Scalp EEG high frequency oscillations as a biomarker of treatment response in epileptic encephalopathy with continuous spike-and-wave during sleep (CSWS)

Cao, Dezhi; Chen, Yan; Liao, Jianxiang; Nariai, Hiroki; Li, Lin; Zhu, Yuhe; Zhao, Xia; Hu, Yanrong; Wen, Feiqiu; Zhai, Qixiao

doi:10.1016/j.seizure.2019.05.023

Cited by 25 publications

(28 citation statements)

References 45 publications

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“…After the successful treatments (medications or surgery), the HFO-related values decreased. Such findings were consistent with the prior studies showing active epilepsy correlated with the presence of scalp EEG HFOs in infantile spasms (Kobayashi et al, 2015), benign Rolandic epilepsy (Kobayashi et al, 2011;van Klink et al, 2016), and epilepsy with continuous spikes and waves during slow-wave sleep (CSWS) (Cao et al, 2019;Kobayashi et al, 2010).…”

Section: Discussionsupporting

confidence: 92%

“…Recent studies have shown EEG fast activities can be recorded non-invasively from the scalp recordings (Andrade-Valenca et al, 2011;Bernardo et al, 2018;Kobayashi et al, 2004;Kobayashi et al, 2015;Kramer et al, 2019;Nariai et al, 2017;Nariai et al, 2018;Pizzo et al, 2016;Wu et al, 2008). Scalp EEG HFOs have the potential to localize seizure onset zones (Andrade-Valenca et al, 2011;Bernardo et al, 2018;Nariai et al, 2017;Tamilia et al, 2020), and to monitor disease activity in epileptic spasms (Kobayashi et al, 2015), Rolandic epilepsy (Kobayashi et al, 2011;van Klink et al, 2016), and epileptic encephalopathy with continuous spike-and-wave during sleep (CSWS) (Cao et al, 2019;Kobayashi et al, 2010). Additionally, HFOs coupled with slow-wave activity strongly localize to epileptic brain regions in children with infantile spasms and other types of focal epilepsy in invasive monitoring (Iimura et al, 2018;Motoi et al, 2018;Nonoda et al, 2016;Song et al, 2017;Weiss et al, 2016) and may reflect disease activity in scalp EEG in epileptic spasms (Bernardo et al, 2020.…”

Section: Introductionmentioning

confidence: 99%

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Scalp EEG interictal high frequency oscillations as an objective EEG biomarker of infantile spasms

Nariai¹,

Hussain²,

Bernardo

et al. 2020

Preprint

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Objective: To investigate the diagnostic utility of high frequency oscillations (HFOs) via scalp electroencephalogram (EEG) in infantile spasms. Methods:We retrospectively analyzed interictal slow-wave sleep EEGs sampled at 2,000 Hz recorded from 30 consecutive patients who were suspected of having infantile spasms. We measured the rate of HFOs (80-500 Hz) and the strength of the cross-frequency coupling between HFOs and slow-wave activity (SWA) at 3-4 Hz and 0.5-1 Hz as quantified with modulation indices (MIs).Results: Twenty-three patients (77%) exhibited active spasms during the overnight EEG recording.Although the HFOs were detected in all children, increased HFO rate and MIs correlated with the presence of active spasms (p < 0.001 by HFO rate; p < 0.01 by MIs at 3-4 Hz; p = 0.02 by MIs at 0.5-1 Hz). The presence of active spasms was predicted by the logistic regression models incorporating HFOrelated metrics (AUC: 0.80-0.98) better than that incorporating hypsarrhythmia (AUC: 0.61). The predictive performance of the best model remained favorable (87.5% accuracy) after a cross-validation procedure.Conclusions: Increased rate of HFOs and coupling between HFOs and SWA are associated with active epileptic spasms.Significance: Scalp-recorded HFOs may serve as an objective EEG biomarker for active epileptic spasms.

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Section: Discussionsupporting

confidence: 92%

Section: Introductionmentioning

confidence: 99%

Scalp EEG interictal high frequency oscillations as an objective EEG biomarker of infantile spasms

Nariai¹,

Hussain²,

Bernardo

et al. 2020

Preprint

Self Cite

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“…Dezhi et al studied HFOs in 22 children with persistent spike-wave encephalopathy during sleep who received methylprednisolone treatment. HFOs disappeared from scalp EEG in children treated with hormones, but children with no response or recurrence after hormone therapy showed persistent HFOs ( Cao et al, 2019 ). In the study, the interaction of curative efficacy × frequency and the interaction of curative efficacy × state are statistically significant.…”

Section: Discussionmentioning

confidence: 99%

Application of High-Frequency Oscillations on Scalp EEG in Infant Spasm: A Prospective Controlled Study

Yan

Chen

et al. 2021

Front. Hum. Neurosci.

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ObjectiveWe quantitatively analyzed high-frequency oscillations (HFOs) using scalp electroencephalography (EEG) in patients with infantile spasms (IS).MethodsWe enrolled 60 children with IS hospitalized from January 2019 to August 2020. Sixty healthy age-matched children comprised the control group. Time–frequency analysis was used to quantify γ, ripple, and fast ripple (FR) oscillation energy changes.Resultsγ, ripple, and FR oscillations dominated in the temporal and frontal lobes. The average HFO energy of the sleep stage is lower than that of the wake stage in the same frequency bands in both the normal control (NC) and IS groups (P < 0.05). The average HFO energy of the IS group was significantly higher than that of the NC group in γ band during sleep stage (P < 0.01). The average HFO energy of S and Post-S stage were higher than that of sleep stage in γ band (P < 0.05). In the ripple band, the average HFO energy of Pre-S, S, and Post-S stage was higher than that of sleep stage (P < 0.05). Before treatment, there was no significant difference in BASED score between the effective and ineffective groups. The interaction of curative efficacy × frequency and the interaction of curative efficacy × state are statistically significant. The average HFO energy of the effective group was lower than that of the ineffective group in the sleep stage (P < 0.05). For the 16 children deemed “effective” in the IS group, the average HFO energy of three frequency bands was not significantly different before compared with after treatment.SignificanceScalp EEG can record HFOs. The energy of HFOs can distinguish physiological HFOs from pathological ones more accurately than frequency. On scalp EEG, γ oscillations can better detect susceptibility to epilepsy than ripple and FR oscillations. HFOs can trigger spasms. The analysis of average HFO energy can be used as a predictor of the effectiveness of epilepsy treatment.

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“…[21][22][23] At present, most research on scalp HFOs has only analyzed ripple band. Recently, some studies have applied scalp HFOs to locate epilepsy generators [24][25][26][27] and to mirror disease activity and treatment response, 23,28 as well as to differentiate distinct disease entities. 29 Nariai et al investigated the diagnostic utility of scalp HFO in IS, 30 and found that increased rate of HFOs and coupling between HFOs and slow-wave activity (SWA) are associated with active epileptic spasms.…”

Section: Introductionmentioning

confidence: 99%

Automatic detection of interictal ripples on scalp EEG to evaluate the effect and prognosis of ACTH therapy in patients with infantile spasms

Wang

Yan

et al. 2021

Epilepsia

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Objective We aimed to explore the feasibility of using scalp‐recorded high‐frequency oscillations (HFOs) to evaluate the efficacy and prognosis of adrenocorticotropic hormone (ACTH) treatment in patients with infantile spasms. Methods Thirty‐nine children with infantile spasms were enrolled and divided into seizure‐free and non–seizure‐free groups after ACTH treatment. Patients who were seizure‐free were further divided into relapse and non‐relapse subgroups based on the observations made during a 6‐month follow‐up period. Scalp ripples were detected and compared during the interictal periods before and after 2 weeks of treatment. Results After ACTH treatment, the number and channels of ripples were significantly lower, whereas the percentage decrease in the number, spectral power, and channels of ripples was significantly higher in the seizure‐free group than in the non–seizure‐free group. In addition, the relapse subgroup showed higher number and spectral power and wider distribution of ripples than did the non‐relapse subgroup. Changes in HFOs in terms of number, spectral power, and channel of ripples were closely related to the severity of epilepsy and can indicate disease susceptibility. Significance Scalp HFOs can be used as an effective biomarker to monitor the effect and evaluate the prognosis of ACTH therapy in patients with infantile spasms.

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Scalp EEG high frequency oscillations as a biomarker of treatment response in epileptic encephalopathy with continuous spike-and-wave during sleep (CSWS)

Cited by 25 publications

References 45 publications

Scalp EEG interictal high frequency oscillations as an objective EEG biomarker of infantile spasms

Scalp EEG interictal high frequency oscillations as an objective EEG biomarker of infantile spasms

Application of High-Frequency Oscillations on Scalp EEG in Infant Spasm: A Prospective Controlled Study

Automatic detection of interictal ripples on scalp EEG to evaluate the effect and prognosis of ACTH therapy in patients with infantile spasms

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