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ORIGINAL ARTICLE |
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| Year : 2014 | Volume
: 9
| Issue : 2 | Page : 105-109 |
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Clinical characteristics and outcome of children with electrical status epilepticus during slow wave sleep
Sanem Yilmaz, Gul Serdaroglu, Ayfer Akcay, Sarenur Gokben
Department of Pediatrics, Division of Child Neurology, Ege University Medical Faculty, Izmir, Turkey
| Date of Web Publication | 21-Aug-2014 |
Correspondence Address:
Sanem Yilmaz
Department of Pediatrics, Division of Child Neurology, Ege University Medical Faculty, Bornova 35100, Izmir
Turkey
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/1817-1745.139266
 Abstract | | |
Background: Electrical status epilepticus in slow wave sleep (ESES) is a rare, age-related, self-limited disorder characterized as epilepsy with different seizure types, neuropsychological impairment in the form of global or selective regression of cognitive functions, motor impairment, and typical electroencephalographic (EEG) findings of continuous epileptic activity occupying 85% of nonrapid eye movement sleep. Aims: The aim is to examine the clinical and electrophysiological findings and treatment modalities of children with ESES and to evaluate the outcome of the disorder. Materials and Methods: Fourteen patients with a diagnosis of electrical status epilepticus during slow wave sleep and followed-up at least 2 years were included. Statistical Analysis: Pearson correlation test was used in the study. Results: Among the 14 patients, eight of them had normal mental development before ESES. Twelve of the patients mentioned cognitive impairment and decline in school performance during ESES. After ESES, seven patients had mental retardation in different severity. One of these patients was diagnosed with benign partial epilepsy of childhood with centrotemporal spikes and had normal intelligence quotient level prior to ESES. The diagnosis of ESES was made after newly occurred different seizure types in four of the patients while two of the previously known epileptic patients presented with only severe psychiatric impairment. Valproic acid and carbamazepine were the mostly frequently used drugs before the onset of ESES. After at least 2 years of follow-up, seven patients were seizure free, but still taking antiepileptic treatment. Five patients were seizure free, while two of them had ongoing seizures despite antiepileptic therapy. Conclusion: ESES should be kept in mind in children with unexplained regression or stagnation of development associated with seizures or not. Sleep EEGs should be performed for timely diagnosis, proper treatment and prevention of permanent cognitive impairment.
Keywords: Cognition, electrical status epilepticus during slow wave sleep, outcome, seizure, treatment
How to cite this article:
Yilmaz S, Serdaroglu G, Akcay A, Gokben S. Clinical characteristics and outcome of children with electrical status epilepticus during slow wave sleep. J Pediatr Neurosci 2014;9:105-9 |
| Introduction | |  |
Continuous spikes and waves during sleep was first described by Patry et al. in 1971 as a subclinical ''electrical status epilepticus'' induced by sleep in children. [1] The syndrome was then acknowledged by the International League Against Epilepsy (ILAE, 1989). According to the last ILAE proposal, the syndrome is defined as an age-related, self-limited disorder characterized as epilepsy with different seizure types, neuropsychological impairment in the form of global or selective regression of cognitive functions, motor impairment, and typical electroencephalographic (EEG) findings of continuous epileptic activity occupying 85% of nonrapid eye movement (REM) sleep. The term ''continuous spikes and waves during slow sleep'' is synonymous for electrical status epilepticus in slow wave sleep (ESES). [2] Epileptic encephalopathy with ESES is defined as a functional disorder of childhood with the following characteristics: Severe EEG disturbance occupying at least 85% of sleep, seizures, behavioral deterioration, no demonstrable brain pathology and stabilization or improvement of behavior once the EEG abnormality resolves. [3]
The condition is age-dependent and self-limited. The interval between the first seizure and electrical status epilepticus in sleep onset is usually 1-2 years with a peak at age 8 years. [4]
Seizures, cognitive and motor impairment are the cardinal features of electrical status epilepticus in sleep. Different seizure types, including generalized tonic clonic, typical absence, atypical absence, simple and complex partial seizures can occur, but tonic seizures are not seen. [5] Electrical status epilepticus in sleep and the IQ levels consists of sleep-induced continuous paroxysmal discharges of spike-wave complexes with a frequency of 1.5-2.5 Hz persisting through all the slow sleep stages. [1]
Electrical status epilepticus in sleep can last for several months or years, but resolves before adulthood. The early diagnosis of electrical status epilepticus in sleep is essential since there is a significant correlation between permanent cognitive impairment and delayed diagnosis. The aim of the current study is to examine the clinical characteristics of 14 children with ESES syndrome and to evaluate the outcome of the disease.
| Materials and Methods | | |
The clinical and electrophysiological findings of 14 patients (male = 8, female = 6) with the diagnosis of ESES and followed-up at least 2 years are presented.
Age of seizure onset, family history of epilepsy, seizure types, medication before and after electrical status epilepticus in sleep, awake and sleep EEG findings before electrical status epilepticus in sleep, interval between the first seizure and the development of electrical status epilepticus in sleep, behavioral problems, intelligence quotient (IQ) of all the patients were recorded.
Electroencephalographic recordings were done during awake, transition to sleep and sleep in every patient. The duration of sleep EEGs was at least 2 h including Stage I and II of nonREM sleep. An international 10-20 electrode placement system was used. Data were recorded with the placement of reference electrodes on the earlobes. Hyperventilation and intermittent photic stimulation were used as standard activation methods. Intermittent photic stimulation was performed with the strobe lamp placed 30 cm away from the patient's closed eyes. We used a range of 3-33 Hz. All EEGs were evaluated by one of two authors (SG and GS). Inclusion criteria were the finding of continuous spike wave index while >85% of slow-wave sleep over a period of 1 month. The degree of epileptic activity during sleep was measured and expressed as an index (spike wave index), which is defined as the total duration of continuous epileptic (diffuse slow spike wave) activity relative to total slow sleep duration with the exception of the REM phase.
Cognitive functions were evaluated both in the beginning and after the period of ESES. The patients were tested for intelligence quotient assessment with Stanford-Binet scales. Mental retardation was classified as mild, moderate or severe. Levels for mental retardation were as follows; mild retardation 55-69; moderate retardation 40-54 and severe retardation 30-39.
Pearson correlation test examined the associations between age at electrical status epilepticus in sleep onset, duration of electrical status epilepticus in sleep and the iq levels.
| Results | | |
The clinical and EEG characteristics of the patients are summarized in [Table 1]. The sex ratio was 1.3:1 (8 = male, 6 = female). The age at seizure onset ranged between 1 and 9 years, the mean age was 4.5 years (standard deviation: ±2.4 years). Six of the patients had a history of perinatal asphyxia and had motor mental impairment prior to electrical status epilepticus in sleep. Two patients (patient 2, 7) had epilepsy with unknown etiology and had normal development before electrical status epilepticus in sleep. Six of the patients were diagnosed with idiopathic partial epilepsy; four of them were benign partial epilepsy of childhood with centrotemporal spikes, and two of them were childhood epilepsy with occipital paroxysms. These patients had normal development before electrical status epilepticus in sleep. | Table 1: Clinical and electroencephalographical features and outcome of the patients
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Cranial magnetic resonance imaging of the patients with a history of prematurity and asphyxia revealed periventricular leukomalacia, cortical atrophy and gliotic lesions respectively. The other patients had normal cranial magnetic resonance imagings.
Seizure types before electrical status epilepticus in sleep were complex partial seizures, focal motor seizures and generalized tonic clonic seizures in 21.4%, 50% and 28.6% of the patients respectively. The history of epilepsy among the first or second degree relatives was positive in 46% of the patients.
There was no relation between the bilaterality of epileptogenic foci and progression into electrical status epilepticus in sleep (P > 0.05).
The mean age of developing electrical status epilepticus in sleep was 7.14 ± 2.1 years. The interval between the first seizure and developing electrical status epilepticus in sleep was 2.64 ± 1.74 years. The duration of electrical status epilepticus in sleep ranged between 3 and 43 months. The mean duration of electrical status epilepticus in sleep was 16.7 ± 11 months. The duration of follow-up was at least 2 years and ranged between 2 and 4 years after ESES.
Some of the patients had additional seizure types during electrical status epilepticus in sleep period. Three of the patients had absence seizures (patient 1, 2, 10) and one patient had versive seizures (patient 7) after electrical status epilepticus in sleep development. Ten of the patients had the same kind of seizures prior to electrical status epilepticus in sleep.
Eight of the patients had normal IQ levels before electrical status epilepticus in sleep. Mild and moderate mental retardation was determined in four and two patients respectively. During electrical status epilepticus in sleep twelve of the patients mentioned cognitive impairment and decline in school performance, only two patients (patient 3, 12) did not have cognitive impairment. Patient 2, 7, 8, 9, 10 and 13 had normal IQ levels before electrical status epilepticus in sleep, but had cognitive impairment during electrical status epilepticus in sleep. There was no statistically significant relation between the age at onset of electrical status epilepticus in sleep and IQ levels. Also, there was no statistically significant relation between the duration of electrical status epilepticus in sleep and IQ levels (P > 0.05).
Hyperactivity (n = 4), aggressivity (n = 4), depression (n = 3), hypersomnia (n = 1) and behavioral changes (n = 1) were determined in patients during electrical status epilepticus in sleep period. Two of the previously known epileptic patients (patient 1, 2) presented with only severe psychiatric impairment at the onset of electrical status epilepticus in sleep. They had disorganized and disruptive behavior such as urination on the floor, putting rubbish into the refrigerator and beating up the mother. The EEGs revealed electrical status epilepticus in sleep pattern, while they didn't have any clinical seizures which could be a clue for the onset of electrical status epilepticus in sleep.
Antipsychotic drugs (risperidone) were used in three patients (patient 1, 2, 11) and selective serotonin reuptake inhibitor was used in one patient (patient 7).
Valproic acid and carbamazepine were the most commonly used drugs before the onset of electrical status epilepticus in sleep. Valproic acid was used in 64.3% of the patients; carbamazepine was used in 50% of the patients.
Topiramate, corticosteroids, levetiracetam, and ethosuximide were used in 50%, 36%, 21.4% and 21.4% of the patients respectively during ESES period.
Four patients (patient 3, 8, 10, 13) were diagnosed with benign partial epilepsy of childhood with centrotemporal spikes. Patients 8 and 10 diagnosed with benign partial epilepsy of childhood with centrotemporal spikes were using carbamazepine before electrical status epilepticus in sleep. The medication was changed to valproic acid and then combined with topiramate in patient 8, but the electrical status epilepticus in sleep pattern did not change and corticosteroid was added. Corticosteroid was successful, but seizures were continued and levetiracetam was also added after the improvement of electrical status epilepticus in sleep.
In patient 10 carbamazepine was changed to ethosuximide. Patients 3, 13 were using valproic acid before development of electrical status epilepticus in sleep; it was changed to topiramate in both patients.
In two patients diagnosed with childhood epilepsy with occipital paroxysms, carbamazepine was changed to valproic acid; and in the other patient carbamazepine was changed to valproic acid and topiramate respectively. Topiramate was used in patients 1 and 2, but it failed in those patients. Levetiracetam was used in patients 6, 7, and 14. It was combined with corticosteroids in two of those patients.
The etiology was unknown in patient 7. The duration of electrical status epilepticus in sleep was 24 months in this patient. She was given corticosteroid and electrical status epilepticus in sleep pattern improved, but she still has seizures and focal epileptic activity in her EEG.
Topiramate and corticosteroids were the most used agents during electrical status epilepticus in sleep period and disappearing of EEG findings was achieved.
Regarding final outcome, seven patients were seizure free but still taking antiepileptic treatment in order to complete 2 years seizure free period. Five patients were seizure free, and their EEGs became normal and their treatment was discontinued. Only two patients still have seizures and are taking antiepileptic therapy. EEGs are completely normal in seven patients (patient 1, 3, 4, 9, 10, 11, 13).
| Discussion | | |
According to the literature approximately 25% of the patients with electrical status epilepticus in sleep have evidence of preexisting brain damage. [5] Forty-three percent of our patients had a history of perinatal asphyxia and had motor mental impairment prior to electrical status epilepticus in sleep. Their magnetic resonance imagings revealed cortical atrophy, periventricular leukomalacia and gliotic lesions. Electrical status epilepticus in sleep can be seen in association with idiopathic partial epilepsies, either the atypical form of benign partial epilepsy with centrotemporal spikes or benign childhood epilepsy with occipital paroxysms. [6],[7] Six of our patients had idiopathic partial epilepsy. The final outcome of these patients was good except one. One patient diagnosed with benign partial epilepsy of childhood with centrotemporal spikes had permanent cognitive impairment.
Most of the patients present with seizures that are typically nocturnal partial motor or generalized. The absence of the tonic seizures is one of the major features of this syndrome. Most of our patients had partial seizures before electrical status epilepticus in sleep period, but additional seizure types like absence seizures and versive seizures were recognized during electrical status epilepticus in sleep period in four of them.
The rate of maturation of the cortical network of the brain is high between the ages of 1 and 8. Disturbances during this period may result in permanent impairment of this network. Scholtes et al. [8] reported that if the epileptic disturbance occurs earlier the functional deficit should be greater. However, in our small patient group we could not find any significant relation between the age of ESES onset and IQ levels as well as the duration of ESES and IQ levels.
Almost half of the patients exhibited other cognitive deficits, such as attention deficit, language disturbances, hyperactivity and behavior problems. Apraxia, hemineglect, dyscalculia, intellectual decline, aggressiveness, encopresis, enuresis, emotional lability, psychotic behavior, anxiety and phobias as well as autistic-like behavioral features have also been described. [9],[10],[11],[12] Raha et al. [3] reported the behavior and academic performance of 14 patients with ESES. They found that 91% of their patients had behavioral issues most prominent being hyperactivity. Furthermore, 53% of their patients showed borderline to moderate cognitive impairment. Liukkonen et al. [13] followed-up 32 children at least 3 years and they reported that only one-third of children with ESES has favorable long-term cognitive outcome without permanent deterioration of cognitive level. Three of our patients had serious psychiatric problems, and they had to use antipsychotic drugs. Half of our patients were seizure free, but still taking antiepileptic treatment. Five patients were seizure free, and their EEGs became normal and their treatment was discontinued. Only two patients still have seizures and are taking antiepileptic therapy.
The pattern of continuous spike wave resolved completely in half of our patients. Before electrical status epilepticus in sleep, the most frequent EEG abnormality was focal epileptiform activity, but there was no relation between the bilaterality of epileptogenic foci and progression into electrical status epilepticus in sleep. Saltik et al. [14] have reported 16 electrical status epilepticus in sleep patients diagnosed with idiopathic partial epilepsy, and they also found no significant relation between the bilaterality of epileptogenic foci and progression into electrical status epilepticus in sleep.
There are many reports on the treatment of electrical status epilepticus in sleep. The efficacy of valproic acid, ethosuximide, clonazepam, lorazepam, short cycles of diazepam and corticosteroids had been reported. There are also reports for the combination therapy of valproic acid and ethosuximide, clonazepam and diazepam, the use of corticosteroids seems to be the most effective approach. [15],[16] Inutsuka et al. [10] have reported that valproic acid and ethosuximide combination was effective in 43% of the patients and this effect was permanent in all responders.
Contrary to these results, Kramer et al. [11] reported that the valproic acid, lamotrigine, topiramate and ethosuximide did not have any effect, and the most efficacious antiepileptic drugs were levetiracetam and clonazepam.
Topiramate and corticosteroids were the most used agents during ESES period in our patients and good for the disappearance of EEG findings. As a result, there is no standardized treatment in patients with electrical status epilepticus in sleep. Some antiepileptic drugs can be used alone or in combination.
| Conclusion | | |
Following-up the epileptic children clinically and electrophysiologically is important to recognize the development of electrical status epilepticus in sleep in epileptic children both for seizure control and prevention of cognitive impairment. Also, appearance of the new type of seizures or behavior problems in epileptic children must alert physician for the development of electrical status epilepticus in sleep.
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[Table 1]
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