Transient Oromotor Deficits in Children with Benign Childhood Epilepsy with Central Temporal Spikes

Transcription

1 Epilepsia, 42(5): , 2001 Blackwell Science, Inc. International League Against Epilepsy Clinical Research Transient Oromotor Deficits in Children with Benign Childhood Epilepsy with Central Temporal Spikes *Uri Kramer, Bruria Ben-Zeev, *Shaul Harel, and Sarah Kivity *Child Developmental Center & Pediatric Neurology Unit, Tel Aviv Sourasky Medical Center, Pediatric Neurology Unit, Chaim Sheba Medical Center, and Pediatric Neurology Unit, Schneider Medical Center, all affiliated with the Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel Summary: Purpose: To describe transient oromotor deficits in benign childhood epilepsy with centrotemporal spikes (BCECTS), an idiopathic age-specific epileptic syndrome with a benign course. Methods: Five children with BCECTS and intermittent dysarthria and drooling not in the context of typical clinical seizures are presented. Results: The periods of oromotor deficits correlated with increased seizure frequency in all children. Concomitant EEGs that were recorded during periods of dysarthria in four of the children revealed focal electrographic seizures. The reported children did not differ from other patients with BCECTS in any other respect. Conclusions: Transient oromotor dysfunction is a rare ictal phenomenon that occurs in children with BCECTS with no other unique clinical features. Key Words: Epilepsy Benign rolandic Speech Language Centrotemporal. Benign childhood epilepsy with centrotemporal spikes (BCECTS) is an idiopathic age-specific epileptic syndrome with a benign course. The seizures are characterized by hemifacial motor seizures and are frequently associated with somatosensory symptoms. They frequently involve the ipsilateral hand or hand and leg and are occasionally generalized. The onset of BCECTS is between the age of 3 and 13 years (1,2). Whereas the syndrome is considered as being benign, subtle deficits in neuropsychological tests of children with BCECTS have been described over the past few years (3 5). In some patients, there is evolution into either a benign atypical pattern of the disease (6,7) or into other epileptic syndromes such as Landau Kleffner syndrome (LKS) and electrical status epilepticus during slow-wave sleep (ESES) (7,8). In addition, there are rare reports describing temporary oromotor dysfunction with speech disturbances in a small subgroup of children with BCECTS. These manifestations were associated with a status epilepticus of unilateral facial clonic activity in seven cases (7,9 11), whereas only anarthria and sialorrhea associated with continuous or frequent noncontinuous discharges, but not Accepted December 21, Address correspondence and reprint requests Dr.U. Kramer at Child Developmental Center, Beit Habriut Strauss, 14 Balfour Street, Tel Aviv 65211, Israel. umkramer@netvision.net.il in the context of clinical seizures, were observed in 10 other cases (7,8,12 16). This condition, which is termed anterior opercular syndrome in the French literature (11,15), is not associated with perisylvian malformation, which is necessary for the diagnosis of opercular syndrome (17,18). In most reported cases, the oromotor deficits resolved with time without sequelae of any permanent speech deficit. The detailed description of these additional five children with BCECTS and different variations of transient oromotor deficits further delineates the boundaries of this phenomenon, thus contributing to our understanding of this condition. CASE REPORTS Case 1 This 7.5-year-old boy had a normal perinatal, family, and medical history. Neurologic examination and developmental status were normal. He presented at the age of 6.5 years with a typical episode of BCECTS. Two months later, he experienced several typical seizures, including a 30-min-long episode of unilateral facial clonic activity, after which treatment with carbamazepine (CBZ) was initiated. The initial sleep EEG revealed a very active left centrotemporal typical rolandic focus. The brain magnetic resonance imaging (MRI) was nor- 616

2 SPEECH DEFICIT IN BENIGN ROLANDIC EPILEPSY 617 mal. Seven months after the first bout of seizures and initiation of treatment, the seizures reappeared. In addition, marked speech deterioration manifested by anomia, slurred speech, as well as drooling and difficulties in swallowing occurred for the first time, but not concomitant with the seizures. An awake EEG performed at that time revealed prolonged periods of continuous focal epileptic activity with rolandic configuration in the left centrotemporal region (Fig. 1). The second brain MRI was also normal. The CBZ blood level at that point was 8.1 g/ml. A paradoxic response to CBZ was suspected, and treatment was changed to phenytoin (PHT),which led to immediate improvement. Three months later, PHT was replaced by lamotrigine (LTG) to avoid PHT-related adverse reactions, whereupon another seizure episode ensued. Drooling and dysarthria also reappeared. LTG was tapered, and treatment with valproate (VPA) was initiated. Since the introduction of VPA, 1 year ago, there have been no episodes of seizures, drooling, or dysarthria. A comprehensive evaluation by a speech pathologist that was conducted several weeks after the acute period of speech deterioration revealed a mild deficit in the production of oral pressure with tight lips and a mild deficit in tongue movements. In addition, there were naming and word-retrieving deficits. A second evaluation performed a month later revealed an improvement of naming but no change in word-retrieving ability. Case 2 This 15-year-old girl with nonsignificant family, perinatal, and medical history presented with typical events of BCECTS at the age of 10.5 years. Repetitive EEGs revealed bilateral independent rolandic spikes, at times temporal and at times either frontotemporal or occipital. The brain MRI was normal. Treatment with CBZ was initiated after the third occurrence. Seizures recurred after a seizure-free period of 3 years. During each of the past 2 years, there were a few single days during which she had multiple episodes of slurred speech, unaccompanied by drooling. Typical seizures also occurred on some of these days. The CBZ dosage was gradually increased after each episode. The EEG performed on one of the days during which there was a seizure with speech disturbance revealed no increase of interictal epileptic activity. Case 3 This 9-year-old boy had a normal prenatal and perinatal history as well as an unremarkable neonatal period and normal developmental milestones. At age 5 years, the parents noticed a change in speech fluency: the speech had become slurred, and it was accompanied by excessive drooling. The change was related to aphtostomatitis. During the next few weeks, he developed occasional unilateral blinking which was not medically evaluated. The patient was admitted to hospital after a nocturnal generalized tonic clonic seizure (GTC). An awake EEG showed continuous bilateral rolandic spikes activity, predominantly in the frontotemporal regions, that secondarily generalized during drowsiness (Fig. 2). The child was alert but demonstrated slow responses and altered speech fluency. The rest of the neurologic exami- FIG. 1. Interictal activity showing continuous focal rolandic activity at C3-T3 in patient 1.

3 618 U. KRAMER ET AL. FIG. 2. Ictal activity showing continuous rolandic activity in the frontotemporal regions bilaterally in patient 3. nation was normal. There was only temporary response to benzodiazepine (BZD) injection. Treatment with VPA resulted in moderate improvement in the frequency of epileptiform activity on EEG. There were no more GTCs, but speech remained slurred, and the excessive drooling persisted. The parents noticed occasional orolingual seizure during sleep. The MRI performed at that point was normal. Treatment was then changed to sulthiame, and the parents noticed significant improvement 3 weeks later. Speech became fluent, and the drooling subsided. An EEG performed in the awake state was normal, whereas a sleep EEG showed infrequent rolandic spikes. The child has been seizure free for 4 years. Speech is normal, but reading skills are poor. The EEG still shows occasional bilateral rolandic spikes. Case 4 This 9-year-old girl with uneventful perinatal and medical history, first presented at age 4 years with recurrent nocturnal partial seizures and typical bilateral rolandic spikes on EEG aggravated in sleep. After the diagnosis of BCECTS, treatment with CBZ was initiated, and the seizures subsequently resolved. Eight months later, the parents reported prolonged episodes of drooling and slurred speech during the awake state. During one of these episodes (that lasted 3 h), an EEG was performed and showed continuous bilateral spike wave activity with right parietocentral predominance. The neurologic examination was normal except for orolingual dyspraxia. The brain MRI was also normal. Treatment with BZDs [clobazam (CLB) p.o. and diazepam (DZP) i.v.] and VPA did not have any significant effects. She was then given a combination of CLB and sulthiame, after which the orolingual symptoms (including slurred speech, drooling and nocturnal facial twitching) disappeared entirely. The EEG during awake and sleep states had completely normalized. Eight months later, a follow-up sleep EEG did show occasional infrequent rolandic spikes; however, the patient remained free of seizures, and there was no recurrence of the orolingual symptoms. She is currently being tapered off antiepileptic drugs (AEDs). Case 5 This 17-year-old boy had an uneventful family, perinatal, and medical history. He presented with typical unilateral clonic movements of face and hand at the age of 8 years. A routine EEG revealed bilateral independent typical rolandic spikes in the centrotemporal region, more prominent on the left. Two weeks later, after a second attack, treatment with CBZ was initiated. A follow-up EEG showed a marked decrease in the frequency of epileptic activity. After a 2-year seizure-free

4 SPEECH DEFICIT IN BENIGN ROLANDIC EPILEPSY 619 period, the CBZ was tapered. Six months after discontinuation of treatment, the patient presented with a brief typical third seizure. After this seizure, there was a period of anarthria and drooling that lasted 90 min and resolved after administration of i.v. DZP. An EEG study performed during that episode revealed continuous focal epileptic activity in the right centrotemporal region. The spikes had a typical rolandic configuration. CBZ was readministrated, and the child has been seizure free since. There were no more events of anarthria, and consequent EEGs were normal. DISCUSSION Five children with BCECTS and transient dysarthria and drooling are presented (Table 1). The periods of oromotor deficits correlated with increased seizure frequency in all except one and could occur any time during the course of the disease. The age of seizure onset in this group was years. The patients had from one to ten typical seizures each. One patient (case 3) was also reported to have multiple brief episodes of eye blinking, which was probably unilateral facial twitching. Neurologic examination and developmental status were normal for all five children. Four patients underwent brain MRI with normal results. In two patients, either an increase in or reintroduction of CBZ dosage resulted in the resolution of the oromotor deficit, whereas in other two patients, a change to other AEDs (e.g., PHT, sulthiame, VPA, and CLB) was needed. We do not think that this phenomenon is directly related to CBZ but rather is a feature of disease deterioration, which may be either part of its natural course in some patients or the result of CBZ-related exacerbation in others, as described by Deonna et al. (8). This hypothesis is supported by Prats et al. (19), who describe six patients with BCECTS that deteriorated with evolution to ESES with neuropsychological deterioration. Four of these patients were treated with CBZ and two with VPA. All six patients remitted after either discontinuation of drug treatment or substitution to another drug. In addition, one of our patients (case 5) presented with transient oromotor deficit while not being treated. In only one of our patients (patient 4) did sulthiame succeed in resolving the deterioration, which failed to be resolved by CBZ; thus our data cannot support the observation of others that sulthiame might be superior to CBZ in BCECTS (20). In addition, our data are not conclusive enough to recommend any specific treatment in the case of failure of CBZ. The benign nature of BCECTS was recently challenged by evidence of subtle cognitive deficits, such as attention, visuomotor skills, and a variety of specific language deficits including recall of auditory verbal material, auditory perception, reading, spelling, expressive grammar, and verbal fluency (3,21). Verbal tasks are particularly influenced by left-sided discharges (22). Using a dual-task procedure test, Piccirilli et al. (23) demonstrated that there is a partial transfer of speech functions to the right hemisphere in children with BCECTS and a left temporal epileptic focus. Oromotor deficits characterized by facial weakness, hypersialorrhea, difficulties in chewing and swallowing, reduced speech fluency, and difficulties in pronunciation and articulation were described in patients with BCECTS (7,8,13 15). Although these deficits were correlated with continuous epileptic discharges in some of the patients, there was only an increase of the frequency of interictal discharges in others. An EEG recorded during periods of dysarthria in four children in our study revealed focal electrographic seizures. The EEG of the fifth child (patient 2), which was performed during periods of events of oromotor deficit but not during an event, did not show any increase from baseline spike frequency. Thus, the events fit the definition of an electroclinical event in four of the patients, whereas there were multiple, brief clinical events in a fifth one in whom a continuous discharge was not evidenced. We postulate that an EEG performed during an event would have revealed a continuous discharge in this patient. It is also possible that a transient oromotor deficit is caused by an increased interictal epileptic activity as part of an inhibitory mechanism (14,24) affecting functions of the lower motor strip. It is suggested that these phenomena represent a step of the continuum that includes also Landau Kleffner syndrome (LKS) and ESES (7,8). We believe, however, that these are clearly separate entities. Whereas the continuous focal epileptic activity causes a localized specific cognitive deficits in LKS and ESES, the deficits in BCECTS are transient and second- Case TABLE 1. Patients with transient oromotor deficits: relationship with typical seizures, EEG, and treatment Onset (yr) Increased Sz frequency EEG during event Interictal EEG Lat. of EEG abn. Initial AED AED at resolution Yes ND Continuous Left CBZ PHT Yes ND Epileptic Bilateral CBZ CBZ 3 5 Yes Continuous Bilateral None Sulthiame 4 4 No Continuous Bilateral CBZ Clobazam + sulthiame 5 8 Yes Continuous Right None CBZ Sz, seizures; ND, not done; CBZ, carbamazepine; PHT, phenytoin; Lat, lateralization; abn, abnormality.

5 620 U. KRAMER ET AL. ary to sensorimotor dysfunction of specific organs due to continuous or almost continuous activation. The temporal pattern of the deficit varied from patient to patient: Two patients had prolonged single episodes lasting a few hours each, whereas three other patients had multiple brief episodes during periods that lasted from a single day to a few weeks. All our patients showed rapid improvement after a change in or an increase of AEDs. This was also the case in the patients described by Deonna et al (8). All the patients in their series, as well as those described in their review, presented with bilateral epileptic discharges. Two of our patients had unilateral epileptic discharges, either on the right or on the left, whereas the other three had bilateral epileptic activity. The significance of this observation is not entirely clear. One of our patients (patient 1) was found to have word-retrieving difficulties in a formal language test. Word-retrieving difficulties were also described in one patient in another study (14). Difficulties in word retrieving should not be influenced by a sensorimotor deficit and represent a higher function deficit. The significance of this finding is not clear, especially when a preevent test is not available. None of our patients presented with any sequelae of a motor speech deficit. There are rare descriptions, however, of permanent speech dysfluency after periods of oromotor deficits (8,12). Scheffer et al. (25) described family members with autosomal dominant rolandic epilepsy, which is a separate syndrome from BCECTS: these patients presented with speech dyspraxia either at childhood, when the disease was still active, or at longterm follow-up. Our five patients were identified in three busy outpatients clinics in the same city during a period of a few years, suggesting that transient oromotor dysfunction is not as rare as it is traditionally held to be. According to Fejerman et al. (7), its prevalence is believed to be 0.6% of patients with BCECTS. We believe that obtaining a careful history will elicit an even higher prevalence. Although the symptoms of oromotor dysfunction were seen during periods of high seizure frequency, it was characteristic of the parents not to seek help for oromotor deficits but provided the information retrospectively when the child was seen after a typical rolandic seizures. These specific periodic oromotor deficits should be regarded as part of the clinical spectrum of BCECTS syndrome and should be identified and promptly treated because it is usually a manifestation of clinical deterioration. Acknowledgment: We thank Esther Eshkol for editorial assistance. REFERENCES 1. Loiseau P, Beaussart M. The seizures of benign childhood epilepsy with rolandic paroxysmal discharges. Epilepsia 1973;14: Lerman P, Kivity S. The benign focal epilepsies of childhood. In: Pedley TA, Meldrum BS, eds. Recent advances in epilepsy. Edinburgh: Churchill Livingston, 1986;3: Croona C, Kihlgren M, Lundberg S, Eeg-Olofsson O, Eeg- Olofsson KE. Neuropsychological findings in children with benign childhood epilepsy with centrotemporal spikes. Dev Med Child Neurol 1999;41: Gunduz E, Demirbilek V, Korkmaz B. Benign rolandic epilepsy: neuropsychological findings. Seizure 1999;8: Binnie CD, Marston D. Cognitive correlates of interictal discharges. Epilepsia 1992;33(suppl 6):S Aicardi J, Chevrie JJ. Atypical benign partial epilepsy of childhood. Dev Med Child Neurol 1982;24: Fejerman N, Caraballo R, Tenembaum SN. Atypical evolutions of benign localization-related epilepsies in children; are they predictable? Epilepsia 2000;41: Deonna TW, Roulet E, Fontan D, Marcoz JP. Speech and oromotor deficits of epileptic origin in benign partial epilepsy of childhood with rolandic spikes (BPERS): relationship to the acquired aphasia-epilepsy syndrome. Neuropediatrics 1993;24: Fejerman N, Di Blasi M. Status epilepticus in benign partial epilepsies in children: report of two cases. Epilepsia 1987;28: Colamaria V, Sgro V, Caraballo R, et al. Status epilepticus in benign rolandic epilepsy manifesting as anterior operculum syndrome. Epilepsia 1991;32: Boulloche J, Husson A, Le Luyer B,Le Roux P. Dysphagia, speech disorders and centrotemporal spikes-waves. Arch Fr Pediatr 1990; 47: Roulet E, Deonna T, Despland PA. Prolonged intermittent drooling and oromotor apraxia in childhood epilepsy with centrotemporal spikes. Epilepsia 1989;30: Puig JS, Ramos E, Mateos V. Sindrome opercular bilateralepileptico. Congresso National de Neuropediatria. Sevilla (Spain) Abstract de Saint Martin A, Petiau C, Massa R, et al. Idiopathic rolandic epilepsy with interictal facial myoclonia and oromotor deficit: a longitudinal EEG and PET study. Epilepsia 1999;40: Septtien L, Grass P, Giroud M, Dumas R. Acute anterior biopercular syndrome of cortical origin in epilepsy with rolandic spikes. Rev Neurol Paris 1992;148: Shafrir Y, Prensky L. Acquired epileptiform opercular syndrome: a second case report, review of the lterature, and comparison to the Landau-Kleffner syndrome. Epilepsia 1995;36: Iannetti P, Rauci U, Basile LA, et al. Benign epilepsy of childhhod with centrotemporal spikes and unilateral developmental opercular dysplasia. Childs Nerv Syst 1994;10: Kuzniecky R, Andermann F, Guerrini R. The epileptic spectrum in the congenital bilateral perisylvian syndrome: CBPS multicenter collaborative study. Neurology 1994;44: Prats JM, Graraizar C, Garcia-Nieto ML, Madoz P. Antiepileptic drugs and atypical evolution of idiopathic partial epilepsy. Pediatr Neurol 1998;18: Lerman P, Lerman-Sagie T. Sulthiame revisited. J Child Neurol 1995;10: Staden U, Isaacs E, Boyd SG, et al. Language dysfunction in children with rolandic epilepsy. Neuropediatrics 1998;29: Rugland AL, Bjoaes H, Henrikson O, Loyning A. The development of computerized tests as a routine procedure in clinical EEG practice for the evaluation of cognitive changes in patients with epilepsy. 17th Epilepsy International Congress (1987): Abstracts P Piccirilli M, D Alessandro P, Tiacci C, Ferroni A. Language lateralization in children with benign partial epilepsy. Epilepsia 1988; 29: Engel J Jr. Excitation and inhibition in epilepsy. Can J Neurol Sci 1996;23: Scheffer IE, Jones L, Pozzebon M, et al. Autosomal dominant rolandic epilepsy and speech dyspraxia: a new syndrome with anticipation. Ann Neurol 1995;3: