terms of B–G test results (p > 0.05).
      Table 4The comparison of the results of Bender-Gestalt test between groups.
      Group I n = 10Group II n = 7Group III n = 11Healthy controls n = 17
      Normal73117
      Abnormal32
      Organicity318
      Group I, Early-onset childhood occipital paroxysm; Group II, late-onset childhood occipital epilepsy; Group III, symptomatic occipital epilepsy.
      There was no correlation between the cognitive test results and the parameters age at onset of seizures, duration of seizures, the presence of extra-occipital EEG abnormalities and the type of antiepileptic treatment used (p > 0.05).

      4. Discussion

      Only a small number of studies describing the neurocognitive status of patients with CEOP have been published.
      • Bourgeois B.F.
      • Prensky A.L.
      • Palkes H.S.
      • Talent B.K.
      • Busch S.G.
      Intelligence in epilepsy: a prospective study in children.
      • Elienberg J.
      • Hirtz D.G.
      • Nelson K.B.
      Do seizures in children cause intellectual deterioration?.
      • Rodin E.A.
      • Schmaltz S.
      • Twitty G.
      Intellectual functions of patients with childhood-onset epilepsy.
      • Ay Y.
      • Gokben S.
      • Serdaroglu G.
      • Polat M.
      • Tekgul H.
      • Solak U.
      • et al.
      Neuropsychologic impairment in children with rolandic epilepsy.
      • Croona C.
      • Kihlgren M.
      • Lundberg S.
      • Eeg-Olofsson O.
      • Eeg-Olofsson K.E.
      Neuropsychological findings in children with benign childhood epilepsy with centrotemporal spikes.
      • Wirrell E.C.
      • Camfield P.R.
      • Gordon K.E.
      • Dooley J.M.
      • Camfield C.S.
      Benign rolandic epilepsy: atypical features are very common.
      • Heijbel J.
      • Bohman M.
      Benign epilepsy of children with centrotemporal EEG foci: intelligence, behavior, and school adjustment.
      Two of these studies evaluated only those patients with early-onset CEOP.
      • Wolff M.
      • Weiskopf N.
      • Serra E.
      • Preissl H.
      • Birbaumer N.
      • Kraegeloh-Mann I.
      Benign partial epilepsy in childhood: selective cognitive deficits are related to the location of focal spikes determined by combined EEG/MEG.
      • Hirano Y.
      • Oguni H.
      • Funatsuka M.
      • Imai K.
      • Osawa M.
      Neurobehavioral abnormalities may correlate with increased seizure burden in children with panayiotopoulos syndrome.
      In this study we investigated both groups of CEOP (early- and late-onset) separately.
      The results for the WISC-R performance test revealed that all of the CEOP patients had lower scores compared to the control group. However, this was not statistically significant. In the study by Gulgonen et al.,
      • Gulgonen S.
      • Demirbilek V.
      • Korkmaz B.
      • Dervent A.
      • Townes B.D.
      Neuropsychological functions in idiopathic occipital lobe epilepsy.
      performance IQ scores were found to be lower in patients with CEOP, similar to our study, although the difference in the scores in that study was not significant. In another study that examined children with occipital sharp waves, the Kaufman-Assessment (K-ABC) test was used to measure IQ. While abnormalities in global IQ and language were not detected, a significantly decreased ability to perform visual transformation tasks was detected.
      • Wolff M.
      • Weiskopf N.
      • Serra E.
      • Preissl H.
      • Birbaumer N.
      • Kraegeloh-Mann I.
      Benign partial epilepsy in childhood: selective cognitive deficits are related to the location of focal spikes determined by combined EEG/MEG.
      When children with CEOP were divided into early-onset and late-onset groups, the IQ scores of patients in the early-onset group were found to be lower. Similarly, in another study, a statistically insignificant lower performance was observed in the IQ scores of these patients. However, in that study, these patients had significantly lower verbal IQ scores compared to the control group. In another recent study, in which Hirano et al. evaluated patients with late-onset CEOP, neurobehavioral disorders, borderline mental retardation and a significant discrepancy in verbal vs performance IQ scores were found.
      • Hirano Y.
      • Oguni H.
      • Funatsuka M.
      • Imai K.
      • Osawa M.
      Neurobehavioral abnormalities may correlate with increased seizure burden in children with panayiotopoulos syndrome.
      We found that, in late-onset CEOP patients, the performance IQ scores and scores of subtests such as picture completion and matrix reasoning were significantly lower than the corresponding scores of the control group. We conclude that visuo-spatial perception in late-onset CEOP patients is affected significantly more than in early-onset CEOP patients.
      We also performed the Bender–Gestalt motor perception test, which is used for the evaluation of visuo-motor perception, of visuo-motor functions, and for rapid measurement of cognitive development. This test is also frequently used for differentiation of special learning disability and to provide a measure of “organicity”.
      • Bender L.
      A visual motor gestalt test and its clinical use.
      According to the results of the Bender Gestalt test, the ratio of “organicity” in both early-onset and late-onset CEOP patients was higher than in the control group. Abnormal performance IQ scores and abnormalities in the Bender-Gestalt test results were more frequently detected in late-onset CEOP patients than in early-onset CEOP patients.
      Jambaque et al.
      • Jambaque I.
      Verbal and visual memory impairment in children with epilepsy.
      reported abnormalities in visual and auditory memory in various epilepsy patients. There are two studies about this subject in the literature, and both involve patients with occipital epilepsies with a benign course. In a study by Gulgonen et al.,
      • Gulgonen S.
      • Demirbilek V.
      • Korkmaz B.
      • Dervent A.
      • Townes B.D.
      Neuropsychological functions in idiopathic occipital lobe epilepsy.
      abnormalities were found not only in the visual field but also in attention, memory and verbal abilities. They suggested that this was due to the effects of subclinical epileptic discharges that propagate globally in the brain instead of only in the parietal and occipital lobes. In a study by Germano et al.
      • Germanò E.
      • Gagliano A.
      • Magazù A.
      • Sferro C.
      • Calarese T.
      • Mannarino E.
      • et al.
      Benign childhood epilepsy with occipital paroxysms: neuropsychological findings.
      involving early-onset CEOP, the authors detected abnormalities in both verbal and visuo-spatial memory tests.
      Hirano et al.
      • Hirano Y.
      • Oguni H.
      • Funatsuka M.
      • Imai K.
      • Osawa M.
      Neurobehavioral abnormalities may correlate with increased seizure burden in children with panayiotopoulos syndrome.
      classified early-onset CEOP into three groups according to the number of seizures. Group 1 had 1–5 seizures, group 2 had 6–9 seizures, and group 3 had more than 10 seizures. No differences were found in the verbal performance in the three groups. However, the authors reported an increased frequency of neurobehavioral disorders in group 3. In our study, we did not find any significant association between seizure frequency or seizure duration and cognitive performance. We also did not find any relationship between the location of epileptic discharges and neurocognitive test results.
      The type of antiepileptic drug used is another factor that has an effect on cognitive test scores in patients with epilepsy. Various studies have reported the adverse effects of antiepileptic drugs.
      • Mandelbaum D.E.
      • Burack G.D.
      The effect of seizure type and medication on cognitive and behavioral functioning in children with idiopathic epilepsy.
      • Vining E.P.
      Cognitive dysfunction associated with antiepileptic drug therapy.
      • Matthews C.G.
      • Harley J.P.
      Cognitive and motor-sensory performances in toxic and nontoxic epileptic subjects.
      Germano et al.
      • Germanò E.
      • Gagliano A.
      • Magazù A.
      • Sferro C.
      • Calarese T.
      • Mannarino E.
      • et al.
      Benign childhood epilepsy with occipital paroxysms: neuropsychological findings.
      reported subtle neuropsychological deficits in their patients, but the majority of these patients were taking phenobarbital or vigabatrin.
      • Germanò E.
      • Gagliano A.
      • Magazù A.
      • Sferro C.
      • Calarese T.
      • Mannarino E.
      • et al.
      Benign childhood epilepsy with occipital paroxysms: neuropsychological findings.
      All of our CEOP patients were taking monotherapy of either valproate or carbamazepine. In our patients, serum antiepileptic drug levels were within usual therapeutic ranges, and we did not observe any evidence of toxic effects during the study period. This makes it less likely that antiepileptic drugs had a significant effect on cognitive functioning in our patients.
      The number of tests for evaluating the cognitive functions in epileptic children is important. Although performed tests evaluated visuo-spatial perception, visuo-motor functions, attention, and visual and auditory memory, more detailed cognitive tests evaluating academic success, verbal performance, verbal memory, and language development are required. In previous studies, the cognitive functions of CEOP patients of all ages or only early-onset CEOP patients were evaluated. In this study late-onset CEOP patients were investigated separately with neurocognitive tests. One limitation to our study may be the small small sample size.
      In conclusion, this study suggests that healthcare professionals need to have a greater awareness of possible neuropsychological impairments in patients with both early-onset and late-onset CEOP. This may help patients to secure appropriate support without delay and to achieve their academic potential.

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