Cognitive functioning in children with self‐limited epilepsy with centrotemporal spikes: A systematic review and meta‐analysis

Wickens, Steven; Bowden, Stephen C.; D’Souza, Wendyl

doi:10.1111/epi.13865

Cited by 110 publications

(99 citation statements)

References 84 publications

(201 reference statements)

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“…These findings suggest that the abnormalities in cortical rhythms observed are not discretely tied to the focal epileptiform spikes characteristic of this disease. Rather, consistent with recent observations that BECTS is a complex neuropsychiatric disease involving broad neurocognitive dysfunctions beyond the observed clinical seizures (Wickens et al, ), we observe that BECTS rhythm abnormalities may be diffuse, involving multiple cortical regions. We note that we did not find a direct relationship between full scale IQ and global beta power or sensorimotor performance and peri‐rolandic beta power.…”

Section: Discussionsupporting

confidence: 92%

“…Patients were required to have a clinical diagnosis of BECTS by a board‐certified child neurologist following 1989 ILAE criteria (Commission on Classification & Terminology of the International League Against Epilepsy, ), a history of at least two clinical seizures characterized by focal facial motor activity or secondary generalized tonic clonic activity, and an EEG that showed sleep activated centrotemporal spikes. Children with attentional disorders and mild learning difficulties were included as these findings are consistent with the known cognitive deficits in BECTS (Wickens, Bowden, & D'Souza, ). Medication history, neurodevelopmental comorbidities, current medication status, and the month of the most recent seizure were recorded at the time of the EEG visit.…”

Section: Methodsmentioning

confidence: 99%

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Beta oscillations in the sensorimotor cortex correlate with disease and remission in benign epilepsy with centrotemporal spikes

et al. 2019

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Introduction Benign epilepsy with centrotemporal spikes (BECTS) is a common form of childhood epilepsy with the majority of those afflicted remitting during their early teenage years. Seizures arise from the lower half of the sensorimotor cortex of the brain (e.g. seizure onset zone) and the abnormal epileptiform discharges observed increase during NREM sleep. To date no clinical factors reliably predict disease course, making determination of ongoing seizure risk a significant challenge. Prior work in BECTS have shown abnormalities in beta band (14.9–30 Hz) oscillations during movement and rest. Oscillations in this frequency band are modulated by state of consciousness and thought to reflect intrinsic inhibitory mechanisms. Methods We used high density EEG and source localization techniques to examine beta band activity in the seizure onset zone (sensorimotor cortex) in a prospective cohort of children with BECTS and healthy controls during sleep. We hypothesized that beta power in the sensorimotor cortex would be different between patients and healthy controls, and that beta abnormalities would improve with resolution of disease in this self‐limited epilepsy syndrome. We further explored the specificity of our findings and correlation with clinical features. Statistical testing was performed using logistic and standard linear regression models. Results We found that beta band power in the seizure onset zone is different between healthy controls and BECTS patients. We also found that a longer duration of time spent seizure‐free (corresponding to disease remission) correlates with lower beta power in the seizure onset zone. Exploratory spatial analysis suggests this effect is not restricted to the sensorimotor cortex. Exploratory frequency analysis suggests that this phenomenon is also observed in alpha and gamma range activity. We found no relationship between beta power and the presence or rate of epileptiform discharges in the sensorimotor cortex or a test of sensorimotor performance. Conclusion These results provide evidence that cortical beta power in the seizure onset zone may provide a dynamic physiological biomarker of disease in BECTS.

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Section: Discussionsupporting

confidence: 92%

Section: Methodsmentioning

confidence: 99%

Beta oscillations in the sensorimotor cortex correlate with disease and remission in benign epilepsy with centrotemporal spikes

et al. 2019

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“…25 In addition, we added tests of intelligence 34 and executive function, 35 based on reports of compromise in BECTS. 5 These test scores were standardized according to age-based norms. Details of the tests and targeted cognitive domains are presented in Table 2.…”

Section: Neuropsychological Assessmentmentioning

confidence: 99%

“…12 In addition, both white matter and functional discrepancies have been reported, comprising lower fractional anisotropy in left inferior frontal and supramarginal regions, and lower functional connectivity between left sensorimotor and right inferior frontal gyrus, respectively. 13,14 Similarly, although interest has been longstanding in regard to the complications of language-based abilities in children with BECTS, [15][16][17] cognitive complications of BECTS have been reported in diverse areas of mentation compared to age-matched control peers, 8,15,18,19 including not only language-related skills but intelligence, memory, attention, and executive function (for reviews, see Wickens et al, 5,20 Pal et al 20 ). Importantly, cognitive and magnetic resonance (MR) abnormalities have been reported in new onset cases as well, with the nature and range of anomalies varying across studies, [21][22][23][24] attesting that these abnormalities are not necessarily secondary to the effects of epilepsy chronicity and medication treatment.…”

Section: Introductionmentioning

confidence: 99%

Network analysis of prospective brain development in youth with benign epilepsy with centrotemporal spikes and its relationship to cognition

et al. 2019

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Objective Benign epilepsy with centrotemporal spikes (BECTS) is the most common childhood idiopathic localization‐related epilepsy syndrome. BECTS presents normal routine magnetic resonance imaging (MRI); however, quantitative analytic techniques have captured subtle cortical and subcortical magnetic resonance anomalies. Network science, including graph theory (GT) analyses, facilitates understanding of brain covariance patterns, potentially informing in important ways how this common self‐limiting epilepsy syndrome may impact normal patterns of brain and cognitive development. Methods GT analyses examined the developmental covariance among cortical and subcortical regions in children with new/recent onset BECTS (n = 19) and typically developing healthy controls (n = 22) who underwent high‐resolution MRI and cognitive assessment at baseline and 2 years later. Global (transitivity, global efficiency, and modularity index [Q]) and regional measures (local efficiency and hubs) were investigated to characterize network development in each group. Associations between baseline‐based GT measures and cognition at both time points addressed the implications of GT analyses for cognition and prospective cognitive development. Furthermore, an individual contribution measure was investigated, reflecting how important for cognition it is for BECTS to resemble the correlation matrices of controls. Results Groups exhibited similar Q and overall network configuration, with BECTS presenting significantly higher transitivity and both global and local efficiency. Furthermore, both groups presented a similar number of hubs, with BECTS showing a higher number in temporal lobe regions compared to controls. The investigated measures were negatively associated with 2‐year cognitive outcomes in BECTS. Significance Children with BECTS present a higher‐than‐normal global developmental configuration compared to controls, along with divergence from normality in terms of regional configuration. Baseline GT measures demonstrate potential as a cognitive biomarker to predict cognitive outcome in BECTS 2 years after diagnosis. Similarities and differences in developmental network configurations and their implications for cognition and behavior across common epilepsy syndromes are of theoretical interest and clinical relevance.

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“…Although children with CECTS usually have IQ scores within the typical range, more specific neuropsychological testing has revealed deficits in attention, processing speed, working memory, and inhibitory control compared both to healthy individuals and to children with other types of epilepsy . These processes are all components of executive function.…”

Section: Functional Network In Cectsmentioning

confidence: 99%

The epileptic network and cognition: What functional connectivity is teaching us about the childhood epilepsies

2019

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Our objective was to summarize and evaluate the rapidly expanding body of literature studying functional connectivity in childhood epilepsy. In the self‐limited childhood epilepsies, awareness of cognitive comorbidities has been steadily increasing, and recent advances in our understanding of the network effects of these disorders promise insights into the underlying neurobiology. We reviewed publications addressing functional connectivity in children with epilepsy with an emphasis on studies of children with self‐limited childhood epilepsies. The majority of studies have been published in the past 10 years and predominantly examine childhood epilepsy with centrotemporal spikes and childhood absence epilepsy. Cognitive network alterations are commonly observed across the childhood epilepsies. Some of these effects appear to be nonspecific to epilepsy syndrome or even to category of neurological disorder. Other patterns, such as changes in the connectivity of cortical language areas in childhood epilepsy with centrotemporal spikes, provide clues to the underlying cognitive deficits seen in affected children. The literature to date is dominated by general observations of connectivity patterns without a priori hypotheses. These data‐driven studies build an important foundation for hypothesis generation and are already providing useful insights into the neuropathology of the childhood epilepsies. Future work should emphasize hypothesis‐driven approaches and rigorous clinical correlations to better understand how the knowledge of network alterations can be applied to guidance and treatment for the children in our clinics.

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Cognitive functioning in children with self‐limited epilepsy with centrotemporal spikes: A systematic review and meta‐analysis

Abstract: The results of the present meta-analysis provide the first clear evidence that children with ECTS display a profile of pervasive cognitive difficulties and thus challenge current conceptions of ECTS as a benign disease or of limited specific or localized cognitive effect.

Cited by 110 publications

References 84 publications

Beta oscillations in the sensorimotor cortex correlate with disease and remission in benign epilepsy with centrotemporal spikes

Beta oscillations in the sensorimotor cortex correlate with disease and remission in benign epilepsy with centrotemporal spikes

Network analysis of prospective brain development in youth with benign epilepsy with centrotemporal spikes and its relationship to cognition

The epileptic network and cognition: What functional connectivity is teaching us about the childhood epilepsies

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