Neurophysiological seizure-onset predictors of epilepsy surgery outcome: a multivariable analysis

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OBJECTIVE

The authors sought to determine which neurophysiological seizure-onset features seen during scalp electroencephalography (EEG) and intracerebral EEG (iEEG) monitoring are predictors of postoperative outcome in a large series of patients with drug-resistant focal epilepsy who underwent resective surgery.

METHODS

The authors retrospectively analyzed the records of 75 consecutive patients with focal epilepsy, who first underwent scalp EEG and then iEEG (stereo-EEG) for presurgical assessment and who went on to undergo resective surgery between 2004 and 2015. To determine the independent prognostic factors from the neurophysiological scalp EEG and iEEG seizure-onset information, univariate and standard multivariable logistic regression analyses were used. Since scalp EEG and iEEG data were recorded at different times, the authors matched scalp seizures with intracerebral seizures for each patient using strict criteria.

RESULTS

A total of 3057 seizures were assessed. Forty-eight percent (36/75) of patients had a favorable outcome (Engel class I–II) after a minimum follow-up of at least 1 year. According to univariate analysis, a localized scalp EEG seizure onset (p < 0.001), a multilobar intracerebral seizure-onset zone (SOZ) (p < 0.001), and an extended SOZ (p = 0.001) were significantly associated with surgical outcome. According to multivariable analysis, the following two independent factors were found: 1) the ability of scalp EEG to localize the seizure onset was a predictor of a favorable postoperative outcome (OR 6.073, 95% CI 2.011–18.339, p = 0.001), and 2) a multilobar SOZ was a predictor of an unfavorable outcome (OR 0.076, 95% CI 0.009–0.663, p = 0.020).

CONCLUSIONS

The study findings show that localization at scalp seizure onset and a multilobar SOZ were strong predictors of surgical outcome. These predictors can help to select the better candidates for resective surgery.

ABBREVIATIONS EEG = electroencephalography; iEEG = intracerebral EEG; SOZ = seizure-onset zone; TLE = temporal lobe epilepsy.
Article Information

Contributor Notes

Correspondence Hideaki Tanaka: Montreal Neurological Institute and Hospital, McGill University, Montreal, QC, Canada. hideaki08seven@gmail.com.INCLUDE WHEN CITING Published online November 29, 2019; DOI: 10.3171/2019.9.JNS19527.Disclosures Dr. Gotman reports being on the scientific advisory board of Precisis AG.
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References
  • 1

    Barba CRheims SMinotti LGuénot MHoffmann DChabardès S: Temporal plus epilepsy is a major determinant of temporal lobe surgery failures. Brain 139:4444512016

    • Search Google Scholar
    • Export Citation
  • 2

    Bartolomei FChauvel PWendling F: Epileptogenicity of brain structures in human temporal lobe epilepsy: a quantified study from intracerebral EEG. Brain 131:181818302008

    • Search Google Scholar
    • Export Citation
  • 3

    Beniczky SLantz GRosenzweig IÅkeson PPedersen BPinborg LH: Source localization of rhythmic ictal EEG activity: a study of diagnostic accuracy following STARD criteria. Epilepsia 54:174317522013

    • Search Google Scholar
    • Export Citation
  • 4

    Engel J Jr: Surgery for seizures. N Engl J Med 334:6476521996

  • 5

    Engel J Jr: Surgical Treatment of the Epilepsiesed 2. New York: Raven Press1993

  • 6

    Engel J JrMcDermott MPWiebe SLangfitt JTStern JMDewar S: Early surgical therapy for drug-resistant temporal lobe epilepsy: a randomized trial. JAMA 307:9229302012

    • Search Google Scholar
    • Export Citation
  • 7

    Foldvary NKlem GHammel JBingaman WNajm ILüders H: The localizing value of ictal EEG in focal epilepsy. Neurology 57:202220282001

    • Search Google Scholar
    • Export Citation
  • 8

    Hall JAKhoo HM: Robotic-assisted and image-guided MRI-compatible stereoelectroencephalography. Can J Neurol Sci 45:35432018

  • 9

    Holtkamp MSharan ASperling MR: Intracranial EEG in predicting surgical outcome in frontal lobe epilepsy. Epilepsia 53:173917452012

    • Search Google Scholar
    • Export Citation
  • 10

    Jobst BCCascino GD: Resective epilepsy surgery for drug-resistant focal epilepsy: a review. JAMA 313:2852932015

  • 11

    Kim DWKim HKLee SKChu KChung CK: Extent of neocortical resection and surgical outcome of epilepsy: intracranial EEG analysis. Epilepsia 51:101010172010

    • Search Google Scholar
    • Export Citation
  • 12

    Kim DWLee SKMoon HJJung KYChu KChung CK: Surgical treatment of nonlesional neocortical epilepsy: long-term longitudinal study. JAMA Neurol 74:3243312017

    • Search Google Scholar
    • Export Citation
  • 13

    Kovac SVakharia VNScott CDiehl B: Invasive epilepsy surgery evaluation. Seizure 44:1251362017

  • 14

    Lagarde SBonini FMcGonigal AChauvel PGavaret MScavarda D: Seizure-onset patterns in focal cortical dysplasia and neurodevelopmental tumors: relationship with surgical prognosis and neuropathologic subtypes. Epilepsia 57:142614352016

    • Search Google Scholar
    • Export Citation
  • 15

    Olivier ABoling WWTanriverdi T: Techniques in Epilepsy Surgery: The MNI Approach. New York: Cambridge University Press2012

  • 16

    Olivier AGermano IMCukiert APeters T: Frameless stereotaxy for surgery of the epilepsies: preliminary experience. Technical note. J Neurosurg 81:6296331994

    • Search Google Scholar
    • Export Citation
  • 17

    Perucca PDubeau FGotman J: Intracranial electroencephalographic seizure-onset patterns: effect of underlying pathology. Brain 137:1831962014

    • Search Google Scholar
    • Export Citation
  • 18

    Pittau FDubeau FGotman J: Contribution of EEG/fMRI to the definition of the epileptic focus. Neurology 78:147914872012

  • 19

    Rosenow FLüders H: Presurgical evaluation of epilepsy. Brain 124:168317002001

  • 20

    Singh SSandy SWiebe S: Ictal onset on intracranial EEG: Do we know it when we see it? State of the evidence. Epilepsia 56:162916382015

    • Search Google Scholar
    • Export Citation
  • 21

    Spanedda FCendes FGotman J: Relations between EEG seizure morphology, interhemispheric spread, and mesial temporal atrophy in bitemporal epilepsy. Epilepsia 38:130013141997

    • Search Google Scholar
    • Export Citation
  • 22

    Sperling MRO’Connor MJ: Auras and subclinical seizures: characteristics and prognostic significance. Ann Neurol 28:3203281990

  • 23

    Steinhoff BJSo NKLim SLüders HO: Ictal scalp EEG in temporal lobe epilepsy with unitemporal versus bitemporal interictal epileptiform discharges. Neurology 45:8898961995

    • Search Google Scholar
    • Export Citation
  • 24

    Tanaka HKhoo HMDubeau FGotman J: Association between scalp and intracerebral electroencephalographic seizure-onset patterns: a study in different lesional pathological substrates. Epilepsia 59:4204302018

    • Search Google Scholar
    • Export Citation
  • 25

    Wetjen NMMarsh WRMeyer FBCascino GDSo EBritton JW: Intracranial electroencephalography seizure onset patterns and surgical outcomes in nonlesional extratemporal epilepsy. J Neurosurg 110:114711522009

    • Search Google Scholar
    • Export Citation
  • 26

    Widdess-Walsh PJeha LNair DKotagal PBingaman WNajm I: Subdural electrode analysis in focal cortical dysplasia: predictors of surgical outcome. Neurology 69:6606672007

    • Search Google Scholar
    • Export Citation
  • 27

    Wiebe SBlume WTGirvin JPEliasziw M: A randomized, controlled trial of surgery for temporal-lobe epilepsy. N Engl J Med 345:3113182001

    • Search Google Scholar
    • Export Citation
  • 28

    Worrell GASo ELKazemi JO’Brien TJMosewich RKCascino GD: Focal ictal beta discharge on scalp EEG predicts excellent outcome of frontal lobe epilepsy surgery. Epilepsia 43:2772822002

    • Search Google Scholar
    • Export Citation
  • 29

    Yun CHLee SKLee SYKim KKJeong SWChung CK: Prognostic factors in neocortical epilepsy surgery: multivariate analysis. Epilepsia 47:5745792006

    • Search Google Scholar
    • Export Citation
  • 30

    Zakaria TNoe KSo ECascino GDWetjen NVan Gompel JJ: Scalp and intracranial EEG in medically intractable extratemporal epilepsy with normal MRI. ISRN Neurol 2012:9428492012

    • Search Google Scholar
    • Export Citation
  • 31

    Zangaladze ANei MLiporace JDSperling MR: Characteristics and clinical significance of subclinical seizures. Epilepsia 49:201620212008

    • Search Google Scholar
    • Export Citation
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