Preoperative localization of seizure onset zones by magnetic source imaging, EEG-correlated functional MRI, and their combination

View More View Less
  • 1 Department of Neurosurgery,
  • 2 Sagol Brain Institute,
  • 3 Department of Neurology, and
  • 6 Department of Radiology, Tel Aviv Medical Center, Tel Aviv;
  • 4 Department of Neurology, Hadassah Medical Center, Jerusalem;
  • 5 Department of Neurosurgery, Rambam Health Care Campus, Haifa;
  • 7 Sackler Faculty of Medicine, Tel-Aviv University, Tel Aviv;
  • 8 Hebrew University Hadassah Medical School, Jerusalem; and
  • 9 Rappaport Faculty of Medicine-Technion, Haifa, Israel
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

Preoperative localization of seizure onset zones (SOZs) is an evolving field in the treatment of refractory epilepsy. Both magnetic source imaging (MSI), and the more recent EEG-correlated functional MRI (EEG-fMRI), have shown applicability in assisting surgical planning. The purpose of this study was to evaluate the capability of each method and their combination in localizing the seizure onset lobe (SL).

METHODS

The study included 14 patients who underwent both MSI and EEG-fMRI before undergoing implantation of intracranial EEG (icEEG) as part of the presurgical planning of the resection of an epileptogenic zone (EZ) during the years 2012–2018. The estimated location of the SL by each method was compared with the location determined by icEEG. Identification rates of the SL were compared between the different methods.

RESULTS

MSI and EEG-fMRI showed similar identification rates of SL locations in relation to icEEG results (88% ± 31% and 73% ± 42%, respectively; p = 0.281). The additive use of the coverage lobes of both methods correctly identified 100% of the SL, significantly higher than EEG-fMRI alone (p = 0.039) and nonsignificantly higher than MSI (p = 0.180). False-identification rates of the additive coverage lobes were significantly higher than MSI (p = 0.026) and EEG-fMRI (p = 0.027). The intersecting lobes of both methods showed the lowest false identification rate (13% ± 6%, p = 0.01).

CONCLUSIONS

Both MSI and EEG-fMRI can assist in the presurgical evaluation of patients with refractory epilepsy. The additive use of both tests confers a high identification rate in finding the SL. This combination can help in focusing implantation of icEEG electrodes targeting the SOZ.

ABBREVIATIONS DRE = drug-resistant epilepsy; EZ = epileptogenic zone; FCD = focal cortical dysplasia; fMRI = functional MRI; FP = false positive; icEEG = intracranial EEG; IED = interictal epileptiform discharge; MEG = magnetoencephalography; MSI = magnetic source imaging; SL = seizure onset lobe; SOZ = seizure onset zone.

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 Assaf Berger: Tel Aviv Medical Center, Tel Aviv, Israel. assaf.berger@gmail.com.

INCLUDE WHEN CITING Published online May 15, 2020; DOI: 10.3171/2020.3.JNS192794.

A.B., N.C., T.G., and I.S. contributed equally to this work.

Disclosures Dr. Medvedovsky reports being one of the authors of the patent related to the dual-array EEG-fMRI approach.

  • 1

    World Health Organization . Newsroom Fact Sheets. Epilepsy . June 20, 2019 . Accessed March 18, 2020. https://www.who.int/news-room/fact-sheets/detail/epilepsy

    • Search Google Scholar
    • Export Citation
  • 2

    Kwan P , Sperling MR . Refractory seizures: try additional antiepileptic drugs (after two have failed) or go directly to early surgery evaluation? Epilepsia . 2009 ;50 (suppl 8 ):57 62 .

    • Search Google Scholar
    • Export Citation
  • 3

    Engel J Jr. The current place of epilepsy surgery . Curr Opin Neurol . 2018 ;31 (2 ):192 197 .

  • 4

    Engel J Jr. What can we do for people with drug-resistant epilepsy? The 2016 Wartenberg Lecture . Neurology . 2016 ;87 (23 ):2483 2489 .

    • Search Google Scholar
    • Export Citation
  • 5

    Vakharia VN , Duncan JS , Witt JA , Getting the best outcomes from epilepsy surgery . Ann Neurol . 2018 ;83 (4 ):676 690 .

  • 6

    Englot DJ , Han SJ , Rolston JD , Epilepsy surgery failure in children: a quantitative and qualitative analysis . J Neurosurg Pediatr . 2014 ;14 (4 ):386 395 .

    • Search Google Scholar
    • Export Citation
  • 7

    Englot DJ , Nagarajan SS , Imber BS , Epileptogenic zone localization using magnetoencephalography predicts seizure freedom in epilepsy surgery . Epilepsia . 2015 ;56 (6 ):949 958 .

    • Search Google Scholar
    • Export Citation
  • 8

    Englot DJ , Raygor KP , Molinaro AM , Factors associated with failed focal neocortical epilepsy surgery . Neurosurgery . 2014 ;75 (6 ):648 656 .

    • Search Google Scholar
    • Export Citation
  • 9

    Hari R , Salmelin R . Magnetoencephalography: from SQUIDs to neuroscience. Neuroimage 20th anniversary special edition . Neuroimage . 2012 ;61 (2 ):386 -396 .

    • Search Google Scholar
    • Export Citation
  • 10

    Medvedovsky M , Taulu S , Gaily E , Sensitivity and specificity of seizure-onset zone estimation by ictal magnetoencephalography . Epilepsia . 2012 ;53 (9 ):1649 1657 .

    • Search Google Scholar
    • Export Citation
  • 11

    Wilenius J , Medvedovsky M , Gaily E , Interictal MEG reveals focal cortical dysplasias: special focus on patients with no visible MRI lesions . Epilepsy Res . 2013 ;105 (3 ):337 348 .

    • Search Google Scholar
    • Export Citation
  • 12

    Vulliemoz S , Lemieux L , Daunizeau J , The combination of EEG source imaging and EEG-correlated functional MRI to map epileptic networks . Epilepsia . 2010 ;51 (4 ):491 505 .

    • Search Google Scholar
    • Export Citation
  • 13

    Bénar CG , Grova C , Kobayashi E , EEG-fMRI of epileptic spikes: concordance with EEG source localization and intracranial EEG . Neuroimage . 2006 ;30 (4 ):1161 1170 .

    • Search Google Scholar
    • Export Citation
  • 14

    Khoo HM , Hao Y , von Ellenrieder N , The hemodynamic response to interictal epileptic discharges localizes the seizure-onset zone . Epilepsia . 2017 ;58 (5 ):811 823 .

    • Search Google Scholar
    • Export Citation
  • 15

    Klovatch-Podlipsky I , Gazit T , Fahoum F , Dual array EEG-fMRI: an approach for motion artifact suppression in EEG recorded simultaneously with fMRI . Neuroimage . 2016 ;142 :674 686 .

    • Search Google Scholar
    • Export Citation
  • 16

    Liu JV , Kobylarz EJ , Darcey TM , Improved mapping of interictal epileptiform discharges with EEG-fMRI and voxel-wise functional connectivity analysis . Epilepsia . 2014 ;55 (9 ):1380 1388 .

    • Search Google Scholar
    • Export Citation
  • 17

    van Graan LA , Lemieux L , Chaudhary UJ . Methods and utility of EEG-fMRI in epilepsy . Quant Imaging Med Surg . 2015 ;5 (2 ):300 312 .

    • Search Google Scholar
    • Export Citation
  • 18

    Iida K , Otsubo H , Matsumoto Y , Characterizing magnetic spike sources by using magnetoencephalography-guided neuronavigation in epilepsy surgery in pediatric patients . J Neurosurg . 2005 ;102 (2)(suppl):187–196 .

    • Search Google Scholar
    • Export Citation
  • 19

    Ramachandran VS , Altschuler EL . The use of visual feedback, in particular mirror visual feedback, in restoring brain function . Brain . 2009 ;132 (Pt 7 ):1693 1710 .

    • Search Google Scholar
    • Export Citation
  • 20

    Rosenow F , Lüders H . Presurgical evaluation of epilepsy . Brain . 2001 ;124 (Pt 9 ):1683 1700 .

  • 21

    Stefan H , Hummel C , Scheler G , Magnetic brain source imaging of focal epileptic activity: a synopsis of 455 cases . Brain . 2003 ;126 (Pt 11 ):2396 2405 .

    • Search Google Scholar
    • Export Citation
  • 22

    Agarwal N , Krishnan B , Burgess RC , Magnetoencephalographic characteristics of cortical dysplasia in children . Pediatr Neurol . 2018 ;78 :13 19 .

    • Search Google Scholar
    • Export Citation
  • 23

    Thornton R , Laufs H , Rodionov R , EEG correlated functional MRI and postoperative outcome in focal epilepsy . J Neurol Neurosurg Psychiatry . 2010 ;81 (8 ):922 927 .

    • Search Google Scholar
    • Export Citation
  • 24

    Heers M , Hedrich T , An D , Spatial correlation of hemodynamic changes related to interictal epileptic discharges with electric and magnetic source imaging . Hum Brain Mapp . 2014 ;35 (9 ):4396 4414 .

    • Search Google Scholar
    • Export Citation
  • 25

    Pittau F , Grouiller F , Spinelli L , The role of functional neuroimaging in pre-surgical epilepsy evaluation . Front Neurol . 2014 ;5 :31 .

    • Search Google Scholar
    • Export Citation
  • 26

    Vaudano AE , Carmichael DW , Salek-Haddadi A , Networks involved in seizure initiation. A reading epilepsy case studied with EEG-fMRI and MEG . Neurology . 2012 ;79 (3 ):249 253 .

    • Search Google Scholar
    • Export Citation
  • 27

    Bulacio JC , Jehi L , Wong C , Long-term seizure outcome after resective surgery in patients evaluated with intracranial electrodes . Epilepsia . 2012 ;53 (10 ):1722 1730 .

    • Search Google Scholar
    • Export Citation
  • 28

    Lazow SP , Thadani VM , Gilbert KL , Outcome of frontal lobe epilepsy surgery . Epilepsia . 2012 ;53 (10 ):1746 1755 .

  • 29

    Malmgren K , Edelvik A . Long-term outcomes of surgical treatment for epilepsy in adults with regard to seizures, antiepileptic drug treatment and employment . Seizure . 2017 ;44 :217 224 .

    • Search Google Scholar
    • Export Citation
  • 30

    Blumcke I , Spreafico R , Haaker G , Histopathological findings in brain tissue obtained during epilepsy surgery . N Engl J Med . 2017 ;377 (17 ):1648 1656 .

    • Search Google Scholar
    • Export Citation
  • 31

    Cohen-Gadol AA , Ozduman K , Bronen RA , Long-term outcome after epilepsy surgery for focal cortical dysplasia . J Neurosurg . 2004 ;101 (1 ):55 65 .

    • Search Google Scholar
    • Export Citation
  • 32

    Fauser S , Essang C , Altenmüller DM , Long-term seizure outcome in 211 patients with focal cortical dysplasia . Epilepsia . 2015 ;56 (1 ):66 76 .

    • Search Google Scholar
    • Export Citation
  • 33

    Lee SK , Kim DW . Focal cortical dysplasia and epilepsy surgery . J Epilepsy Res . 2013 ;3 (2 ):43 47 .

  • 34

    Tassi L , Colombo N , Garbelli R , Focal cortical dysplasia: neuropathological subtypes, EEG, neuroimaging and surgical outcome . Brain . 2002 ;125 (Pt 8 ):1719 1732 .

    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 134 134 134
Full Text Views 53 53 53
PDF Downloads 43 43 43
EPUB Downloads 0 0 0