EEG in Benign and Malignant Epileptic Syndromes of Childhood
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1 Epilepsia, 43(Suppl. 3):17 26, 2002 Blackwell Publishing, Inc. International League Against Epilepsy EEG in Benign and Malignant Epileptic Syndromes of Childhood Ivo Drury Department of Neurology, Henry Ford Health System, Detroit, Michigan, U.S.A. Summary: Characteristic appearances of epileptiform EEG activity in children aged between 2 and 10 years are described. Emphasis is placed on the value of careful analysis of background EEG and how the epileptiform activity itself may overlap between benign and malignant epileptic syndromes. Illustrations are used to underscore this emphasis. Irrespective of how classic an EEG appearance is, accurate classification of a child s epileptic syndrome requires integration of all available clinical data. EEG is just one component of this equation. Key Words: Children Epilepsy EEG Background activity Epileptiform activity. This article reviews the EEG features seen in some of the childhood epilepsies. In my opinion, skill in EEG interpretation is in decline, in part of course a product of the many exciting advances in diagnostic techniques in neurology. There remains, however, great value in a careful analytic examination of the EEG. Children have always offered the greatest learning material for the neophyte electroencephalographer. I use the EEG appearance in certain classic epileptic syndromes of childhood to teach an approach to EEG interpretation that has broad applicability. APPROACH TO EEG INTERPRETATION Each EEG should be read with maximal possible objectivity. Ideally an EEGer should describe the findings and make an EEG diagnosis (thus, the first two components of a well-prepared EEG report) without knowledge of the patient s history. The clinical significance of the findings can then be judged by integrating the EEG diagnosis with the history. Interictal activities must be distinguished from ongoing background features. The background features must be judged against the age and behavioral state of the patient. Individuals must be sensitive to the vast range of normal in the child s EEG. I usually teach that one should allow the same latitude in terms of what is normal in a child s EEG that we would for their maturation of their behavior. I strongly recommend the teaching atlas Address correspondence and reprint requests to Dr. I. Drury at Department of Neurology, Henry Ford Health System, 2799 W. Grand Boulevard, Detroit, MI 48202, U.S.A. idrury@neuro.hfh.edu of pediatric EEG by Blume et al. (1). Those transients that are determined to be potentially epileptiform must satisfy the following criteria: (a) they are clearly of cerebral and not artifactual origin, (b) they are abnormal for the age and behavioral state of the patient, and (c) these transients have a significant epileptiform character (i.e., they are not one of the benign epileptiform variants). A useful algorithm for an orderly approach to the analysis of EEG activity is displayed in Fig. 1. Interictal activities can occur in individuals who will never have an epileptic condition. In two studies (2,3), epileptiform discharges were found in 1.5% and 1.9% of healthy children aged from 1 to 16 years, carefully screened to exclude disease of the nervous system. Interictal waveforms are supportive of an underlying seizure disorder but are never diagnostic. To be diagnostic of a seizure disorder, an EEG must include a clinical change in conjunction with an electrical change. There are a large number of benign epileptiform variants (4). These include normal features that may in some patients look epileptiform or activity that is epileptiform but has no known association with seizure disorders. Some initial studies will show abnormalities that are minor but no unequivocal epileptiform activity. Followup studies will increase sampling time, but more important, the study can be repeated in a different state of awareness or with more activation procedures, special electrodes, etc. Tests such as long-term video-eeg monitoring or polysomnography may be viewed as complementary to EEG. As is true of all investigative tools, EEG has limitations. In the Ajmone-Marsan and Zivins 1970 study (5) 17
2 18 I. DRURY FIG. 1. Algorithm displaying an approach to the orderly visual analysis of EEG activity. of 1,824 EEG records from 308 patients with a reasonably certain diagnosis of epilepsy (average, six records/ patient), 30% had consistently positive (i.e., interictal activity present) EEGs, 52% had some positive and some negative studies, and 17.5% had consistently negative EEGs. Interictal activity was much more likely to be present in the EEG of a child than in that of an adult, with a frequency of 77% in the first decade of life compared with 51% in the fourth. Generally, the type of seizure disorder was unrelated to positivity or negativity of the records. SPECIFIC EEG PATTERNS TO BE DESCRIBED The EEG features (with an emphasis on interictal epileptiform activity) listed in the right-hand column of Table 1 are discussed in detail. Almost always they belong in one of the four major categories of epileptic syndromes listed in the left-hand column. Idiopathic generalized epilepsies 3-Hz spike-and-wave This pattern occurs in idiopathic generalized epilepsies of the absence type, but also in patients with tonic TABLE 1. Specific EEG patterns described Idiopathic generalized Idiopathic localization related Symptomatic generalized Symptomatic localization related 3 Hz spike-and-wave Atypical spike-and-wave Centrotemporal sharp waves Occipital spike-wave Slow spike-and-wave Generalized paroxysmal fast activity Multiple independent spike foci Midline spikes clonic and myoclonic seizures. The waking background EEG activity is normal. The spike-and-wave is a bisynchronous, symmetric discharge of sudden onset and resolution with a frequency of Hz at the onset, slowing to Hz at resolution (Fig. 2). As a burst evolves, the spike discharges become smaller. Its greatest amplitude is at the superior frontal electrodes. Isolated fragments may occur but usually average out over a single recording. Such asymmetric discharges must be distinguished from the discharges seen in patients with secondary bilateral synchrony. Even a repeated focal amplitude emphasis to the discharges is probably not significant unless accompanied by focal background slowing and disorganization, where a secondarily generalized discharge is more probable. The morphology of the discharges is best seen in referential montages. The discharges are reactive, being inhibited by eye opening and alertness. Hyperventilation (6) and hypoglycemia readily activate them. In drowsiness, the discharges must be distinguished from hypnogogic hypersynchrony, bursts of high-amplitude theta in the frontocentral area that may have intermixed spike and sharp-wave like activity, seen most commonly from ages 5 months to 5 years (Fig. 3). This normal activity can be distinguished from epileptiform activity by its occurrence solely in the drowsy state. In sleep, the discharges become more irregular with a polyspike wave quality, more frequent but often of briefer duration (7). Ten to fifteen percent of patients show an associated photoparoxysmal response (PPR) with photic stimulation (6). The typical clinical accompaniment of 3-Hz spikeand-wave discharge is the absence seizure. Discharges of 2 3 s will usually show a clinically apparent decrease
3 EEG IN CHILDHOOD EPILEPSIES 19 FIG. 2. Recorded absence seizure from a patient with juvenile absence epilepsy. Spike wave frequency slows from 3.5 to 2.5Hz during this simple staring spell. in responsiveness, but response testing may demonstrate an earlier decline in maximal alertness (8). Atypical spike-and-wave This entity has an inexact nosology but may be best considered as a generalized spike wave discharge at a frequency of 3 6 Hz and with an irregular polyspikeand-wave appearance in the waking state. It is distinct from the slow-spike-and-wave of Lennox Gastaut syndrome and the typical 3-Hz spike-andwave described earlier. It can be seen both in idiopathic generalized epilepsies [e.g., juvenile myoclonic epilepsy of Janz (9,10)], or in symptomatic generalized epilepsies such as the progressive myoclonic type (11). It has no particular age predilection, but is most common after the first decade. The background EEG activities are normal in patients with an idiopathic epilepsy (Fig. 4). In those with symptomatic epilepsy, it may be normal or mildly abnormal initially (Fig. 5), but ultimately will always become slowed and disorganized. Interictal patterns consist of bursts of atypical spike-and-wave, the ictal patterns consist of more prolonged atypical spike wave bursts, trains of high-amplitude 10- to 16-Hz spikes or when absence seizures occur, bursts of regular 3-Hz spike waves (9). Discharges are usually bilaterally synchronous and have an amplitude emphasis over the superior frontal regions (Fig. 4); the morphology is best demonstrated on referential montages, and like the 3-Hz spike-and-wave discharge, isolated fragments may occur independently over either anterior head region. The number of spike discharges tends to increase in sleep. The effect of hyperventilation is more variable. Activation occurs in some but much less commonly than FIG. 3. Hypnogogic hypersynchrony recorded during drowsiness in a 2-year-old girl with a single febrile seizure. Note the intermixed spiky components, best seen in the left superior frontal region. This activity was apparent only during drowsiness, and the record was entirely normal during all states of wakefulness and sleep.
4 20 I. DRURY FIG. 4. Generalized bisynchronous atypical polyspike-and-wave in a boy with a history of tonic clonic seizures and photosensitivity. in patients with typical 3-Hz spike-and-wave. Overall, photic stimulation induces a PPR in 35% of patients with atypical spike-and-wave. PPR may be more common in some forms of progressive myoclonic epilepsy (11). Epileptiform activity triggered by light stimulation consists of generalized atypical spike-and-waves that may be time locked to the stimulus, self-limited, and cease during stimulation, or continue beyond the duration of the stimulus. PPR is usually seen best at the middle flash frequencies of Hz. When it occurs, the stimulus should be repeated at the same and adjacent flash rates to test for reproducibility of the response. A limited clinical accompaniment may occur and usually consists of brief jerks of the body with or without impairment of consciousness, but absence and tonic clonic seizures also can occur. Technologists should be instructed to stop light stimulation once a spike-and-wave discharge appears, or else the patient may develop a generalized tonic clonic seizure. IDIOPATHIC LOCALIZATION-RELATED EPILEPSIES The International League Against Epilepsy classifies the benign childhood partial epilepsies among the ageand localization-related epilepsies. They are seen in children whose neurologic and laboratory examinations, with the exception of the EEG, are normal. They comprise one well-recognized syndrome and one more rare yet relatively consistent syndrome (both discussed individually later), but also a number of less well defined entities that share significant overlap. Some authorities (12) believe that all these epileptic syndromes should be unified as benign childhood partial epilepsies, distinguished by clinical features dependent on the location of FIG. 5. Two EEG samples from a patient in the early stages of Lafora disease. The left panel shows an irregular spike wave pattern superimposed on a slowed and disorganized background. The right panel shows background slowing and focal occipital spikes.
5 EEG IN CHILDHOOD EPILEPSIES 21 FIG. 6. Bilateral independent centrotemporal sharp-wave discharges (parasagittal expression only displayed) during stage II sleep in a 7-year-old boy with a single nocturnal tonic clonic seizure at age 4 years. the EEG focus, but representing phenotypic variations of the same genetic trait. Benign focal epilepsy of childhood with centrotemporal spikes This is an age-dependent, strongly inherited (13), epilepsy of childhood. It is characterized by nocturnal generalized tonic clonic seizures, sometimes preceded by focal seizure activity. Diurnal seizures (especially in the early morning) are usually focal and consist of twitching of the face and/or hand, motor speech arrest without aphasia, excess salivation because of inability to swallow, and tingling of the side of the mouth, tongue, or cheek (14). They occur between ages 4 and 12 years and are not seen after age 16 years. Seizures are rare and commonly isolated. The background EEG activities in wakefulness and sleep are normal. High-amplitude di- or triphasic, blunted sharp waves, sometimes followed by an aftercoming slow wave, are present in wakefulness but markedly activated by drowsiness and sleep, when they are particularly likely to occur in short repetitive clusters and be bilateral (Fig. 6). The discharges may be unilateral, bilateral, or have shifting laterality in single or serial FIG. 7. Appearance of a horizontal dipole in a 9-year-old girl with benign epilepsy of childhood with centrotemporal spikes. The sharp waves are of surface-negative polarity at the right central and midtemporal electrodes and surfacepositive in the frontal regions.
6 22 I. DRURY FIG. 8. EEG from a 9-year-old child with benign epilepsy of childhood with centrotemporal spikes. There are frequent left centrotemporal sharp waves, but the most striking feature is the generalized spike-and-wave discharge, and the independent focal sharp waves in the left occipital and right posterior regions. Note the normal background in contrast to Fig. 9. recordings. Typically, they arise from the lower rolandic area with maximal expression in the central midtemporal leads of the conventional placement. The discharges were seen in atypical locations in 21% of patients with a single focus and in 37.5% of patients with more than one focus (15). Horizontal dipoles are common and usually have a maximal negativity in the centrotemporal area and positivity in the frontal area (16) (Fig. 7). Some children have associated generalized spike-and-wave discharges, with an incidence of 14.6% in the study of Beydoun et al. (17). Multiple independent sharp-wave foci (MISF) occurred in 9.8% of 41 patients (17) (Fig. 8). As MISF are much more likely to be seen in patients with symptomatic generalized epilepsy, the importance of careful analysis of background EEG is again relevant. Contrast, for example, the normal background in Fig. 8 from a patient with BECTS and MISF, with the disturbed background seen in Fig. 9 from a patient with MISF and symptomatic generalized epilepsy. Hyperventilation and photic stimulation have no effect on the focal discharges of BECTS. Benign focal epilepsy of childhood with occipital spikes Benign focal epilepsy of childhood with occipital spikes (BOE) is an age-dependent, inherited epilepsy of childhood most common in girls aged between 3 and 5 years. Clinical manifestations are infrequent, sometimes prolonged seizures consisting mainly of tonic deviation of the eyes and vomiting, often with evolution to unilateral or generalized convulsions (18,19). In children with onset of the syndrome later in the first decade, symptoms such as amaurosis, visual hallucinations, or visual illusion may occur as a prodrome. The EEG shows normal background rhythms in wakefulness and sleep. With eyes closed, near-continuous, high-amplitude, 1- to 3-Hz, spike wave discharges arise independently or bisynchronously from the occipital and/ or posterior temporal regions (Fig. 10). In most but not all cases, the discharges are suppressed by visual fixation. The discharges are commonly asymmetric. They are not activated by photic stimulation. FIG. 9. Multiple independent spike foci with a midline emphasis, from a patient with symptomatic generalized epilepsy. Note the disturbed background in contrast to Fig. 9.
7 EEG IN CHILDHOOD EPILEPSIES 23 FIG. 10. Bilateral occipital spike wave activity reactive to eye opening from a patient with benign focal epilepsy of childhood with occipital spikes. SYMPTOMATIC GENERALIZED EPILEPSIES The age-dependent epileptic syndromes of neonates, infants, and children include the Ohtahara, West, and Lennox Gastaut syndromes. Ohtahara (20) believes that these syndromes represent successive stages in maturation of an epileptic process, with the clinical and EEG features dependent on the particular age of the patient. Slow spike and wave These bilaterally synchronous discharges occur in the symptomatic generalized epilepsies and are the typical EEG feature of children with Lennox Gastaut syndrome: slow spike-and-wave, mental retardation, and multiple seizure types (21 23). The age at onset is 1 6 years (mean, 26 months). Slow spike-and-wave may evolve from a previously normal EEG, or from patterns of hypsarrhythmia or MISF. The waking background shows generalized slowing. The epileptiform discharges are 1- to 2.5-Hz bilaterally synchronous spike-and-wave or sharp-andslow-wave complexes (Fig. 11). These have an amplitude emphasis in the frontal and temporal regions (21,23). Some of the discharges may be asymmetric and have a shifting focal emphasis. They may appear in very long and at times continuous bursts, commonly without an identified change in the level of awareness. Hyperventilation and photic stimulation usually provoke no significant change. Some patients will show features of both slow-spike-and-wave and MISF on a single EEG. FIG. 11. Bisynchronous slow spike-and-wave and generalized background slowing from a patient with symptomatic generalized epilepsy.
8 24 I. DRURY FIG. 12. Periodic bursts of slow spike-and-wave activity during sleep in a young girl with symptomatic generalized epilepsy. In sleep, normal background features are absent or poorly developed. The discharges commonly increase during sleep, assume a more polyspike-and-wave character, and in some subjects, show a strikingly periodic pattern (Fig. 12), with attenuation of background between the epileptiform bursts (24). Paroxysmal fast discharges (discussed later) with or without accompanying tonic seizures are typically seen in sleep and are considered by some to be the hallmark of the condition (25). The ictal patterns are variable and may consist of diffuse attenuation followed by low-amplitude fast rhythms, generalized paroxysmal fast activity, high-voltage spikes of very short duration, more hypersynchronous spike wave discharges, or no change from background features. Paroxysmal fast activity This pattern typically occurs during sleep in patients with symptomatic generalized epilepsies but more rarely may be seen in patients with idiopathic generalized epilepsies or in patients with partial seizure disorders, particularly with a frontal lobe focus. It consists of bursts of 10- to 25-Hz spikes averaging 3 5 s in duration, preceded or followed by generalized sharp-and-slow-wave complexes (26) (Fig. 13). There is no change in the frequency of the spikes during the burst, but the amplitude may decrease as the discharge progresses. It typically has an amplitude maximum at the superior frontal electrodes, is bilaterally synchronous, but may have a shifting voltage emphasis between the two hemispheres, and rarely may occur unilaterally. The waking background is usu- FIG. 13. Three-second-long train of generalized paroxysmal fast activity associated with arousal and brief tonic activity in a patient with symptomatic generalized epilepsy. Note how the discharge ends in a slow spike-and-wave.
9 EEG IN CHILDHOOD EPILEPSIES 25 ally slowed, and normal sleep features are absent or poorly developed in the majority of patients. Tonic seizures are the typical clinical accompaniment, but most bursts in sleep occur without any clinical change. In wakefulness, most bursts are ictal. Activation procedures such as hyperventilation and photic stimulation have no effect on the discharges, whereas sleep enhances the number of discharges considerably. Multiple independent spike foci This is defined as three or more independent, noncontiguous foci of epileptiform activity, at least one of which arises from each hemisphere within a single EEG recording (27) (Fig. 9). It occurs in children with the same clinical features as Lennox Gastaut syndrome. The pattern arises from the same diverse etiologies that cause hypsarrhythmia and slow-spike-and-wave discharges. The background activity in wakefulness is slowed and disorganized, and normal sleep features are commonly absent. Sleep may lead to a greater synchrony of discharges and a slow spike-and-wave appearance, or an increase in the number of foci. Some children will show a slow spike-and-wave discharge on one EEG with multiple independent spike foci on another. Spikes are most frequently seen in the temporal regions and then, in decreasing order of frequency, the occipital, central, frontal, and parietal regions. Hyperventilation and photic stimulation have little effect. Symptomatic localization-related epilepsies Partial-seizure disorders due to focal cortical neuronal disturbances are the commonest cause of seizures in the epilepsy population as a whole. The clinical features vary and depend on the location of the epileptic focus. Seizures may remain focal or secondarily generalize. Not all foci that are defined electrographically are associated with clinical seizures, and in some locations, particularly the centroparietal and occipital regions, the overall incidence of seizures may be quite low. I have selected one pattern to describe in more detail. Midline spikes are relatively common, but frequently overlooked. Moreover, benign sleep activity is sometimes read as epileptiform activity in this region. Midline spikes These are discrete spikes or sharp waves that arise from only midline electrodes in 35%, or reflect to adjacent parasagittal electrodes. More than 80% of patients have an accompanying seizure history, consisting of a variety of focal or generalized types. When the discharges occur in sleep only, care must be taken to distinguish them from normal vertex waves (Fig. 14). Most of the patients show discharges only in sleep (28,29). The central electrodes are most commonly involved, followed by the parietal and superior frontal. In studies that included patients of all age groups, midline spikes were much more common in children (28,29). FIG. 14. Midline spikes at Pz. Normal background sleep features. Note the distinction between the midline spikes and vertex waves. From a 5-year-old girl with tonic clonic seizures.
10 26 I. DRURY CONCLUSIONS EEG in children offers challenges and rewards much greater than those of the adult. Nowhere is this distinction more evident than in the childhood epilepsies. The challenges in interpretation lie in knowing the vast range of what constitutes the normal EEG in children, and avoiding the trap of overreading. Paying attention to the fundamentals, notably careful analysis of background features, will pay great dividends. Irrespective of how distinctive the patient s EEG may appear, accurate classification of the child s epileptic syndrome requires integration of all clinical data. EEG is just one component of this equation. REFERENCES 1. Blume WT, Kaibara M. Atlas of pediatric electroencephalography. 2nd ed. Philadelphia: Lippincott Williams & Wilkins, Petersén I, Eeg-Olofasson O, Selldén U. Paroxysmal activity in EEG of normal children. In: Kellaway P, Petersen I, eds. Clinical Electroencephalography of Children. New York: Grune & Stratton,1968: Eeg-Olafsson O, Petersén I, Sellden U. The development of the electroencephalogram in normal children from the age of 1 through 15 years: paroxysmal activity. Neuropaediatrie 1971;2: Klass DW, Westmoreland BF. Nonepileptogenic epileptiform electroencephalographic activity. Ann Neurol 1985;18: Ajmone Marsan C, Zivin LS. Factors related to the occurrence of typical paroxysmal abnormalities in the EEG records of epileptic patients. Epilepsia 1970;11: Dalby MA. Epilepsy and 3 per second spike and wave rhythms: a clinical, electroencephalographic and prognostic analysis of 346 patients. Acta Neurol Scand 1969;45(suppl 40): Sato S, Dreifuss FE, Penry JK. The effect of sleep on spike-wave discharges in absence seizures. Neurology 1973;23: Browne TR, Penry JK, Porter RJ, et al. Responsiveness before, during and after spike-wave paroxysms. Neurology 1974;24: Delgado-Escueta AV, Enrile-Bascal F. Juvenile myoclonic epilepsy of Janz. Neurology 1984;34: Asconape J, Penry JK. Some clinical and EEG aspects of benign juvenile myoclonic epilepsy. Epilepsia 1984;25: Roger J. Progressive myoclonic epilepsy in childhood and adolescence. In: Roger J, Dravet C, Bureau M, et al., eds. Epileptic syndromes in infancy, childhood and adolescence. London: John Libbey, 1985: Panayiotopoulos CP. Benign childhood partial epilepsies: benign childhood seizure susceptibility syndromes. J Neurol Neurosurg Psychiatry 1993;56: Heijbel J, Blom S, Rasmuson M. Benign epilepsy of childhood with centrotemporal EEG foci: a genetic study. Epilepsia 1975;16: Loiseau P, Pestre M, Dartigues JF. Long term prognosis in two forms of childhood epilepsy: typical absence seizures and epilepsy with rolandic (centrotemporal) EEG foci. Ann Neurol 1983;13: Drury I, Beydoun A. Benign partial epilepsy of childhood with monomorphic sharp waves in centrotemporal and other locations. Epilepsia 1991;32: Gregory DL, Wong PK. Topographical analysis of the centrotemporal discharges in benign Rolandic epilepsy of childhood. Epilepsia 1984;25: Beydoun AA, Garofalo EA, Drury I. Generalized spike-waves, multiple loci and clinical course in children with EEG features of benign epilepsy of childhood with centrotemporal spikes. Epilepsia 1992;33: Panayiotopoulos CP. Inhibitory effect of central vision on occipital lobe seizures. Neurology 1981;31: Kuzniecky R, Rosenblatt B. Benign occipital epilepsy: a family study. Epilepsia 1987;28: Ohtahara S. Clinico-electrical delineation of epileptic encephalopathies of childhood. Asian Med J 1978;21: Blume WT, David RB, Gomez MR. Generalized sharp and slow wave complexes: associated clinical features and long-term follow up. Brain 1973;96: Chevrie JJ, Aicardi J. Childhood epileptic encephalopathy with slow spike- wave: a statistical study of 80 cases. Epilepsia 1972; 13: Markand ON. Slow spike-wave activity in EEG and associated features: often called Lennox or Lennox-Gastaut syndrome. Neurology 1977;27: Gabor AJ, Seyal M. Effect of sleep on the electrographic manifestations of epilepsy. J Clin Neurophysiol 1986;3: Beaumanoir A. The Lennox-Gastaut syndrome. In: Roger J, Dravet C, Bureau M, et al., eds. Epileptic syndromes in Infancy, childhood and adolescence. London: John Libbey, 1985: Brenner RP, Atkinson R. Generalized paroxysmal fast activity: electroencephalographic and clinical features. Ann Neurol 1982; 11: Blume WT. Clinical and electroencephalographic correlates of the multiple independent spike foci pattern in children. Ann Neurol 1978;4: Pedley TA, Tharp BR, Herman K. Clinical and electroencephalographic characteristics of midline parasagittal foci. Ann Neurol 1981;9: Nelson KR, Brenner RP, de la Paz D. Midline spikes: EEG and clinical features. Arch Neurol 1983;40:473 6.
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