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Dominant harmonic pattern as an ictal marker of the epileptogenic zone in focal neocortical epilepsy

Ye, L.; Hu, L.; Ye, H.; Chen, Y.; Zhu, J.; Zheng, Z.; Jiang, H.; Yang, D.; Chen, C.; Wang, S.; Wang, Z.; Ming, W.; Wang, Y.; Xu, C.; Wang, J.; Ding, M.; Wang, S.

2024-09-26 neurology
10.1101/2024.09.25.24314351 medRxiv
Show abstract

ObjectiveThe ictal Harmonic pattern (H pattern), produced by the non-linear characteristics of EEG waveforms, may hold significant potential for localizing the epileptogenic zone (EZ) in focal epilepsy. However, further validation is needed to establish the H patterns effectiveness as a biomarker for measuring the EZ. MethodsWe retrospectively enrolled 131 patients diagnosed with drug-resistant focal epilepsy, all of whom had complete stereo-electroencephalographic (SEEG) data. From this cohort, we selected 85 patients for outcome analysis. We analyzed the morphological and time-frequency (TF) features of the H pattern using TF plots. A third quartile (Q3) threshold was applied to classify channels expressing either dominant (ChanneldH pattern) or non-dominant H patterns (Channelnon-dH pattern). We then examined associations between the morphological features of the H pattern and patients clinical characteristics, as well as the correlations between the extent of channel removal and seizure outcomes. ResultsWe found no significant correlations between the morphological features of the ictal H pattern and clinical factors, including lesional MRI findings, epileptic onset patterns, epilepsy type, pathology, or surgical outcomes. The non-localizable H pattern appeared exclusively in patients with non-focal onset patterns. Notably, the proportion of ChanneldH pattern was higher in the seizure-onset zone (SOZ) compared to the early propagation zone. The seizure-free group demonstrated significantly higher removal proportions of ChanneldH pattern, both within and outside the SOZ (p = 0.014; p = 0.036), with AUCs of 0.606 and 0.660, respectively, in a seizure freedom prediction model. Survival analysis confirmed that complete removal of these regions correlated with long-term seizure freedom (p = 0.008; p = 0.028). Further subgroup analysis showed a significant correlation in neocortical epilepsy (p = 0.0004; p = 0.011), but not in mesial temporal lobe epilepsy. Additionally, multivariate analysis identified the complete removal of ChanneldH pattern as the only independent predictor for seizure freedom (p = 0.022; OR 6.035, 95% CI 1.291-28.211). ConclusionsOur study supports the notion that the dominance of the ictal H pattern, regardless of its morphology, serves as a novel biomarker for the EZ in focal epilepsy. The non-linearity in EEG waveforms provides new insights into understanding ictal spreading propagation and offers potential improvements for surgical planning in neocortical epilepsy.

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