Neurocognitive Profile and ¹⁸F-Fluorodeoxyglucose Positron Emission Tomography Brain Imaging Correlation in Children with Electrical Status Epilepticus during Sleep

Abstract

Objective Electrical status epilepticus in sleep (ESES) is defined by near-continuous epileptiform discharges during sleep along with cognitive, behavioral, and/or imaging abnormalities. We studied the neurocognitive profile and their correlation with ¹⁸F fluorodeoxyglucose positron emission tomography (FDG PET) brain abnormalities in children with ESES.

Methods Fourteen children with ESES with normal magnetic resonance imaging (MRI) from March to December 2019 were included. The intelligence quotient (IQ) and child behavior checklist (CBCL) scores were estimated using validated scales, and FDG PET brain was done at the same point of time to look for cerebral metabolic defects which was compared with a control group.

Results Fourteen patients with a mean age of 8.2 ± 2.7 years were analyzed. The average duration of epilepsy was 6 ± 2.8 years. The mean IQ was 72.4 ± 18.2 and mean CBCL score was 37.3 ± 11.8. There was negative correlation between IQ and CBCL (r = −0.55, p < 0.001). The duration of epilepsy also showed negative correlation with IQ (r = −4.75, p < 0.001). FDG PET scan showed predominant thalamic hypometabolism in 12 of 14 patients (85.7%) on visual analysis with multiple other hypometabolic cortical and subcortical regions in the brain. The quantitative analysis showed significant difference in metabolism of basal ganglion when compared with control group. The total number of hypometabolic regions seen in the brain showed moderate positive correlation with CBCL score but no significant correlation with the IQ of cases.

Conclusion This study demonstrates functional impairment of cerebral cortical, basal ganglia, and thalamic hypometabolism in a cohort of ESES patients with normal structural MRI brain study. There was a moderate correlation of extent and pattern of cerebral hypometabolism with the neuropsychological status of the child and duration of epilepsy.

Keywords

absolute asymmetry index - CBCL - CSWS - ESES - ¹⁸F FDG PET-CT - thalamic hypometabolism - Weschler's scale

Publikationsverlauf

Artikel online veröffentlicht:
27. Juni 2023

• References

• 1 Patry G, Lyagoubi S, Tassinari CA. Subclinical “electrical status epilepticus” induced by sleep in children. A clinical and electroencephalographic study of six cases. Arch Neurol 1971; 24 (03) 242-252
• 2 Galanopoulou AS, Bojko A, Lado F, Moshé SL. The spectrum of neuropsychiatric abnormalities associated with electrical status epilepticus in sleep. Brain Dev 2000; 22 (05) 279-295
• 3 Morikawa T, Seino M, Watanabe Y, Watanabe M, Yagi K. Clinical relevance of continuous spike-wave during slow-wave sleep. In: Manelis J, Bental E, Loeber JN, Dreifuss FE. eds. Advances in Epileptology. Vol. 17. New York, NY: Raven Press; 1989: 359-63
• 4 Tassinari CA, Michelucci R, Forti A. et al. The electrical status epilepticus syndrome. Epilepsy Res Suppl 1992; 6: 111-115
• 5 Tassinari CA, Rubboli G, Volpi L. et al. Encephalopathy with electrical status epilepticus during slow sleep or ESES syndrome including the acquired aphasia. Clin Neurophysiol 2000; 111 (Suppl. 02) S94-S102
• 6 Veggiotti P, Termine C, Granocchio E, Bova S, Papalia G, Lanzi G. Long-term neuropsychological follow-up and nosological considerations in five patients with continuous spikes and waves during slow sleep. Epileptic Disord 2002; 4 (04) 243-249
• 7 Morikawa T, Seino M, Watanabe M. Long-term outcome of CSWS syndrome. In: A Beaumanoir, M Bureau, T Deonna, et al, eds. Continuous Spikes and Waves during Slow Sleep. London, United Kingdom: John Libbey& Company; 1995: 27-36
• 8 Roulet Perez E, Seeck M, Mayer E, Despland PA, de Tribolet N, Deonna T. Childhood epilepsy with neuropsychological regression and continuous spike waves during sleep: epilepsy surgery in a young adult. Eur J Paediatr Neurol 1998; 2 (06) 303-311
• 9 Sánchez Fernández I, Loddenkemper T, Peters JM, Kothare SV. Electrical status epilepticus in sleep: clinical presentation and pathophysiology. Pediatr Neurol 2012; 47 (06) 390-410
• 10 Achenbach TM, Rescorla LA. Manual for the ASEBA School-Age Forms & Profiles: An Integrated System of Multi-informant Assessment. Burlington, VT: ASEBA; 2001
• 11 Kamat VV. A revision of the Binet scale for Indian children:(Kanarese and Marathi speaking). Br J Educ Psychol 1934; 4 (03) 296-309
• 12 Chen WP, Matsunari I, Noda A. et al. Rapid scanning protocol for brain (18)F-FDG PET: a validation study. J Nucl Med 2005; 46 (10) 1633-1641
• 13 Agarwal R, Kumar A, Tiwari VN, Chugani H. Thalamic abnormalities in children with continuous spike-wave during slow-wave sleep: An F-18-fluorodeoxyglucose positron emission tomography perspective. Epilepsia 2016; 57 (02) 263-271
• 14 Yilmaz S, Serdaroglu G, Akcay A, Gokben S. Clinical characteristics and outcome of children with electrical status epilepticus during slow wave sleep. J Pediatr Neurosci 2014; 9 (02) 105-109
• 15 Scholtes FB, Hendriks MP, Renier WO. Cognitive deterioration and electrical status epilepticus during slow sleep. Epilepsy Behav 2005; 6 (02) 167-173
• 16 Kelemen A, Barsi P, Gyorsok Z, Sarac J, Szűcs A, Halász P. Thalamic lesion and epilepsy with generalized seizures, ESES and spike-wave paroxysms–report of three cases. Seizure 2006; 15 (06) 454-458
• 17 Incorpora G, Pavone P, Smilari PG, Trifiletti R, Parano E. Late primary unilateral thalamic hemorrhage in infancy: report of two cases. Neuropediatrics 1999; 30 (05) 264-267
• 18 Monteiro JP, Roulet-Perez E, Davidoff V, Deonna T. Primary neonatal thalamic haemorrhage and epilepsy with continuous spike-wave during sleep: a longitudinal follow-up of a possible significant relation. Eur J Paediatr Neurol 2001; 5 (01) 41-47
• 19 Guzzetta F, Battaglia D, Veredice C. et al. Early thalamic injury associated with epilepsy and continuous spike-wave during slow sleep. Epilepsia 2005; 46 (06) 889-900
• 20 De Tiège X, Goldman S, Laureys S. et al. Regional cerebral glucose metabolism in epilepsies with continuous spikes and waves during sleep. Neurology 2004; 63 (05) 853-857
• 21 Aghakhani Y, Kobayashi E, Bagshaw AP. et al. Cortical and thalamic fMRI responses in partial epilepsy with focal and bilateral synchronous spikes. Clin Neurophysiol 2006; 117 (01) 177-191
• 22 Greene DJ, Marek S, Gordon EM. et al. Integrative and network-specific connectivity of the basal ganglia and thalamus defined in individuals. Neuron 2020; 105 (04) 742-758.e6
• 23 Afifi AK. The basal ganglia: a neural network with more than motor function. Semin Pediatr Neurol 2003; 10 (01) 3-10