Phase-amplitude coupling of interictal fast activities modulated by slow waves on scalp EEG and its correlation with seizure outcomes of disconnection surgery in children with intractable nonlesional epileptic spasms

View More View Less
  • 1 Department of Neurosurgery, Osaka City University Graduate School of Medicine;
  • 2 Departments of Pediatric Neurosurgery and
  • 3 Pediatric Neurology, Osaka City General Hospital, Osaka, Japan; and
  • 4 Department of Neurology, The Hospital for Sick Children, Toronto, Ontario, Canada
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00
Print or Print + Online

OBJECTIVE

Epileptic spasms (ESs) are classified as focal, generalized, or unknown onset ESs. The classification of ESs and surgery in patients without lesions apparent on MRI is challenging. Total corpus callosotomy (TCC) is a surgical option for diagnosis of the lateralization and possible treatment for ESs. This study investigated phase-amplitude coupling (PAC) of fast activity modulated by slow waves on scalp electroencephalography (EEG) to evaluate the strength of the modulation index (MI) before and after disconnection surgery in children with intractable nonlesional ESs. The authors hypothesize that a decreased MI due to surgery correlates with good seizure outcomes.

METHODS

The authors studied 10 children with ESs without lesions on MRI who underwent disconnection surgeries. Scalp EEG was obtained before and after surgery. The authors collected 20 epochs of 3 minutes each during non–rapid eye movement sleep. The MI of the gamma (30–70 Hz) amplitude and delta (0.5–4 Hz) phase was obtained in each electrode. MIs for each electrode were averaged in 4 brain areas (left/right, anterior/posterior quadrants) and evaluated to determine the correlation with seizure outcomes.

RESULTS

The median age at first surgery was 2.3 years (range 10 months–9.1 years). Two patients with focal onset ESs underwent anterior quadrant disconnection (AQD). TCC alone was performed in 5 patients with generalized or unknown onset ESs. Two patients achieved seizure freedom. Three patients had residual generalized onset ESs. Disconnection surgeries in addition to TCC consisted of TCC + posterior quadrant disconnection (PQD) (1 patient); TCC + AQD + PQD (1 patient); and TCC + AQD + hemispherotomy (1 patient). Seven patients became seizure free with a mean follow-up period of 28 months (range 5–54 months). After TCC, MIs in 4 quadrants were significantly lower in the 2 seizure-free patients than in the 6 patients with residual ESs (p < 0.001). After all 15 disconnection surgeries in 10 patients, MIs in the 13 target quadrants for each disconnection surgery that resulted in freedom from seizures were significantly lower than in the 26 target quadrants in patients with residual ESs (p < 0.001).

CONCLUSIONS

In children with nonlesional ESs, PAC for scalp EEG before and after disconnection surgery may be a surrogate marker for control of ESs. The MI may indicate epileptogenic neuronal modulation of the interhemispheric corpus callosum and intrahemispheric subcortical network for ESs. TCC may be a therapeutic option to disconnect the interhemispheric modulation of epileptic networks.

ABBREVIATIONS AQD = anterior quadrant disconnection; EEG = electroencephalography; ES = epileptic spasm; HFO = high-frequency oscillation; ILAE = International League Against Epilepsy; IS = infantile spasm; MI = modulation index; PAC = phase-amplitude coupling; PQD = posterior quadrant disconnection; ROC = receiver operating characteristic; TCC = total corpus callosotomy; vEEG = video EEG.

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00

Contributor Notes

Correspondence Takehiro Uda: Osaka City University Graduate School of Medicine, Osaka, Japan. uda@med.osaka-cu.ac.jp.

INCLUDE WHEN CITING Published online February 26, 2021; DOI: 10.3171/2020.9.PEDS20520.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

  • 1

    Fisher RS, Cross JH, D’Souza C, Instruction manual for the ILAE 2017 operational classification of seizure types. Epilepsia. 2017;58(4):531542.

    • Search Google Scholar
    • Export Citation
  • 2

    Chugani HT, Ilyas M, Kumar A, Surgical treatment for refractory epileptic spasms: the Detroit series. Epilepsia. 2015;56(12):19411949.

    • Search Google Scholar
    • Export Citation
  • 3

    Chipaux M, Dorfmüller G, Fohlen M, Refractory spasms of focal onset—a potentially curable disease that should lead to rapid surgical evaluation. Seizure. 2017;51:163170.

    • Search Google Scholar
    • Export Citation
  • 4

    Barba C, Mai R, Grisotto L, Unilobar surgery for symptomatic epileptic spasms. Ann Clin Transl Neurol. 2016;4(1):3645.

  • 5

    Baba H, Toda K, Ono T, Surgical and developmental outcomes of corpus callosotomy for West syndrome in patients without MRI lesions. Epilepsia. 2018;59(12):22312239.

    • Search Google Scholar
    • Export Citation
  • 6

    Iwasaki M, Uematsu M, Sato Y, Complete remission of seizures after corpus callosotomy. J Neurosurg Pediatr. 2012;10(1):713.

  • 7

    Baba S, Vakorin VA, Doesburg SM, EEG before and after total corpus callosotomy for pharmacoresistant infantile spasms: fast oscillations and slow-wave connectivity in hypsarrhythmia. Epilepsia. 2019;60(9):18491860.

    • Search Google Scholar
    • Export Citation
  • 8

    Buzsáki G, Draguhn A. Neuronal oscillations in cortical networks. Science. 2004;304(5679):19261929.

  • 9

    Canolty RT, Edwards E, Dalal SS, High gamma power is phase-locked to theta oscillations in human neocortex. Science. 2006;313(5793):16261628.

    • Search Google Scholar
    • Export Citation
  • 10

    Cohen MX, Elger CE, Fell J. Oscillatory activity and phase-amplitude coupling in the human medial frontal cortex during decision making. J Cogn Neurosci. 2009;21(2):390402.

    • Search Google Scholar
    • Export Citation
  • 11

    Tort AB, Komorowski R, Eichenbaum H, Kopell N. Measuring phase-amplitude coupling between neuronal oscillations of different frequencies. J Neurophysiol. 2010;104(2):11951210.

    • Search Google Scholar
    • Export Citation
  • 12

    Hülsemann MJ, Naumann E, Rasch B. Quantification of phase-amplitude coupling in neuronal oscillations: comparison of phase-locking value, mean vector length, modulation index, and generalized-linear-modeling-cross-frequency-coupling. Front Neurosci. 2019;13:573.

    • Search Google Scholar
    • Export Citation
  • 13

    Ibrahim GM, Wong SM, Anderson RA, Dynamic modulation of epileptic high frequency oscillations by the phase of slower cortical rhythms. Exp Neurol. 2014;251:3038.

    • Search Google Scholar
    • Export Citation
  • 14

    Iimura Y, Jones K, Hattori K, Epileptogenic high-frequency oscillations skip the motor area in children with multilobar drug-resistant epilepsy. Clin Neurophysiol. 2017;128(7):11971205.

    • Search Google Scholar
    • Export Citation
  • 15

    Motoi H, Miyakoshi M, Abel TJ, Phase-amplitude coupling between interictal high-frequency activity and slow waves in epilepsy surgery. Epilepsia. 2018;59(10):19541965.

    • Search Google Scholar
    • Export Citation
  • 16

    Nonoda Y, Miyakoshi M, Ojeda A, Interictal high-frequency oscillations generated by seizure onset and eloquent areas may be differentially coupled with different slow waves. Clin Neurophysiol. 2016;127(6):24892499.

    • Search Google Scholar
    • Export Citation
  • 17

    von Ellenrieder N, Frauscher B, Dubeau F, Gotman J. Interaction with slow waves during sleep improves discrimination of physiologic and pathologic high-frequency oscillations (80-500 Hz). Epilepsia. 2016;57(6):869878.

    • Search Google Scholar
    • Export Citation
  • 18

    Weiss SA, Orosz I, Salamon N, Ripples on spikes show increased phase-amplitude coupling in mesial temporal lobe epilepsy seizure-onset zones. Epilepsia. 2016;57(11):19161930.

    • Search Google Scholar
    • Export Citation
  • 19

    Kobayashi K, Akiyama T, Oka M, A storm of fast (40-150Hz) oscillations during hypsarrhythmia in West syndrome. Ann Neurol. 2015;77(1):5867.

    • Search Google Scholar
    • Export Citation
  • 20

    Iimura Y, Jones K, Takada L, Strong coupling between slow oscillations and wide fast ripples in children with epileptic spasms: investigation of modulation index and occurrence rate. Epilepsia. 2018;59(3):544554.

    • Search Google Scholar
    • Export Citation
  • 21

    Iimura Y, Sugano H, Nakajima M, Is decremental modulation index on scalp EEG a sign of good seizure outcome? A Sturge-Weber syndrome case with epileptic spasms. Clin Neurophysiol. 2019;130(9):14991501.

    • Search Google Scholar
    • Export Citation
  • 22

    Miyakoshi M, Delorme A, Mullen T, Automated detection of cross-frequency coupling in the electrocorticogram for clinical inspection. Annu Int Conf IEEE Eng Med Biol Soc. 2013;2013:32823285.

    • Search Google Scholar
    • Export Citation
  • 23

    Fluss R, Faraggi D, Reiser B. Estimation of the Youden Index and its associated cutoff point. Biom J. 2005;47(4):458472.

  • 24

    Daniel RT, Meagher-Villemure K, Farmer JP, Posterior quadrantic epilepsy surgery: technical variants, surgical anatomy, and case series. Epilepsia. 2007;48(8):14291437.

    • Search Google Scholar
    • Export Citation
  • 25

    Umaba R, Uda T, Nakajo K, Anatomic understanding of posterior quadrant disconnection from cadaveric brain, 3D reconstruction and simulation model, and intraoperative photographs. World Neurosurg. 2018;120:e792e801.

    • Search Google Scholar
    • Export Citation
  • 26

    Ono T, Baba H, Toda K, Ono K. Callosotomy and subsequent surgery for children with refractory epilepsy. Epilepsy Res. 2011;93(2-3):185191.

    • Search Google Scholar
    • Export Citation
  • 27

    Wilmshurst JM, Ibekwe RC, O’Callaghan FJK. Epileptic spasms—175 years on: trying to teach an old dog new tricks. Seizure. 2017;44:8186.

    • Search Google Scholar
    • Export Citation
  • 28

    Vigevano F, Fusco L, Pachatz C. Neurophysiology of spasms. Brain Dev. 2001;23(7):467472.

  • 29

    Chugani HT, Shields WD, Shewmon DA, Infantile spasms: I. PET identifies focal cortical dysgenesis in cryptogenic cases for surgical treatment. Ann Neurol. 1990;27(4):406413.

    • Search Google Scholar
    • Export Citation
  • 30

    Palmini A, Gambardella A, Andermann F, Intrinsic epileptogenicity of human dysplastic cortex as suggested by corticography and surgical results. Ann Neurol. 1995;37(4):476487.

    • Search Google Scholar
    • Export Citation
  • 31

    Gibbs FA, Gibbs EL. Atlas of Electroencephalography. Vol. 2. Addison-Wesley; 1952.

Metrics

All Time Past Year Past 30 Days
Abstract Views 469 469 214
Full Text Views 50 50 13
PDF Downloads 34 34 11
EPUB Downloads 0 0 0