Seizure: European Journal of Epilepsy
Volume 19, Issue 4 , Pages 222-225, May 2010

Electroencephalographic generalized features in idiopathic childhood focal epilepsies

  • Mi-Sun Yum

      Affiliations

    • The Saul R. Korey Department of Neurology, Albert Einstein College of Medicine, Bronx, NY 10461, USA.
    • ,
  • Tae-Sung Ko

      Affiliations

    • Corresponding Author InformationCorresponding author. Tel.: +82 2 3010 3390; fax: +82 2 473 3725.
    • ,
  • Eun Hye Lee
    • ,
  • Min-Hee Jeong

Department of Pediatrics, Asan Medical Center, University of Ulsan College of Medicine, 388-1 Poongnap-dong, Songpa-ku, Seoul 138-736, Republic of Korea

Received 20 November 2009; received in revised form 21 January 2010; accepted 12 February 2010. published online 22 March 2010.

Article Outline

Abstract 

Purpose

Idiopathic focal epilepsies in childhood including benign childhood epilepsy with occipital paroxysms (BEOP) or benign childhood epilepsy with centro-temporal spikes (BCECTS) are characterized by specific focal electrographic patterns as the name indicates. Generalized spike-wave discharges in children with idiopathic focal epilepsy can suggest a neurobiological continuum with the idiopathic generalized epilepsies. We assessed the prevalence of generalized epileptiform discharges and generalized seizures in BEOP/BCECTS patients.

Methods

Between August 2005 and November 2008, we identified 220 cases with electroclinical features typical of idiopathic focal epilepsies, 172 patients with BCECTS and 48 patients with BEOP, excluding patients whose neurological examinations or brain MRI were abnormal. We analyzed gender, age at onset, manifestation of generalized seizures, and serial EEG records to detect generalized abnormalities.

Results

Of our population, 42 patients (19.1%, 22 boys), 30 (17.4%) of 172 BCECTS patients and 12 (25.0%) of 48 BEOP patients, showed generalized spike-wave discharges once or more during follow-up. The typical 3-Hz generalized spike wave discharge was noticed in 7 patients and concurrence with clinical generalized seizure was observed in 11.

Conclusion

A relatively high incidence of generalized spike-wave discharge and concurrence with generalized seizure were observed in patients with BEOP/BCECTS, with the incidence being higher in BEOP patients than in those with BCECTS. It may be inferred that idiopathic focal epilepsy is not a fixed syndrome but is a part of a broad, age-related, benign, seizure susceptibility syndrome.

Keywords: Benign partial epilepsy of childhood, Idiopathic epilepsy, EEG, Childhood seizure susceptibility

 

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1. Introduction 

Idiopathic focal epileptic syndromes, which are related to benign childhood focal seizures, affect a considerable number of children with non-febrile seizures and constitute a significant proportion of patients admitted to pediatric epilepsy clinics. The conditions are characterized by childhood onset, absence of demonstrable brain lesions, infrequent and brief partial seizures, paradoxically abundant interictal EEG abnormalities, and spontaneous remission before the end of adolescence.1 Idiopathic focal epilepsies in childhood recognized by the International League Against Epilepsy (ILAE)2 include three identifiable electroclinical syndromes: benign childhood epilepsy with centro-temporal spikes (BCECTS, rolandic epilepsy); and benign childhood epilepsy with occipital paroxysms (BEOP), which includes the idiopathic childhood occipital epilepsy of Gastaut (ICOE-G) and Panayiotopoulos syndrome (PS). The most useful diagnostic test is the EEG. The hallmark of BCECTS is the centro-temporal spikes that are mainly localized in the C3 and C4 (high central) or C5 and C6 (low central) supra-sylvian area, are often bilateral, and are typically activated by drowsiness and slow (non-REM) sleep.3, 4 However, the occurrence of generalized spike-wave discharges in such patients is known to be reasonably common and brief, generalized 3–5-Hz slow wave bursts intermixed with small spikes, with or without clinical seizures, were reported to occur in 4% of patients with rolandic epilepsy.5, 6 In Panayiotopoulos syndrome, despite the characteristic clustering of autonomic manifestations, the EEG reveals occipital paroxysms in one-third of patients and shows great variability, sometimes with brief generalized discharge of slow waves.7 On the other hand, the interictal EEG of ICOE-G shows occipital paroxysms in most instances. Although diagnosis of BCECTS/BEOP is easily made using these EEG characteristics, it has been observed that generalized spike discharges, observed in childhood absence epilepsy (CAE) or the idiopathic generalized epilepsies, appear with or without seizures during follow-up periods. Because idiopathic localization-related epilepsies and idiopathic generalized epilepsies are benign, age-related, and age-limited syndromes, these findings suggest a neurobiological continuum between the two epilepsies. Therefore, critical analysis and comparison of EEG changes in children with BCECTS/BEOP during follow-up should yield meaningful results on developmental EEG changes in patients with the benign idiopathic childhood epilepsy. This study thus examined the prevalence of generalized epileptiform discharges and generalized seizures in BEOP/BCECTS patients during follow-up, and we hypothesize that there may be a time-specific developmental pattern of generalized EEG features.

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2. Methods 

Data from patients attending the pediatric neurologic department of the Asan Medical Center, a 2800-bed teaching hospital in Seoul, Korea, have been computerized since 2005 with demographics as well as diagnostic and treatment details. The data were reviewed and revised on each visit of the patient. Between August 2005 and November 2008, we identified 220 patients with idiopathic focal epilepsies from this computerized database. Diagnosis was based on strict inclusion criteria, including a history of focal seizures, a normal neurological examination, normal brain MRI, and supportive EEG findings.8 A careful syndromic classification was made using clinical manifestations, such as unilateral facial sensory-motor symptoms or oro-pharyngo-laryngeal symptoms for BCECTS patients9; autonomic symptoms for those with PS; and visual hallucination, blindness, eyeball deviation, or ictal headache for children with ICOE-G.10 In total, 172 patients with BCECTS and 48 with BEOP including 32 with PS and 16 with ICOE-G were identified.

We reviewed these patient data and analyzed gender, age at onset, family history of epilepsy, personal history of febrile convulsions, clinical manifestations of generalized seizure or absence of seizure, and treatment responses. EEG recording was performed while patients were both awake including hyperventilation provocation and asleep using partial sleep deprivation, with electrodes placed according to the international 10–20 system. EEG recording was repeated longitudinally in patients, at 1-year intervals, and two pediatric neurologists with extensive experience analyzing pediatric EEG traces (T.S. Ko and M.S. Yum) reviewed their serial EEG records for detection of generalized abnormalities and other specific changes. EEG findings were classified into three groups: focal, generalized, and mixed (where the EEG revealed generalized and focal discharges simultaneously, at the time of evaluation). The 3-Hz spike and wave discharges (3-Hz SW) were regarded as a generalized spike and wave lasted longer than 2s (Fig. 1A). Generalized spike wave discharges (GSW) were defined as brief (<2s) discharges and sometimes diffuse spike wave discharges (which were not really generalized) were included in this category (Fig. 1B).

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3. Results 

During a mean follow-up period of 5 years (range, 1–13 years), 42 (19.1%, 22 boys) of the 220 patients with idiopathic focal epilepsies revealed generalized spike-wave discharges. Age at onset of seizure ranged from 3.4 to 14.4 years, with a mean age of 7.0 years. Thirty (17.4%) of 172 BCECTS patients and 12 (25.0%) of 48 BEOP patients including 9 (28.1%) of 32 PS patient and 3 (18.8%) of 16 ICOE-G patients showed generalized spike-wave discharges more than once during follow-up.

In the group of patients who showed generalized spike discharges, the mean age at seizure onset was 7.3 years in the BCECTS group and 6.1 years in the group with BEOP (8.4 years in patients with ICOE-G and 5.4 years in patients PS). The mean age at first EEG evaluation was 8.4 years in BCECTS patients and 7 years in those with BEOP (9.6 years in patients with ICOE-G and 6.2 years in patients PS). The mean follow-up duration was 4.5 years in both groups. Sixteen (53.3%) of the BCECTS and 6 (50%) of the BEOP patients were boys. Four of the 30 patients (13.3%) with BCECTS and 2 of 12 patients (16.7%) with BEOP (none of 3 with ICOE-G and 2 of 9 with PS) had a family history of epilepsy and 10 of the BCECTS (33.3%) and 3 of the BEOP patients (25%, 1 of 3 with ICOE-G and 2 of 9 with PS) had a history of febrile seizures (Table 1).

Table 1. The clinical variables of idiopathic focal epilepsies with generalized spike.
BCECTSaBEOPb
Total patients (N)3012
Gender ratio (male:female)16:146:6
Seizure onset (month)8774
Age at first EEG (month)10184
Follow-up duration (month)5454
Family history of epilepsy (N)32
History of febrile seizure (N)103

aBCECTS, benign childhood epilepsy with centro-temporal spikes.

bBEOP, benign epilepsy with occipital paroxysms.

EEG evaluation was performed once on 6 patients, whereas the other 36 patients received 2 or more EEG evaluations at 1-year intervals. A total of 133 serial EEG records, 92 from children with BCECTS and 41 from children with BEOP, were analyzed to identify age-related changes. Most children who received serial EEG evaluation showed transitional EEG findings, from generalized to mixed or focal in 5 patients, from focal to generalized or mixed in 17 patients, and from mixed to focal or generalized in 9 patients. Three patients showed consistently mixed EEG findings and the EEG of two patients were normalized (Fig. 2 and Table 2).

  • View full-size image.
  • Fig. 2. 

    The diagram of EEG evolution in our series of patients with idiopathic focal epilepsies and generalized spike and wave discharges; BCECTS, benign childhood epilepsy with centro-temporal spikes; BEOP, benign epilepsy with occipital paroxysms; CAE, childhood absence epilepsy; *the patient presented with partial epilepsy but detailed history and electroencephalogram revealed that she also has absence seizures; generalized, generalized spike and wave discharges on EEG; focal, focal spike discharges on EEG; mixed, generalized and focal spike discharges at a time of EEG.

Table 2. The comparison of electroencephalographic characteristics between benign childhood epilepsy with centro-temporal spikes (BCECTS) and benign epilepsy with occipital paroxysms (BEOP).
Within BCECTSa (N) (total 172)Within BEOPb (N) (total 48)
Patients with GSWc (%)30 (17.4%)12 (25.0%)
Patients with 3Hz GSWc (%)6 (3.5%)1 (2.1%)
With clinical generalized seizure (%)10 (5.8%)1 (2.1%)
With initial focal discharges115
With initial mixed discharges146
With initial generalized discharges51

aBCECTS, benign childhood epilepsy with centro-temporal spikes.

bBEOP, benign epilepsy with occipital paroxysms.

cGSW, generalized spike and waves.

Turning to the EEG pattern of patients with BCECTS, 11 showed centro-temporal spike discharges and 14 displayed both centro-temporal spike discharges and generalized spike and slow wave discharges at the time of first EEG monitoring. Three patients who experienced febrile convulsions with evidence of GSW on EEG, one patient with CAE, and one with juvenile absence epilepsy (JAE), were later diagnosed with BCECTS and their prior EEG records were included in the analysis.

The EEG traces of BEOP patients at diagnosis revealed that five showed focal spike discharges from the occipital area and one showed generalized spike discharges. A mixed pattern of spikes appeared in another six patients with BEOP. Four of the patients with PS patients also displayed centro-temporal spikes during follow-up.

Typical 3-Hz GSW was noticed in seven patients. Six of the 30 patients with BCECTS and one of the 12 patients with BEOP showed the 3-Hz spike and also slow wave bursts. Concurrence with clinical generalized seizures was observed in 11 patients, including 5 with absences, 2 with myoclonic seizure, 1 with myoclonic and generalized tonic clonic seizure (GTCS), and 4 with GTCS on awakening. Ten patients from the BCECTS group and one from the BEOP group showed clinical generalized seizures.

From the 47 EEG records that showed generalized spike and wave discharges, 4 of them failed to provoke hyperventilation properly and 17 of them revealed generalized spike and wave discharges during hyperventilation.

Most children showed a good response to antiepileptic treatment and seizures were controlled using one or two antiepileptic drugs.

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4. Discussion 

The diagnosis of a specific syndrome or a classification of epilepsy in childhood can be important to guide appropriate treatment decisions and offer useful advice on epilepsy prognosis. However, a definitive diagnosis is not always possible because a child may have a vague clinical history. For example, it can be difficult to differentiate between a secondarily generalized seizure or a primary generalized tonic clonic seizure. EEG findings are not fixed and sometimes can reveal changing features, as shown both in our patients and other case series.11, 12 Although the clinical features and pathophysiology are well defined, idiopathic focal epilepsy syndromes such as BCECTS, BEOP, and idiopathic generalized epilepsies, including childhood absence epilepsy, share some common features. These include age of onset, overall good prognosis, and an idiopathic etiology suggestive of a genetic basis. Other researchers have also observed the coincidence of rolandic and absence features,11, 13, 14, 15 and the clinical overlap between BEOP and idiopathic generalized epilepsies.16, 17 Varying percentages of patients with GSW are noted in BCECTS patients of different study groups.5, 15, 18 This may be partly due to inconsistent interpretation of GSW between groups and partly attributable to variation in patient recruitment protocols.

Consistent with this observation, we found GSW, or absence-like or generalized seizures in patients with BCECTS and in those with BEOP, and the frequency of GSW was slightly higher in the BEOP group than in those with BCECTS. Sometimes, patients with BEOP also showed spikes from centro-temporal areas, as has been previously reported.7, 19 Such EEG changes may be explained by different rates of development in genetically determined epileptic brains. Idiopathic benign childhood epilepsy might be a non-focal condition in the anatomic sense, but a genetic age-related etiologic mechanism could be expected to create multifocal epileptic circuits widely disseminated throughout the cortex.18, 20, 21 Such multifocal circuits might differ individually in virulence and the circuits may be turned on and off independently over time, thereby providing the illusion that an electroencephalographic focus has changed in a child.

In our study, most children revealed changes in epileptiform discharges with time and we aimed to describe an age-related or developmental rule for the transition of the EEG from generalized to partial, or from partial to mixed or generalized (Fig. 2). Changes in both directions, thus from generalized to focal or mixed, and from focal to mixed or generalized, were, however, seen in our patients, and there seemed to be no rule governing EEG transitions. The only definite observation was that some proportion of patients with idiopathic focal epilepsies, either BCECTS or BEOP, showed generalized EEG features at some point of their development. This evolution of idiopathic focal epilepsy syndrome may be attributable to age-related expression, as described above, or might be caused by secondary bilateral synchrony.12, 17 For example of secondary bilateral synchrony, one patient from the previous study17 presented that the patient's ictal finding consists of occipital seizure followed by typical absence.

The relatively short follow-up period might be a possible reason why only a vague sequence of EEG changes was seen in our group of patients with idiopathic focal epilepsies. Our case series include two patients who followed only one year. However, it is impossible to intervene and recruit patients with idiopathic focal epilepsies at the start of such electroclinical syndromes because the time of commencement cannot be determined. Caraballo et al.22 also published a 2–10.5 year follow-up series of patients with childhood absence epilepsy associated with electroencephalographic findings similar to those of benign focal epilepsies. In this series, the course of the patients who showed coexistence of these focal paroxysms was benign and the coexistence were more frequent in males, which appears to represent the similar group of our series.

In our patient series, those who experienced previous febrile convulsions or absence seizures, and who were diagnosed with BCECTS later, were included in the analysis; these five children experienced generalized seizures and generalized epileptiform discharges before the appearance of clinical focal seizures. Further long-term follow-up of these patients might explain the evolution of the idiopathic benign epilepsies.

Genetic studies on the idiopathic focal epilepsies and idiopathic generalized epilepsies have also been performed.16, 23 Our study showed that overlap between idiopathic generalized and focal epilepsies occurred in individual patients. However, this overlap can be reflected in the mixed syndromic picture emerging in relatives.16, 24 These data indicate that a complex inheritance profile may underlie the common idiopathic epilepsies, with contributions from several genes. Combi et al.23 could not identify any significant phenotype differences between generations, nor were differences between the genders significant. Taylor et al.16 showed that monozygotic twin pairs did not have a higher concordance rate than did dizygotic twin pairs, indicating that idiopathic epilepsies may not be purely genetic disorders. The latter report also showed that BEOP children displayed an electroclinical spectrum, with the Panayiotopoulos and Gastaut syndromes at either end. Many patients showed mixed features, indicating that both idiopathic focal and generalized epilepsies are not discrete categories of idiopathic epilepsies but are instead likely to share some common genetic determinants. Our finding of generalized EEG and seizure phenotypes concomitant with or evolving from BCECTS or BEOP also raises the possibility that molecular determinants associated with these conditions are shared with idiopathic generalized epilepsies.

Since the epilepsy classification was concentrated on dividing patients into distinct groups, these clinical observations could not draw attention. The limitations of our work are, first, that we conducted a single-center study in a tertiary hospital and, second, that our observations did not define any specific developmental pattern of EEG changes in idiopathic focal epilepsies. However, the idea that age-related, benign seizure susceptibility to idiopathic epilepsies represents a continuum of pathogenicity deserves wider recognition and further study.

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5. Conclusion 

Relatively high incidence of generalized spike-wave discharges were observed in patients with BEOP/BRE and the occurrence was higher in BEOP than BECTS. It could be inferred that idiopathic focal epilepsy is not a fixed syndrome but is a part of broad age-related, benign seizure susceptibility syndrome.

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Conflict of interest statement 

We have no conflict of interest.

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PII: S1059-1311(10)00035-X

doi:10.1016/j.seizure.2010.02.006

Seizure: European Journal of Epilepsy
Volume 19, Issue 4 , Pages 222-225, May 2010

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