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1 Seizure 21 (2012) Contents lists available at SciVerse ScienceDirect Seizure journal homepage: Case report Two epileptic syndromes, one brain: Childhood absence epilepsy and benign childhood epilepsy with centrotemporal spikes Caterina Cerminara *, Antonella Coniglio, Nadia El-Malhany, Livia Casarelli, Paolo Curatolo Department of Neuroscience, Pediatric Neurology Unit, Tor Vergata University of Rome, Viale Oxford 81, Rome, Italy ARTICLE INFO ABSTRACT Article history: Received 30 June 2011 Received in revised form 15 September 2011 Accepted 15 September 2011 Keywords: Epilepsy Absence seizures Centrotemporal spikes Childhood absence epilepsy (CAE) and benign childhood epilepsy with centrotemporal spikes (BCECTS), or benign rolandic epilepsy (BRE), are the most common forms of childhood epilepsy. CAE and BCECTS are well-known and clearly defined syndromes; although they are strongly dissimilar in terms of their pathophysiology, these functional epileptic disturbances share many features such as similar age at onset, overall good prognosis, and inheritance factors. Few reports are available on the concomitance of CAE and BCECTS in the same patients or the later occurrence of generalized epilepsy in patients with a history of partial epilepsy. In most cases described in the literature, absence seizures always started after the onset of benign focal epilepsy but the contrary has never occurred yet. We describe two patients affected by idiopathic generalized epileptic syndrome with typical absences, who experienced BCECTS after remission of seizures and normalization of EEG recordings. While the coexistence of different seizure types within an epileptic syndrome is not uncommon, the occurrence of childhood absence and BCECTS in the same child appears to be extremely rare, and this extraordinary event supports the hypothesis that CAE and BCECTS are two distinct epileptic conditions. However, recent interesting observations in animal models suggest that BCECTS and CAE could be pathophysiologically related and that genetic links could play a large role. ß 2011 British Epilepsy Association. Published by Elsevier Ltd. All rights reserved. 1. Introduction Childhood absence epilepsy (CAE) is an age-dependent, idiopathic form of generalized epilepsy, characterized by the following features: multiple typical absence seizures each day accompanied with bilateral, symmetrical, and synchronous discharges of 3-Hz generalized spike and waves (GSW) in the electroencephalogram (EEG). CAE accounts for 2 10% of all childhood epilepsies and 8 15% of school-aged childhood epilepsies. 1 Benign childhood epilepsy with centrotemporal spikes (BCECTS), or benign rolandic epilepsy (BRE), is one of the most common childhood epilepsy syndromes and represents about 20% of epilepsy in children younger than 15 years of age. 2 5 Characteristically, the seizures begin between 3 and 10 years of age, with a peak at 7 8, and resolve by puberty. CAE and BCECTS are well-known and clearly defined syndromes; although they are strongly dissimilar in terms of their pathophysiology, these functional epileptic disturbances share many features such as similar age at onset, overall good prognosis, and inheritance factors. * Corresponding author. Tel.: ; fax: address: caterinacerminara@hotmail.com (C. Cerminara). The occurrence, even later, of CAE in patients with a history of benign focal epilepsy is extraordinary, but some authors have also described 6 the spontaneous coexistence of clinical and/or EEG features of CAE in BCECTS and vice versa. 7 While the coexistence of different seizure types within an epileptic syndrome is not uncommon, the phenomenon of one and the same patient experiencing both generalized seizures as absence and partial seizures as rolandic seizures, separated by a period of seizure freedom between both seizure types, appears to be extremely rare. We describe for the first time the atypical evolution of CAE in two patients who experienced BCECTS some months after remission of absence seizures and normalization of electroencephalographic recordings, while under adequate anticonvulsant treatment. 2. Patient 1 A 10-year-old right-handed boy whose family history was positive for his father with epilepsy in childhood. All developmental milestones were achieved. At the age of 3 years and 10 months, he began to have typical absence occurring several times a day with abrupt and clear impairment of consciousness, sometimes with mild clonic components. His waking video-eeg showed typical absence seizures, with the spike-and-slow-wave complexes occurring at a frequency of 3 Hz and lasting s /$ see front matter ß 2011 British Epilepsy Association. Published by Elsevier Ltd. All rights reserved. doi: /j.seizure
2 [(Fig._1)TD$FIG] C. Cerminara et al. / Seizure 21 (2012) Fp1-F3 F3-C3 C3-P3 P3-O1 Fp1-T3 T3-O1 T3-C3 C3-Cz Cz-C4 C4-T4 Fp2-F4 F4-C4 C4-P4 P4-O2 Fp2-T4 T4-O2 MK-RF TM-RF Fig. 1. Ictal EEG: spike-waves with typical absence seizures at 3 c/s (Patient 1). Posterior delta rhythm (2.5 3 Hz) was found (Fig. 1). Physical and neurological examinations were normal. Treatment with valproic acid (VPA) was started (25 mg/kg/day), but he did not respond to VPA (30 mg/kg/day). Lamotrigine was introduced as an add-on to VPA with a slow titration, beginning with 0.2 mg/kg/day, and no further seizures occurred. The child had neuropsychological screening tests (Wechsler Intelligence Scale for Children-III and Child Behavior Checklist) when he was absence seizure-free with a combination of valproic acid and lamotrigine; the results were total IQ = 95; verbal IQ = 96 and performance IQ = Structured [(Fig._2)TD$FIG] questionnaires completed by his parents revealed normal anxiety, depression and somatization indices. The patient did not show cognitive impairment, learning disabilities or behavioral disorders. Six months later, an EEG recording in wakefulness and sleep displayed left diphasic sharp-waves localized over the centrotemporal leads, with a marked increase in frequency during sleep (Fig. 2). In the same week, the child had two nocturnal attacks with excessive pooling of saliva, speech arrest, tonic clonic activity of the face and preservation of consciousness. A 24-h EEG recording was performed that showed bilateral synchronous and asynchro- Fig. 2. Interictal EEG: bilateral centro-temporal spikes (Patient 1).
3 72 C. Cerminara et al. / Seizure 21 (2012) nous subcontinuous centrotemporal spikes during nocturnal sleep. The boy had a neurocognitive reassessment using Colored Progressive Matrices, which proved to be normal. His parents reported that the child never showed behavioral disturbances. Treatment was discontinued 2 years and 6 months later, and no further seizures have occurred. The EEG continues to show several abnormalities in the centrotemporal areas. The brain MRI was normal. 3. Patient 2 An 8-year-old right-handed girl with normal psychomotor development. Her family history was positive for an uncle with epileptic seizures. At the age of 3 years and 3 months, she experienced her first and only complex febrile seizure. An EEG revealed sporadic spikes in the frontal-temporal regions, which were more evident on the right side. At the age of 7 years, she was referred to our hospital because she had seizures described as absences lasting a few seconds, with sudden onset and cessation. A video-eeg was performed which showed bilateral, synchronous and symmetric spike-and-wave discharges at 3 cycles per second associated with loss of consciousness, lasting 8 12 s (Fig. 3). Photic stimulation induced absence seizures. Neurological and physical examinations and brain MRI were all normal. Valproic acid was introduced at 20 mg/kg/day, and she has responded very well to therapy. The girl showed a normal neuropsychological profile as evaluated by the Wechsler Intelligence Scale for Children-III and the Child Behavior Checklist; her total IQ was 102, verbal IQ was 105 and performance IQ was Four months later, a subsequent EEG showed bilateral centrotemporal spikes which tended to increase in frequency during slow-wave sleep, especially phase II (Fig. 4). Her mother had noticed, one hour after the girl fell asleep, one episode characterized by tonic deviation of the mouth, with speech arrest and drooling. The seizure lasted less than 1 min, and the child was conscious during the whole seizure. She is taking VPA (25 mg/kg/day) and, 18 months after the partial seizure, she has been seizure-free until now. Her parents have not reported any scholastic difficulties or behavioral problems. Ten months later, the patient had a neuropsychological reassessment using Colored Progressive Matrices, which showed normal cognitive performance. [(Fig._3)TD$FIG] 4. Discussion We have described two patients, with normal neurocognitive profiles, affected by idiopathic generalized epileptic syndrome with typical absences, 9 who experienced BCECTS after remission of seizures and normalization of EEG recordings. To the best of our knowledge, this is the first description of seizures with generalized onset and focal electroclinical evolution. There are some reports, albeit not many, that show the concomitance of CAE and BCECTS in the same patients or the later occurrence of generalized epilepsy in patients with a history of partial epilepsy. We did not find any description of clinical cases with idiopathic generalized epilepsy onset, such as childhood absence epilepsy, who, after a period of seizure freedom, experienced partial seizures with the electroclinical characteristics of BCECTS. In most cases described in the literature, absence seizures always started after the onset of benign focal epilepsy and the contrary has never occurred yet. Gambardella et al. 5 reported patients who experienced absence epilepsy 1 4 years after recovering from an electroclinical picture characteristic of BCECTS. Ramelli et al. 9 found five children who showed generalized synchronous 3 Hz spike-and-wave complexes as well as centrotemporal spikes in the same EEG or in different EEGs. These EEG findings did not always correspond with the electroclinical presentation. In a recent study, Dimova and Daskalov 6 investigated the possible presence and incidence of clinical and/or EEG features of absences in rolandic epilepsy and vice versa. Five cases out of 34 children with childhood absence epilepsy were identified with an EEG focus of the rolandic type. Only one child in this study shares certain clinical and EEG characteristics with ours: Dimova s patient experienced both absence and rolandic seizures, separated by a period of seizure freedom between both seizure types, while under adequate anticonvulsant treatment. Furthermore, 4 children with manifestations of absences in the course of treated rolandic epilepsy were those initially receiving carbamazepine (CBZ). In these patients described by Dimova et al., it is possible that CBZ may induce absence seizures. For example, carbamazepine (CBZ) may exacerbate both absence seizures and focal seizures. Dimova et al. reported this kind of change in four patients who started on CBZ and one with valproic acid. There have been previous reports that CBZ may exacerbate absence seizures or atypical AS, especially in children Fig. 3. Ictal EEG: spike-waves with typical absence seizures at 3 c/s (Patient 2).
4 [(Fig._4)TD$FIG] C. Cerminara et al. / Seizure 21 (2012) Fp2-F8 F8-T4 T4-T6 T6-O2 Fp2-F4 F4-C4 C4-P4 P4-O2 Fz-Cz Cz-Pz Fp1-F7 F7-T3 T3-T5 T5-O1 Fp1-F3 F3-C3 C3-P3 P3-O1 MK TM SONNO Fig. 4. Interictal EEG: bilateral centro-temporal spikes (Patient 2). Similar findings have been reported for phenobarbital, lamotrigine and vigabatrin One of our patients did not respond well to the therapy with valproic acid; lamotrigine was started, and the absences disappeared. Lamotrigine can induce seizure deterioration, and the appearance of a new seizure type in patients with idiopathic or cryptogenic epilepsies could be attributed to the introduction of an antiepileptic drug or to an untypical course of the disease. 19,20 However, in our case it is not possible to clearly define a temporal relation between the occurrence of interictal centrotemporal spikes on the EEG and the introduction of lamotrigine. Valproic acid and lamotrigine were discontinued 2 years and 6 months after seizure remission and no further seizures have occurred, but the EEG continues to show several epileptic abnormalities in the centrotemporal areas, primarily during stage I II of sleep. So we could not attribute this finding to the medication prescribed, and this observation could support the hypothesis that some crossover phenomena may occur between BCECTS and CAE. Both absence epilepsy and BCECTS have multifactorial pathogenesis, and genetic factors play a large role in these epileptic syndromes. 21,22 Some authors have suggested that the two epileptic phenotypes with similar hereditary patterns may indicate a neurobiological continuum. On the other hand, the extreme rarity of coexistence or the later occurrence of two different types of epileptic syndromes in the same patient makes the hypothesis of a neurobiological and genetic continuum less feasible. Moreover, family studies of idiopathic localization-related epilepsies and idiopathic generalized epilepsies (IGE) show that BCECTS and CAE are not part of a continuum but are polygenic disorders, with individual phenotypes being due to a particular grouping of genes. 23 Although the interactions of several genetic factors are the rule in childhood epilepsy, until recently, no family studies have provided the basis for a genetic link between EEG focal and generalized traits. 21 The evolving concepts on the pathophysiology of absence seizures, such as the cortical focus theory, suggest that absence seizures could originate from restricted regions of the cerebral cortex. The new theories support the idea that spike-wave discharges have a focal onset in the cortex. Results of recent studies in animal models suggest that a cortical focus is the dominant factor in initiating the paroxysmal oscillation within the corticothalamic loops, and that the large-scale synchronization is mediated by means of an extremely fast intracortical spread of seizure activity. 24 The authors propose that these mechanisms may form the basis for a hypothesis concerning the pathophysiology of human absence. Furthermore, in line with the cortical focus theory, the bidirectional character of corticothalamic interaction could vary in its dominant direction not only throughout one seizure but also during periods of brain maturation. 24 Specific life periods of greater susceptibility to changes in the brain networks, such as childhood and puberty, might influence the internal facilitation or suppression of the corticothalamic loops, thus giving rise to the expression of different epileptic phenomena that could be manifested simultaneously or subsequently, as observed in our cases. 7 Several findings in patients with generalized epilepsy support the focal origin of generalized seizures. Clinical studies have suggested a cortical origin with maximal frontal lobe involvement. 25 Niedermeyer et al. 25 implanted electrodes in patients with absence seizures and found continuous focal spikes in the frontal lobe. These results indicate that the frontal lobe may be related to the occurrence of 3 spike-and-wave complexes. 26,27 However, the epileptic foci observed in our patients 4 6 months after the absence seizures remission were located in the centrotemporal area. There is no clear evidence that generalized spike-and-wave can be induced by focal discharges in other regions of the brain than the frontal lobe. In the context of exploring the underlying circuit mechanisms of spike-wave discharge and the circuit pathology of benign focal epilepsy, some investigators include EEG findings. On the EEG, a
5 74 C. Cerminara et al. / Seizure 21 (2012) variable fraction of benign focal epilepsy patients will exhibit diffuse spike-and-wave discharge; these discharges can be modulated by the arousal level, and often occur during sleep. The possible occurrence of generalized spike-and-wave discharges in patients with BCECTS has been well documented. 28,29 Some studies on hypersynchronous thalamocortical activity in mouse mutants suggest interesting implications for the mechanisms of pathogenesis and understanding epileptiform activity. An important synaptic element in the thalamocortical circuit is a demonstrated reciprocal connectivity between TRN cells. 30,31 It has been proposed that this can either promote or desynchronize thalamocortical oscillations. 32 Huntsman et al. 32 have shown that mutant mice which were devoid of a particular GABA subunit (p3) lacked functional connectivity between TRN cells; these mice had absence seizures and a very high degree of widespread hypersynchrony in isolated thalamic slices. These findings suggest that the reciprocal interconnections between TRN cells normally serve to desynchronize thalamocortical activity and prevent widespread (i.e., generalized) activity. An interesting observation in the p3 mouse mutant study was that, in a small fraction ( 10%) of isolated thalamic slices from control animals, focal reverberant activity was found. In other words, network responses that resembled the activity of absence seizure could be evoked in control thalamic slices, but this activity remained restricted to small regions of the slice. The authors conclude that, at least in the isolated thalamus, circuit mechanisms exist for the production of local recurrent oscillatory responses. This experimental study provides some interesting speculations about a subtle defect in cortical excitability, specifically within the appropriate cortical region, which may allow the expression of rolandic spikes. 33 In conclusion, while the coexistence of different seizure types within an epileptic syndrome is not uncommon, the occurrence of childhood absence and BCECTS in the same child appears to be extremely rare, and this extraordinary event supports the hypothesis that CAE and BCECTS are two distinct epileptic conditions. However, recent interesting observations in animal models suggest that BCECTS and CAE could be pathophysiologically related and genetic links could play a large role. References 1. Callenbach PM, Geerts AT, Arts WF, van Donselaar CA, Peters AC, Stroink H, et al. Familial occurrence of epilepsy in children with newly diagnosed multiple seizure: dutch study of epilepsy in childhood. Epilepsia 1998;39: Watanabe K. Benign partial epilepsies. In: Wallace SJ, Farrell K, editors. Epilepsy in children. 2nd ed. London: Arnold; p Dalla Bernardina B, Sgrò V, Fejerman N. Epilepsy with centro-temporal spikes and related syndrome. In: Roger J, Bureau M, Dravet Ch., Genton P, Tassinari C, Wolf P, editors. Epileptic syndromes in infancy, childhood and adolescent. London: John Libbey Eurotext Ltd.; p Panayotopoulos CP. Idiopathic generalized epilepsies. In: Panayotopoulos CP, editor. The epilepsies: seizures, syndromes and management. 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Clin Neurophysiol 2004;115(January (1)): Corda D, Gelisse P, Genton P, Dravet C, Balbdy-Moulinier M. Incidence of druginduced aggravation in benign epilepsy with centrotemporal spikes. Epilepsia 2001;40: Montenegro MA, Guerriero MM. Coexistence if childhood absence and rolandic epilepsy. J Child Neurol 2006;21: Cerminara C, Montanaro ML, Curatolo P, Seri S. Lamotrigine-induced seizure aggravation and negative myoclonus in idiopathic rolandic epilepsy. Neurology 2004;27: Doose H, Brigger-Heuer B, Neubauer B. Children with focal sharp waves: clinical and genetic aspects. Epilepsia 1997;38: Neubauer B, Stefani U, Doose H. The genetics of rolandic epilepsy and related condition: multifactorial inheritance with a major gene effect. In: Berkovic SF, Genton P, Hirsch E, Picard F, editors. The idiopatic age-related focal epilepsies. Genetics of focal epilepsies: clinical and molecular biology. London: John Libbey & Company; p Berkovich SF. Regional manifestations of idiopathic epilepsies: an antithesis. In: Wolf P, editor. Epileptic seizures and syndromes. London: J. Libbey Ltd.; p Meeren HK, Pijn JP, Van Luijtelaar EL, Coenen AM, Lopes da Silva FH. Cortical focus drives widespread corticothalamic networks during spontaneous absence seizure in rats. J Neurosci 2002;22: Hughes JR. Absence seizures: a review of recent reports with new concepts. Epilepsy and behaviour 2009;15(August (4)): [Epub 2009 July 24]. 25. Niedermeyer E. Primary (idiophatic) generalized epilepsy and underlying mechanisms. Clin Electroencephalogr 1996;27: Holmes MD, Brown M, Tucker DM. Are generalized seizures truly generalized? Evidence of localized mesial frontal and frontopolar discharges in absence. Epilepsia 2004;45(December (12)): Gelisse P, Genton P, Bureau M, Dravet C, Guerrini R, Viallat D, et al. Are there generalised spike waves and typical absences in benign rolandic epilepsy? Brain Dev 1999;21: Lombroso CT. 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