Epilepsy Research (2014) 108, 1604—1608
journal homepage: www.elsevier.com/locate/epilepsyres
Lacosamide efficacy in epileptic syndromes with continuous spike and waves during slow sleep (CSWS) Salvatore Grosso a,d,∗, Pasquale Parisi b, Lucio Giordano c, Rosanna di Bartolo d, Paolo Balestri d a
Neurology-Immunology and Endocrinology Unit, University of Siena, Italy Child Neurology, Chair of Pediatrics, NESMOS Department, Faculty of Medicine and Psychology, ‘‘Sapienza University’’, Rome, Italy c Child Neuropsychiatric Unit, Civile Hospital, Brescia, Italy d Department of Pediatrics, University of Siena, Italy b
Received 5 July 2013; received in revised form 9 August 2014; accepted 31 August 2014 Available online 16 September 2014
KEYWORDS Epileptic encephalopathy; ESES; Epilepsy; Antiepileptic drugs; Pediatrics
Summary Background: Epileptic syndromes with continuous spikes-waves during sleep (CSWS) represent a wide spectrum of epileptic disorders having CSWS as a common EEG-feature. Defined therapeutic strategies are still lacking. We evaluated the efficacy of lacosamide add-on therapy on the EEG, behavior, and cognition in children with CSWS. Material and methods: Eight children with CSWS refractory to other conventional antiepileptic drugs were included in the study. A 24-h EEG recording was performed at 6-month-interval in all patients. The spike-wave index (SWI) was obtained in each 24-h EEG recording. Neuropsychological data were obtained before lacosamide introduction and after a minimum of 12 months of therapy. Results: After a 6-month period of therapy, 75% of patients was defined as responder, 12.5% as partial responder and another 12.5% as non-responder. In particular, 24-h EEG normalized in 3 cases (37%). After a minimum of 12 months, 24-h EEG normalized in another patient while two patients showed electroclinical relapses. A total of 62.5% of patients was therefore defined as responder. Neuropsychological functions slightly improved in 25% of patients. Conclusion: Although further studies are needed to validate our observations, this study suggests that lacosamide add-on therapy may be safe and effective in children affected by CSWS. © 2014 Elsevier B.V. All rights reserved.
∗ Corresponding author at: Neurology-Immunology and Endocrinology Unit, Department of Pediatrics, University of Siena, Viale M. Bracci, Le Scotte, 53100 Siena, Italy. Tel.: +39 0577 586546; fax: +39 0577 586143. E-mail address: [email protected] (S. Grosso).
http://dx.doi.org/10.1016/j.eplepsyres.2014.08.021 0920-1211/© 2014 Elsevier B.V. All rights reserved.
VPA, CLN, CBZ, TPM, AZM, ESM, LEV, Hyd ESM + LEV 20.5 VPA, CLN, LEV, ESM, Hyd
VPA + CLB 13.9
Total AEDs before Lacosamide
Current treatment Lacosamide dose (mg/kg/day)
VPA 12.5
VPA + LEV 9
VPA+ CLN 11.8
VPA 7
VPA, CLB, LEV, ESM, CLN, AZM, TPM, NTZ, Hyd VPA + LEV 14.5 VPA, TPM, CLB VPA, CLB, ESM, Deflazacort VPA, CLB, ESM, Hyd
9.4 yrs/F 4.3 yrs CPS with SG Cryptogenic 4.4 yrs 32 None 12.8 yrs/F 3.2 yrs CPS with SG Cryptogenic 4.8 yrs 38 None 15.9 yrs/F 10.8 CPS Symptomatic 14.1 yrs 14 Sporadic atypical absences 9.2 yrs/M 3.9 yrs CPS Cryptogenic 4.9 yrs 37 None 10.2 yrs/M 5.2 yrs CPS Cryptogenic 6.1 yrs 32 None Age (years)/sex Age at seizure onset (years) Seizure types Etiology Age at CSWS detection CSWS duration (months) Type of seizure recorded
VPA, CLN, ESM, LEV, Hyd
3 2 1 Patient no.
Clinical findings. Table 1
Patients’ characteristic are listed in Table 1. All patients fulfilled the following criteria: (i) behavioral and/or cognitive deterioration and (ii) CSWS pattern on sleep EEG, i.e., epileptic discharges occupying more than 80% during slow wave sleep, a presence of 3—3.5 Hz diffuse bilateral spike-waves, absence of physiologic sleep patterns (spindles, vertex waves), and lack of sleep stage differentiation (1). Etiology was symptomatic in two patients (perisylvian polymicrogyria related to prenatal CMV infection and inversion-duplication of the long-arm of chromosome 13, respectively) and cryptogenic in another six. Three (37%) patients were still experiencing seizures with sporadic atypical absences (patients 2, 5, and 8) and atonic seizures (patient 8) when lacosamide was introduced in therapy. There was no patient affected by Landau—Kleffner syndrome. All patients underwent metabolic screenings, brain MRI, 24-h EEG recording and neuropsychological testing using Wechsler Intelligence Scale for Children III (WISC-III) and Wechsler Preschool and Primary Scale of Intelligence Revised (WPPSI-R). In two patients the Leiter International Performance Scale was used because of severe cognitive deterioration and lack of the ability to cooperate with verbal tasks. The assessment of cognitive development was based on the full IQ (intelligent quotient) scores: 80—100, normal, 60—80, mild delay, 50—60, moderate delay and 50% SWI reduction) in another three (37%) cases. Two patients who were responders after 6 months (cases 2 and 3) relapsed clinically as well as electroencephalographically with the reappearance of the previous EEG (Table 2). Sporadic atypical absences also occurred in patient 6 (Table 2). Neuropsychological data before the introduction of lacosamide and after a minimum of 12 months of treatment were available in 5 (62%) patients (Table 2). Neuropsychological functions improved in two cases (patients 7 and 8) and remained unchanged in another three (patients 3, 4 and 6). A complete neuropsychological assessment was not possible in two children (patients 2 and 5) because of a lack of compliance related to severe cognitive impairments. In addition, no re-testing was performed in patient 1 in whom lacosamide was tailored off after 6 months of therapy. Behavior rated by their parents and the school teacher improved in 75% of patients under lacosamide.
6
Results
Left C-T 90 0
7
8
24-h EEG recording was performed before lacosamide introduction, after a 6-month period and then after a minimum of 12 months of therapy. The difference in SWI pre- and post-lacosamide was defined as the electrographic response to lacosamide add-on treatment, and was subsequently graded as follows: Responders: reduction in SWI > 50%; Partial responders: reduction in SWI between 25 and 50%. Non responders: reduction in SWI < 25% or an increase in SWI.
0
S. Grosso et al. Bilateral C-T 92 10
1606
Lacosamide efficacy in epileptic syndromes with CSWS Valproic acid (VPA), alone or in combination with benzodiazepines, is the treatment of choice of epilepsies with CSWS (Veggiotti et al., 2012; Caraballo et al., 2013). A paradoxical reaction with worsening of seizure frequency and CSWS has been observed in patients placed under oxcarbazepine (Grosso et al., 2006), carbamazepine and phenytoin (Kramer et al., 2009). ACTH and steroids such as prednisone and deflazacort (Grosso et al., 2008) probably remain the most effective medications. However, the long-term use of corticosteroids has several side effects that limit their use for refractory patients (Grosso et al., 2008). Levetiracetam is also effective in CSWS (Capovilla et al., 2004). Lacosamide is a new anticonvulsant effective in focal epilepsy (Verrotti et al., 2013). This is the first study showing lacosamide efficacy in children with CSWS. After 6 months of lacosamide add-on therapy, 75% of patients were responder with more than 50% SWI reduction. Three of them (37%) showed 24-h EEG normalization. Almost all patients (87%) had better attention at school, were more alert and less anxious. After a minimum of 12 months of follow-up, another patient became responder (Table 2). However, two patients who had responded to lacosamide after 6 months, experienced relapse in the following months without modification of the AED regimen. Therefore, after 12 months of lacosamide add-on therapy, 67% of patients were defined as responder, including two patients with complete 24-h EEG normalization. A transitory effect of conventional AED on the CSWS pattern is a very frequent finding and outlines the need to perform long-term observations when studying the efficacy of AED in epileptic children with CSWS (Aeby et al., 2005). Lacosamide was also able to control tonic seizures and atypical absences in two of the three patients who were still experiencing seizures when the drug was placed in therapy. Although two-thirds of our patients experienced a significant improvement in alertness and behavior under lacosamide, neuropsychological functions slightly improved in only two cases. No substantial changes were observed in the remaining group of patients. Our data are in line with results of previous studies (Atkins and Nikanorova, 2011). Of course, main limitations of studies evaluating the effectiveness of medications in the treatment of CSWS are represented by the possible spontaneous recovery which may occur in some patients, the transient electrographic and clinical changes that are not necessarily related to alterations in medication, and the unpredictability of relapse (Atkins and Nikanorova, 2011). We have tried to overcome these problems by evaluating children over a minimum period of 12 months and performing 24-h sleep EEG investigations at 6-month interval after lacosamide introduction. Moreover, concomitant medications and their plasmatic levels remained unchanged during the study (data not shown). So, in our opinion the results we observed in our patients may be directly correlated to lacosamide effects. Of interest, all our patients presented with a refractory type of CSWS since more than three AEDs had already been used before lacosamide therapy. In conclusion, this study shows that lacosamide is a safe AED which may be able to improve the electroclinical impairment in over half of the CSWS patients. Although further investigation on larger series of patients are needed to confirm the present data, our observations might expand the
1607 number of new AEDs reported to be potentially effective in CSWS.
References Aeby, A., Poznanski, N., Verheulpen, D., Wetzburger, C., Van Bogaert, P., 2005. Levetiracetam efficacy in epileptic syndromes with continuous spikes and waves during slow sleep: experience in 12 cases. Epilepsia 46, 1937—1942. Atkins, M., Nikanorova, M., 2011. A prospective study of levetiracetam efficacy in epileptic syndromes with continuous spikes-waves during slow sleep. Seizure 20, 635—639. Capovilla, G., Beccaria, F., Cagdas, S., Montagnini, A., Segala, R., Paganelli, D., 2004. Efficacy of levetiracetam in pharmacoresistant continuous spikes and waves during slow sleep. Acta Neurol. Scand. 110, 144—147. Caraballo, R.H., Veggiotti, P., Kaltenmeier, M.C., Piazza, E., Gamboni, B., Avaria, M.F., Noli, D., Adi, J., Cersosimo, R., 2013. Encephalopathy with status epilepticus during sleep or continuous spikes and waves during slow sleep syndrome: a multicenter, long-term follow-up study of 117 patients. Epilepsy Res. 105, 164—173. Dalla Bernardina, B., Fontana, E., Michelizza, B., Colamaria, V., Capovilla, G., Tassinari, C.A., 1989. Partial epilepsies of childhood, bilateral synchronization, continuous spike-waves during slow sleep. In: Manelis, S., Bental, E., Loeber, J.N., Dreifuss, F.E. (Eds.), Advances in Epileptology. Raven Press, New York, pp. 295—302. Debiais, S., Tuller, L., Barthez, M.A., Monjauze, C., Khomsi, A., Praline, J., de Toffol, B., Autret, A., Barthelemy, C., Hommet, C., 2007. Epilepsy and language development: the continuous spikewaves during slow sleep syndrome. Epilepsia 48, 1104—1110. Grosso, S., Balestri, M., Di Bartolo, R.M., Corbini, L., Vatti, G., Curatolo, P., Balestri, P., 2006. Oxcarbazepine and atypical evolution of benign idiopathic focal epilepsy of childhood. Eur. J. Neurol. 13, 1142—1145. Grosso, S., Farnetani, M., Mostardini, R., Cordelli, D., Berardi, R., Balestri, P., 2008. A comparative study of hydrocortisone versus deflazacort in drug-resistant epilepsy of childhood. Epilepsy Res. 81, 80—85. Kramer, U., Sagi, L., Goldberg-Stern, H., Zelnik, N., Nissenkorn, A., Ben-Zeev, B., 2009. Clinical spectrum and medical treatment of children with electrical status epilepticus in sleep (ESES). Epilepsia 50, 1517—1524. Nickels, K., Wirrel, E., 2008. Electrical status epilepticus in sleep. Semin. Pediatr. Neurol. 15, 60. Panayiotopoulos, C.P., 2005. Epileptic encephalopathies in infancy and early childhood. In: The Epilepsies: Seizures, Syndromes, and Management. Bladon Medical Publishing, Oxford, pp. 183—189. Patry, G., Lyagoubi, S., Tassinari, C.A., 1971. Subclinical electrical status epilepticus induced by sleep in children. A clinical and electroencephalographic study of six cases. Arch. Neurol. 24, 242—252. Scheltens-de Boer, M., 2009. Guidelines for EEG in encephalopathy related to ESES/CSWS in children. Epilepsia 50 (Suppl. 7), 13—17. Tassinari, C.A., Ruboli, G., 2006. Cognition and paroxysmal EEG activities: from a single spike to electrical status epilepticus during sleep. Epilepsia 47 (Suppl. 2), S40—S43. Tassinari, C.A., Rubboli, G., Volpi, L., Billard, C., Bureau, M., 2005. Electrical status epilepticus during slow sleep, including acquired epileptic aphasia. In: Roger, J., Bureau, M., Dravet, C., Genton, P., Tassinari, C.A., Wolf, P. (Eds.), Epileptic Syndromes in Infancy, Childhood and Adolescence. , 4th ed. John Libby Eurotext, Paris, pp. 295—314.
1608 Tassinari, C.A., Cantalupo, G., Rios-Pohl, L., Della Giustina, E., Rubboli, G., 2009. Encephalopathy with status epilepticus during slow sleep: the Penelope syndrome. Epilepsia 50 (Suppl. 7), 4—8. Van Hirtum-Das, M., Licht, E.A., Koh, S., Wu, J.Y., Shields, W.D., Sankar, R., 2006. Children with ESES: variability in the syndrome. Epilepsy Res. 70 (Suppl. 1), 248—258. Veggiotti, P., Cardinali, S., Granocchio, E., Avantaggiato, P., Papalia, G., Cagnana, A., Lanzi, G., 2005. Motor impairment on awakening in a patient with an EEG pattern of unilateral, continuous spikes and waves during slow sleep. Epileptic Disord. 7, 131—136.
S. Grosso et al. Veggiotti, P., Pera, M.C., Teutonico, M.C., Brazzo, D., Ballottin, U., Tassinari, C.A., 2012. Therapy of encephalopathy with status epilepticus during sleep (ESE/CSWS syndrome): an update. Epileptic Disord. 14, 1—11. Verrotti, A., Loiacono, G., Pizzolorusso, A., Parisi, P., Bruni, O., Luchetti, A., Zamponi, N., Cappanera, S., Grosso, S., Kluger, G., Janello, C., Franzoni, E., Elia, M., Spalice, A., Coppola, G., Striano, P., Pavone, P., Savasta, S., Viri, M., Romeo, A., Aloisi, P., Gobbi, G., Ferretti, A., Cusmai, R., Curatolo, P., 2013. Lacosamide in pediatric and adult patients: comparison of efficacy and safety. Seizure 22, 210—216.
journal homepage: www.elsevier.com/locate/epilepsyres
Lacosamide efficacy in epileptic syndromes with continuous spike and waves during slow sleep (CSWS) Salvatore Grosso a,d,∗, Pasquale Parisi b, Lucio Giordano c, Rosanna di Bartolo d, Paolo Balestri d a
Neurology-Immunology and Endocrinology Unit, University of Siena, Italy Child Neurology, Chair of Pediatrics, NESMOS Department, Faculty of Medicine and Psychology, ‘‘Sapienza University’’, Rome, Italy c Child Neuropsychiatric Unit, Civile Hospital, Brescia, Italy d Department of Pediatrics, University of Siena, Italy b
Received 5 July 2013; received in revised form 9 August 2014; accepted 31 August 2014 Available online 16 September 2014
KEYWORDS Epileptic encephalopathy; ESES; Epilepsy; Antiepileptic drugs; Pediatrics
Summary Background: Epileptic syndromes with continuous spikes-waves during sleep (CSWS) represent a wide spectrum of epileptic disorders having CSWS as a common EEG-feature. Defined therapeutic strategies are still lacking. We evaluated the efficacy of lacosamide add-on therapy on the EEG, behavior, and cognition in children with CSWS. Material and methods: Eight children with CSWS refractory to other conventional antiepileptic drugs were included in the study. A 24-h EEG recording was performed at 6-month-interval in all patients. The spike-wave index (SWI) was obtained in each 24-h EEG recording. Neuropsychological data were obtained before lacosamide introduction and after a minimum of 12 months of therapy. Results: After a 6-month period of therapy, 75% of patients was defined as responder, 12.5% as partial responder and another 12.5% as non-responder. In particular, 24-h EEG normalized in 3 cases (37%). After a minimum of 12 months, 24-h EEG normalized in another patient while two patients showed electroclinical relapses. A total of 62.5% of patients was therefore defined as responder. Neuropsychological functions slightly improved in 25% of patients. Conclusion: Although further studies are needed to validate our observations, this study suggests that lacosamide add-on therapy may be safe and effective in children affected by CSWS. © 2014 Elsevier B.V. All rights reserved.
∗ Corresponding author at: Neurology-Immunology and Endocrinology Unit, Department of Pediatrics, University of Siena, Viale M. Bracci, Le Scotte, 53100 Siena, Italy. Tel.: +39 0577 586546; fax: +39 0577 586143. E-mail address: [email protected] (S. Grosso).
http://dx.doi.org/10.1016/j.eplepsyres.2014.08.021 0920-1211/© 2014 Elsevier B.V. All rights reserved.
VPA, CLN, CBZ, TPM, AZM, ESM, LEV, Hyd ESM + LEV 20.5 VPA, CLN, LEV, ESM, Hyd
VPA + CLB 13.9
Total AEDs before Lacosamide
Current treatment Lacosamide dose (mg/kg/day)
VPA 12.5
VPA + LEV 9
VPA+ CLN 11.8
VPA 7
VPA, CLB, LEV, ESM, CLN, AZM, TPM, NTZ, Hyd VPA + LEV 14.5 VPA, TPM, CLB VPA, CLB, ESM, Deflazacort VPA, CLB, ESM, Hyd
9.4 yrs/F 4.3 yrs CPS with SG Cryptogenic 4.4 yrs 32 None 12.8 yrs/F 3.2 yrs CPS with SG Cryptogenic 4.8 yrs 38 None 15.9 yrs/F 10.8 CPS Symptomatic 14.1 yrs 14 Sporadic atypical absences 9.2 yrs/M 3.9 yrs CPS Cryptogenic 4.9 yrs 37 None 10.2 yrs/M 5.2 yrs CPS Cryptogenic 6.1 yrs 32 None Age (years)/sex Age at seizure onset (years) Seizure types Etiology Age at CSWS detection CSWS duration (months) Type of seizure recorded
VPA, CLN, ESM, LEV, Hyd
3 2 1 Patient no.
Clinical findings. Table 1
Patients’ characteristic are listed in Table 1. All patients fulfilled the following criteria: (i) behavioral and/or cognitive deterioration and (ii) CSWS pattern on sleep EEG, i.e., epileptic discharges occupying more than 80% during slow wave sleep, a presence of 3—3.5 Hz diffuse bilateral spike-waves, absence of physiologic sleep patterns (spindles, vertex waves), and lack of sleep stage differentiation (1). Etiology was symptomatic in two patients (perisylvian polymicrogyria related to prenatal CMV infection and inversion-duplication of the long-arm of chromosome 13, respectively) and cryptogenic in another six. Three (37%) patients were still experiencing seizures with sporadic atypical absences (patients 2, 5, and 8) and atonic seizures (patient 8) when lacosamide was introduced in therapy. There was no patient affected by Landau—Kleffner syndrome. All patients underwent metabolic screenings, brain MRI, 24-h EEG recording and neuropsychological testing using Wechsler Intelligence Scale for Children III (WISC-III) and Wechsler Preschool and Primary Scale of Intelligence Revised (WPPSI-R). In two patients the Leiter International Performance Scale was used because of severe cognitive deterioration and lack of the ability to cooperate with verbal tasks. The assessment of cognitive development was based on the full IQ (intelligent quotient) scores: 80—100, normal, 60—80, mild delay, 50—60, moderate delay and 50% SWI reduction) in another three (37%) cases. Two patients who were responders after 6 months (cases 2 and 3) relapsed clinically as well as electroencephalographically with the reappearance of the previous EEG (Table 2). Sporadic atypical absences also occurred in patient 6 (Table 2). Neuropsychological data before the introduction of lacosamide and after a minimum of 12 months of treatment were available in 5 (62%) patients (Table 2). Neuropsychological functions improved in two cases (patients 7 and 8) and remained unchanged in another three (patients 3, 4 and 6). A complete neuropsychological assessment was not possible in two children (patients 2 and 5) because of a lack of compliance related to severe cognitive impairments. In addition, no re-testing was performed in patient 1 in whom lacosamide was tailored off after 6 months of therapy. Behavior rated by their parents and the school teacher improved in 75% of patients under lacosamide.
6
Results
Left C-T 90 0
7
8
24-h EEG recording was performed before lacosamide introduction, after a 6-month period and then after a minimum of 12 months of therapy. The difference in SWI pre- and post-lacosamide was defined as the electrographic response to lacosamide add-on treatment, and was subsequently graded as follows: Responders: reduction in SWI > 50%; Partial responders: reduction in SWI between 25 and 50%. Non responders: reduction in SWI < 25% or an increase in SWI.
0
S. Grosso et al. Bilateral C-T 92 10
1606
Lacosamide efficacy in epileptic syndromes with CSWS Valproic acid (VPA), alone or in combination with benzodiazepines, is the treatment of choice of epilepsies with CSWS (Veggiotti et al., 2012; Caraballo et al., 2013). A paradoxical reaction with worsening of seizure frequency and CSWS has been observed in patients placed under oxcarbazepine (Grosso et al., 2006), carbamazepine and phenytoin (Kramer et al., 2009). ACTH and steroids such as prednisone and deflazacort (Grosso et al., 2008) probably remain the most effective medications. However, the long-term use of corticosteroids has several side effects that limit their use for refractory patients (Grosso et al., 2008). Levetiracetam is also effective in CSWS (Capovilla et al., 2004). Lacosamide is a new anticonvulsant effective in focal epilepsy (Verrotti et al., 2013). This is the first study showing lacosamide efficacy in children with CSWS. After 6 months of lacosamide add-on therapy, 75% of patients were responder with more than 50% SWI reduction. Three of them (37%) showed 24-h EEG normalization. Almost all patients (87%) had better attention at school, were more alert and less anxious. After a minimum of 12 months of follow-up, another patient became responder (Table 2). However, two patients who had responded to lacosamide after 6 months, experienced relapse in the following months without modification of the AED regimen. Therefore, after 12 months of lacosamide add-on therapy, 67% of patients were defined as responder, including two patients with complete 24-h EEG normalization. A transitory effect of conventional AED on the CSWS pattern is a very frequent finding and outlines the need to perform long-term observations when studying the efficacy of AED in epileptic children with CSWS (Aeby et al., 2005). Lacosamide was also able to control tonic seizures and atypical absences in two of the three patients who were still experiencing seizures when the drug was placed in therapy. Although two-thirds of our patients experienced a significant improvement in alertness and behavior under lacosamide, neuropsychological functions slightly improved in only two cases. No substantial changes were observed in the remaining group of patients. Our data are in line with results of previous studies (Atkins and Nikanorova, 2011). Of course, main limitations of studies evaluating the effectiveness of medications in the treatment of CSWS are represented by the possible spontaneous recovery which may occur in some patients, the transient electrographic and clinical changes that are not necessarily related to alterations in medication, and the unpredictability of relapse (Atkins and Nikanorova, 2011). We have tried to overcome these problems by evaluating children over a minimum period of 12 months and performing 24-h sleep EEG investigations at 6-month interval after lacosamide introduction. Moreover, concomitant medications and their plasmatic levels remained unchanged during the study (data not shown). So, in our opinion the results we observed in our patients may be directly correlated to lacosamide effects. Of interest, all our patients presented with a refractory type of CSWS since more than three AEDs had already been used before lacosamide therapy. In conclusion, this study shows that lacosamide is a safe AED which may be able to improve the electroclinical impairment in over half of the CSWS patients. Although further investigation on larger series of patients are needed to confirm the present data, our observations might expand the
1607 number of new AEDs reported to be potentially effective in CSWS.
References Aeby, A., Poznanski, N., Verheulpen, D., Wetzburger, C., Van Bogaert, P., 2005. Levetiracetam efficacy in epileptic syndromes with continuous spikes and waves during slow sleep: experience in 12 cases. Epilepsia 46, 1937—1942. Atkins, M., Nikanorova, M., 2011. A prospective study of levetiracetam efficacy in epileptic syndromes with continuous spikes-waves during slow sleep. Seizure 20, 635—639. Capovilla, G., Beccaria, F., Cagdas, S., Montagnini, A., Segala, R., Paganelli, D., 2004. Efficacy of levetiracetam in pharmacoresistant continuous spikes and waves during slow sleep. Acta Neurol. Scand. 110, 144—147. Caraballo, R.H., Veggiotti, P., Kaltenmeier, M.C., Piazza, E., Gamboni, B., Avaria, M.F., Noli, D., Adi, J., Cersosimo, R., 2013. Encephalopathy with status epilepticus during sleep or continuous spikes and waves during slow sleep syndrome: a multicenter, long-term follow-up study of 117 patients. Epilepsy Res. 105, 164—173. Dalla Bernardina, B., Fontana, E., Michelizza, B., Colamaria, V., Capovilla, G., Tassinari, C.A., 1989. Partial epilepsies of childhood, bilateral synchronization, continuous spike-waves during slow sleep. In: Manelis, S., Bental, E., Loeber, J.N., Dreifuss, F.E. (Eds.), Advances in Epileptology. Raven Press, New York, pp. 295—302. Debiais, S., Tuller, L., Barthez, M.A., Monjauze, C., Khomsi, A., Praline, J., de Toffol, B., Autret, A., Barthelemy, C., Hommet, C., 2007. Epilepsy and language development: the continuous spikewaves during slow sleep syndrome. Epilepsia 48, 1104—1110. Grosso, S., Balestri, M., Di Bartolo, R.M., Corbini, L., Vatti, G., Curatolo, P., Balestri, P., 2006. Oxcarbazepine and atypical evolution of benign idiopathic focal epilepsy of childhood. Eur. J. Neurol. 13, 1142—1145. Grosso, S., Farnetani, M., Mostardini, R., Cordelli, D., Berardi, R., Balestri, P., 2008. A comparative study of hydrocortisone versus deflazacort in drug-resistant epilepsy of childhood. Epilepsy Res. 81, 80—85. Kramer, U., Sagi, L., Goldberg-Stern, H., Zelnik, N., Nissenkorn, A., Ben-Zeev, B., 2009. Clinical spectrum and medical treatment of children with electrical status epilepticus in sleep (ESES). Epilepsia 50, 1517—1524. Nickels, K., Wirrel, E., 2008. Electrical status epilepticus in sleep. Semin. Pediatr. Neurol. 15, 60. Panayiotopoulos, C.P., 2005. Epileptic encephalopathies in infancy and early childhood. In: The Epilepsies: Seizures, Syndromes, and Management. Bladon Medical Publishing, Oxford, pp. 183—189. Patry, G., Lyagoubi, S., Tassinari, C.A., 1971. Subclinical electrical status epilepticus induced by sleep in children. A clinical and electroencephalographic study of six cases. Arch. Neurol. 24, 242—252. Scheltens-de Boer, M., 2009. Guidelines for EEG in encephalopathy related to ESES/CSWS in children. Epilepsia 50 (Suppl. 7), 13—17. Tassinari, C.A., Ruboli, G., 2006. Cognition and paroxysmal EEG activities: from a single spike to electrical status epilepticus during sleep. Epilepsia 47 (Suppl. 2), S40—S43. Tassinari, C.A., Rubboli, G., Volpi, L., Billard, C., Bureau, M., 2005. Electrical status epilepticus during slow sleep, including acquired epileptic aphasia. In: Roger, J., Bureau, M., Dravet, C., Genton, P., Tassinari, C.A., Wolf, P. (Eds.), Epileptic Syndromes in Infancy, Childhood and Adolescence. , 4th ed. John Libby Eurotext, Paris, pp. 295—314.
1608 Tassinari, C.A., Cantalupo, G., Rios-Pohl, L., Della Giustina, E., Rubboli, G., 2009. Encephalopathy with status epilepticus during slow sleep: the Penelope syndrome. Epilepsia 50 (Suppl. 7), 4—8. Van Hirtum-Das, M., Licht, E.A., Koh, S., Wu, J.Y., Shields, W.D., Sankar, R., 2006. Children with ESES: variability in the syndrome. Epilepsy Res. 70 (Suppl. 1), 248—258. Veggiotti, P., Cardinali, S., Granocchio, E., Avantaggiato, P., Papalia, G., Cagnana, A., Lanzi, G., 2005. Motor impairment on awakening in a patient with an EEG pattern of unilateral, continuous spikes and waves during slow sleep. Epileptic Disord. 7, 131—136.
S. Grosso et al. Veggiotti, P., Pera, M.C., Teutonico, M.C., Brazzo, D., Ballottin, U., Tassinari, C.A., 2012. Therapy of encephalopathy with status epilepticus during sleep (ESE/CSWS syndrome): an update. Epileptic Disord. 14, 1—11. Verrotti, A., Loiacono, G., Pizzolorusso, A., Parisi, P., Bruni, O., Luchetti, A., Zamponi, N., Cappanera, S., Grosso, S., Kluger, G., Janello, C., Franzoni, E., Elia, M., Spalice, A., Coppola, G., Striano, P., Pavone, P., Savasta, S., Viri, M., Romeo, A., Aloisi, P., Gobbi, G., Ferretti, A., Cusmai, R., Curatolo, P., 2013. Lacosamide in pediatric and adult patients: comparison of efficacy and safety. Seizure 22, 210—216.
