Seizure 23 (2014) 155–157

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Seizure semiology and electroencephalography in young children with lesional temporal lobe epilepsy Rui-Juan Lv a,1, Zhen-Rong Sun b,1, Tao Cui a, Xiao-Qiu Shao a,* a b

Department of Neurology, Beijing Tiantan Hospital Affiliated to Capital Medical University, 100050 Beijing, PR China Department of Neurosurgery, Beijing Tiantan Hospital Affiliated to Capital Medical University, 100050 Beijing, PR China

A R T I C L E I N F O

A B S T R A C T

Article history: Received 27 June 2013 Received in revised form 9 October 2013 Accepted 6 November 2013

Purpose: This study aimed to discuss the clinical features of seizure semiology and electroencephalography (EEG) in young children with lesional temporal lobe epilepsy (TLE). Method: Children with lesional TLE received presurgical evaluation for intractable epilepsy. They were followed up for more than one year after temporal lobectomy. We reviewed the medical history and video-EEG monitoring of children with TLE to analyze the semiology of seizures and EEG findings and compared the semiology of seizures and EEG findings of childhood TLE and adult TLE. Results: A total of 84 seizures were analyzed in 11 children (aged 23–108 months). The age of seizure onset was from 1 month to 26 months (a mean of 17.6 months). All of the patients exhibited prominent motor manifestations including epileptic spasm, tonic seizure, and unilateral clonic seizure. Seven children manifested behavioral arrest similar to an automotor seizure in adult TLE but with a shorter duration and higher frequency. The automatisms were typically orofacial, whereas manual automatisms were rarely observed. The EEG recordings revealed that diffuse discharge patterns were more common in younger children, whereas focal or unilateral patterns were more typical in older children. All of the patients were seizure-free after temporal lobectomy with more than one-year follow-up. All of the children had a mental development delay or regression; however, there was improvement after surgery, especially in those with surgery performed early. Conclusion: In contrast to TLE in adults, young children with lesional TLE probably represent a distinct nosological and probably less homogeneous syndrome. Although they had generalized clinical and electrographic features, resective epilepsy surgery should be considered as early as possible to obtain seizure control and improvement in mental development. ß 2013 British Epilepsy Association. Published by Elsevier Ltd. All rights reserved.

Keywords: Seizure semiology EEG Young children Lesional temporal lobe epilepsy

1. Introduction Epilepsy is characterized as recurrent paroxysmal episodes of brain dysfunction manifested by stereotyped alterations in behavior and electroencephalogram (EEG) results. Seizure semiology describes the clinical features of such stereotyped behavior alterations supporting the precise classification of seizures. Knowledge of seizure semiology can facilitate developing an accurate classification of seizures and localize the region of the brain involved in a specific seizure.1 The development of presurgical evaluation, particularly with long term video-EEG monitoring, has increased the understanding of seizure semiology.

* Corresponding author at: Department of Neurology, Beijing Tiantan Hospital affiliated to Capital Medical University, 6 Tiantan Xi Li, Dongcheng District, Beijing 100050, PR China. Tel.: +86 10 67098366; fax: +86 10 67098322. E-mail address: [email protected] (X.-Q. Shao). 1 These authors contributed equally to the present work.

Temporal lobe epilepsy (TLE) is the most common symptomatic localization-related epileptic syndrome; it is resistant to antiepileptic drugs (AEDs) in approximately two-thirds of cases. For medically refractory patients, temporal lobectomy offers a very good possibility for freedom from seizures.2 The key for success from surgery depends on the exact localization of the epileptogenic zone, based on converging evidence from different diagnostic tools including seizure semiology, EEG, magnetic resonance imaging (MRI), positron emission tomography (PET), single proton emission computed tomography (SPECT) and neuropsychology. Recently, the role of seizure semiology in the exact localization of the epileptogenic zone is receiving increasing attention by facilitating the diagnostic process.3 Some authors have described significant differences between adult TLE and childhood TLE semiologies,3–5 but those studies that examined TLE in infants and children were relatively few. The complex semiological patterns of TLE in children cause the clinical diagnosis to be very difficult. Children with TLE frequently do not have evidence of electrographic interictal and ictal focuses in the

1059-1311/$ – see front matter ß 2013 British Epilepsy Association. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.seizure.2013.11.004

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temporal region, and it is difficult to localize the epileptogenic zone exactly. This study aimed to examine the features of seizure semiology and EEG in children with unilateral lesional TLE for whom surgery was successful, which can provide the foundation for diagnosing TLE in children in the future. 2. Patients and methods 2.1. Patients All of the patients had daily seizures despite treatment with appropriate and adequate AEDs. Eleven children with temporal lobe lesions (aged 23–108 months at surgery; a mean of 50.5 months) received presurgical evaluations for intractable epilepsy in our Comprehensive Epilepsy Center from October 2008 to March 2011. The age of seizure onset was less than 3 years. All of the patients were seizure-free after a temporal lobectomy with more than one year follow-up (a range of 1–3 years, a mean of 2 years). Informed consent was obtained from each subject enrolled, and the study was reviewed and approved by the local ethics committee in accordance with the Declaration of Helsinki. 2.2. Seizure and EEG recording Time-labeled video recordings were reviewed by three independent investigators blind to the ictal EEG. We excluded those seizures in which the recording quality did not permit analysis of the complete seizure. The patients were monitored for 24–72 h day and night in waking and sleeping states, and at least three seizures of each type were captured during the monitoring period. The subjects were examined during the seizures by specifically trained EEG technicians to assess the level of consciousness with responses to verbal or nonverbal external stimuli. Each seizure was analyzed independently with regard to the motor, sensory, consciousness, and autonomic spheres of seizure, as well as the manifestations in the postictal period. The data were documented on a specifically designed data sheet including the following seizure components: tonic, myoclonic, clonic, epileptic spasm, hypermotor, hypomotor, and automotor seizures.6 All of the cases were reviewed and classified by the senior investigator (X-Q Shao). We reviewed the medical history and video-EEG results and collected the most important clinical data to analyze the

semiology of seizures and EEG findings to compare with those of adult TLE. 3. Results A total of 84 seizures were recorded and analyzed in 11 children (three girls and eight boys). The age of seizure onset was from 1 month to 26 months (a mean of 17.6 months). All of the patients exhibited prominent motor manifestations, including epileptic spasm, tonic seizure (symmetric or asymmetric), and unilateral clonic seizure. Seven children manifested behavioral arrests similar to automotor seizure in adult TLE, but with shorter duration (several seconds to twenty seconds) and greater frequency. The automatisms were typically orofacial, whereas manual automatisms were rarely observed. Tonic seizures often occurred during sleep, whereas behavioral arrest commonly appeared during wakefulness. Spasm seizures almost always occurred during wakefulness, except in one patient (No. 4). This patient manifested an asymmetric tonic posture seizure during sleep, followed by a cluster of epileptic spasms. The interictal EEG recordings of our patients revealed that multifocal or diffuse high voltage slow wave intermingled with spikes was the most common finding in the waking state. In younger children, this pattern appeared more diffuse, whereas it was more focal or unilaterally consistent with the side of the lesion in older children. There were no typical hypsarrhythmias in our patients during the EEG monitoring in our hospital; however, the EEG results of four young children presented as a brief burst pattern with a high voltage slow wave mixed with a spike or a polyspike in the sleep recordings, which was synchronous or asynchronous. The ictal EEG findings were different depending on the seizure type. The partial seizures frequently appeared as a regional or unilateral slow wave or as fast activities at the onset. The ictal EEG of epileptic spasms typically showed a highamplitude slow wave transient followed by generalized voltage attenuation. The histopathology of the resected tissue showed a benign tumor, focal cortical dysplasia (FCD), malformations of cortical development and tuberous sclerosis. Malformations of cortical development, low-grade neoplasms, and tuberous sclerosis were much more frequent in these children. All of the children had a mental developmental delay or regression; however, the parents of the children reported improvement after surgery, especially in the children with early operations. The details were seen in Table 1.

Table 1 Clinical and semiology features of 11 children with lesional temporal lobe epilepsy. Patient number

Sex

Age at surgery (m)

Age at epilepsy onset (m)

Localizatio

Etiology

Seizure type (duration, frequency)

Possible lateralizing signs

Behavioral arrest (10 s, dozens/d), asymmetric tonic seizure (20-30 s, 3–5/d) Asymmetric posture seizure (10-20 s, 2–4/d) Spasm after behavioral arrest (10-20 s, dozens/d) Atypical absence(10 s, 1 m–1), spasm followed by asymmetric posture seizure (10-20 s, 3–4/d) Spasm (2-5 s, more than twenty clusters/d) Spasm-oral automatism (10-20 s, dozens/d) Staring-oral automatism (10-15 s, 3–5/d) Atypical absence with oral automatism(10-15 s, 3–4/d), asymmetric posture seizure(20 s, 2–3/d) Myoclonic seizure (2-3 s, 4–5/d), asymmetric tonic seizure (10-20 s, 2–3/d) Right limbs twitching (30 s, 3–5/month), atypical absence with left eye blinking (10 s, 2–5/d) Spasm (3-5 s, dozens/d)

Dystonia RH

1

F

48

26

Left mesial

Tumor

2 3 4

F M M

108 26 28

12 12 4

Left mesial + lateral R lateral R mesial

FCD DNT Ganglioglioma

5 6 7 8

M M M M

48 47 60 63

1 26 8 15

L mesial + lateral Left mesial R mesial + lateral L posterior temporal

Malformation FCD Tumor TS

9

M

132

48

R mesial

Tumor

10

M

72

24

L mesial + lateral

Macrogyria

11

F

23

11

L mesial + lateral

Cortical malformation

Dystonia RH No Dystonia LH No No No Dystonia RH

Dystonia LH Right limbs twitching No

Note. m, month; F, female; M, male; R, right; L, left; s, second; d, day; FCD, focal cortical dysplasia; H, hand; TS, tuberous sclerosis; DNT, dysembryoplastic neuroepithelial tumor.

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4. Discussion and conclusion TLE in children has been less well studied than TLE in adults. This study showed that the clinical symptoms and EEG patterns in children with TLE were different from those in adults.5 TLE in very young children might exhibit prominent motor manifestations including epileptic spasm, tonic seizure, and unilateral clonic seizure, which are reminiscent of extra-temporal seizures. These motor manifestations decreased with increasing age and were less common in adults.7 The finding that epilepsies in infants and young children had a limited repertoire of ictal manifestations were similar to the results of a previous study.8 In young children with TLE, the automatisms were typically orofacial, whereas manual automatisms were rarely observed. The automatisms became increasingly complex and discrete with age. Whereas only simple automatisms such as oroalimentary, gestural and blinking automatisms were observed in preschool children, more complex automatisms such as hand clapping, beating hands on a blanket or card shuffling were only observed in children older than eight years.9 The EEG recording in this study revealed that diffuse discharge patterns were more common in younger children, whereas focal or unilateral patterns were more prominent in older children. Although there were no typical hypsarrhythmias in these children, the EEG of four young children presented as a brief burst pattern with a high voltage slow wave mixed with a spike or a polyspike in the recordings during sleep, which was similar to the pattern of fragmented hypsarrhythmia;10 these children were seizure free after the temporal lobectomy. Although the presence of hypsarrhythmias depended on the age at which the EEG was performed, several papers reported that the infants with clusters of epileptic spasms without hypsarrhythmias at onset or throughout the clinical course were typically drug resistant and the epilepsies were related to FCD.11,12 Recognizing the presentations of patients with partial epilepsy who initially demonstrate a nonpartial ictal semiology and EEG pattern is very important because judging the classification of epilepsy based on the initial seizure type could easily result in a misdiagnosis of generalized epilepsy. This has profound implications for presurgical evaluation because epilepsy surgery might render these ‘‘non-surgical candidates’’ seizure-free. The seizure semiology of lesional TLE in young children is an expression of late limbic system maturation as well as rapid and extensive subcortical extratemporal activation.13 The clinical phenomenology of seizures in young children is generated by widespread immature neuronal matrices that are just beginning to become strengthened through repeated use.14 In immature neural matrices, the epileptic electrical activity appears to evolve according to patterns of propagation distinct from those observed during adulthood.6,13 The differences in propagation patterns appear to be influential in the clinical course of complex motor seizures and EEG manifestations in children. It is hypothesized that limbic system immaturity in children leads to the differences in temporal lobe seizure semiology and EEG manifestation between children and adults. This study supported that malformations of cortical development, low-grade neoplasms, and tuberous sclerosis were markedly more frequent in children, whereas hippocampal sclerosis was the most common etiology in adult TLE. The term catastrophic epilepsy describes the clinical picture of severe, intractable epilepsy in infancy or in the early childhood, typically with daily seizures and developmental stagnation or regression.15 Catastrophic epilepsy may be found not only in

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generalized epileptic encephalopathies such as West syndrome and Lennox–Gastaut syndrome but also in extratemporal lobe focal epilepsies frequently caused by cortical development malformations.16 In this study, a group of young children with refractory lesional TLE had cognitive stagnation or regression and frequent seizures with etiologies primarily of cortical development malformations, conforming to the diagnosis of catastrophic epilepsy. All of the patients obtained very good seizure outcomes after resective surgery. Young children with refractory lesional TLE presenting with the clinical and electrographic picture described in this study should not be discouraged from possible epilepsy surgery because surgery at as early an age as possible can result in seizure control and improvement of mental development. There were significant differences between young children and adults with TLE regarding seizure semiology, EEG patterns and etiologies. In contrast to adults with lesional TLE, young children with lesional TLE probably represent a distinct nosological and probably less homogeneous syndrome, which merits our full clinical attention. Although these children with lesional TLE had generalized clinical and electrographic features, a resective epilepsy surgery should be considered as early as possible to obtain seizure control and improvement of mental development. Acknowledgments This work was supported by the Natural Science Foundation of China grant 81301119 and a grant from the Youth Foundation of Beijing Tiantan Hospital KY2011-14. References 1. Fogarasi A. Seizure Semiology of Infants and Young Childeren with Lesional Epilepsy. Ph.D. Thesis 2002. 2. Engel Jr J, Wiebe S, French J, Sperling M, Williamson P, Spencer D, et al. Practice parameter: temporal lobe and localized neocortical resections for epilepsy: report of the Quality Standards Subcommittee of the American Academy of Neurology, in association with the American Epilepsy Society and the American Association of Neurological Surgeons. Neurology 2003;60:538–47. 3. Vendrame M, Zarowski M, Alexopoulos AV, Wyllie E, Kothare SV, Loddenkemper T. Localization of pediatric seizure semiology. Clin Neurophysiol 2011; 122:1924–8. 4. Fogarasi A, Tuxhorn I, Janszky J, Janszky I, Rasonyi G, Kelemen A, et al. Agedependent seizure semiology in temporal lobe epilepsy. Epilepsia 2007;48: 1697–702. 5. Rodriguez AJ, Buechler RD, Lahr BD, So EL. Temporal lobe seizure semiology during wakefulness and sleep. Epilepsy Res 2007;74:211–4. 6. Fogarasi A, Jokeit H, Faveret E, Janszky J, Tuxhorn I. The effect of age on seizure semiology in childhood temporal lobe epilepsy. Epilepsia 2002;43:638–43. 7. Ray A, Kotagal P. Temporal lobe epilepsy in children: overview of clinical semiology. Epileptic Disord 2005;7:299–307. 8. Acharya JN, Wyllie E, Luders HO, Kotagal P, Lancman M, Coelho M. Seizure symptomatology in infants with localization-related epilepsy. Neurology 1997;48:189–96. 9. Brockhaus A, Elger CE. Complex partial seizures of temporal lobe origin in children of different age groups. Epilepsia 1995;36:1173–81. ´phalopathie myoclonique 10. Gastaut H, Roger J, Soulayrol R, Pinsard N. L’ence infantile avec hypsarythmie (syndrome de West). Paris: Masson; 1964. 11. Caraballo RH, Ruggieri V, Gonzalez G, Cersosimo R, Gamboni B, Rey A, et al. Infantile spams without hypsarrhythmia: a study of 16 cases. Seizure 2011;20: 197–202. 12. Caraballo RH, Fejerman N, Bernardina BD, Ruggieri V, Cersosimo R, Medina C, et al. Epileptic spasms in clusters without hypsarrhythmia in infancy. Epileptic Disord 2003;5:109–13. 13. Holmes GL. Epilepsy in the developing brain: lessons from the laboratory and clinic. Epilepsia 1997;38:12–30. 14. Gloor P. Experiential phenomena of temporal lobe epilepsy. Facts and hypotheses. Brain 1990;113(Pt (6)):1673–94. 15. Gennaro G, Sparano A, Mascia A, Sebastiano F, Esposito V, Quarato P. Catastrophic childhood temporal lobe epilepsy. J Neurolog Sci (Turkish) 2005;22: 314–8. 16. Wyllie E, Comair YG, Kotagal P, Bulacio J, Bingaman W, Ruggieri P. Seizure outcome after epilepsy surgery in children and adolescents. Ann Neurol 1998;44:740–8.