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Respective Contribution of Ictal and Inter-ictal Electrical Source Imaging to Epileptogenic Zone Localization

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Abstract

Interictal electrical source imaging (ESI) encompasses a risk of false localization due to complex relationships between irritative and epileptogenic networks. This study aimed to compare the localizing value of ESI derived from ictal and inter-ictal EEG discharges and to evaluate the localizing value of ESI according to three different subgroups: MRI lesion, presumed etiology and morphology of ictal EEG pattern. We prospectively analyzed 54 of 78 enrolled patients undergoing pre-surgical investigation for refractory epilepsy. Ictal and inter-ictal ESI results were interpreted blinded to- and subsequently compared with stereoelectroencephalography as a reference method. Anatomical concordance was assessed at a sub-lobar level. Sensitivity and specificity of ictal, inter-ictal and ictal plus inter-ictal ESI were calculated and compared according to the different subgroups. Inter-ictal and ictal ESI sensitivity (84% and 75% respectively) and specificity (38% and 50% respectively) were not statistically different. Regarding the sensitivity, ictal ESI was never higher than inter-ictal ESI. Regarding the specificity, ictal ESI was higher than inter-ictal ESI in malformations of cortical development (MCD) (60% vs. 43%) and in MRI positive patients (49% vs. 30%). Within the ictal ESI analysis, we showed a higher specificity for ictal spikes (59%) and rhythmic discharges > 13 Hz (50%) than rhythmic discharges < 13 Hz (37%) and (ii) for MCD (60%) than in other etiologies (29%). This prospective study demonstrates the relevance of a combined interpretation of distinct inter-ictal and ictal analysis. Inter-ictal analysis gave the highest sensitivity. Ictal analysis gave the highest specificity especially in patients with MCD or a lesion on MRI.

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References

  • Abdallah C, Maillard LG, Rikir E et al (2017) Localizing value of electrical source imaging: frontal lobe, malformations of cortical development and negative MRI related epilepsies are the best candidates. Neuroimage Clin 16:319–329

    PubMed  PubMed Central  Google Scholar 

  • Alarcon G, Guy CN, Binnie CD et al (1994) Intracerebral propagation of interictal activity in partial epilepsy: implications for source localisation. J Neurol Neurosurg Psychiatry 57:435–449

    CAS  PubMed  PubMed Central  Google Scholar 

  • Alarcon G, Binnie CD, Elwes RD, Polkey CE (1995) Power spectrum and intracranial EEG patterns at seizure onset in partial epilepsy. Electroencephalogr Clin Neurophysiol 94:326–337

    CAS  PubMed  Google Scholar 

  • Alarcon G, Garcia Seoane JJ et al (1997) Origin and propagation of interictal discharges in the acute electrocorticogram. Implications for pathophysiology and surgical treatment of temporal lobe epilepsy. Brain 120:2259–2282

    PubMed  Google Scholar 

  • Bancaud J, Angelergues R, Bernouilli C et al (1970) Functional stereotaxic exploration (SEEG) of epilepsy. Electroencephalogr Clin Neurophysiol 28(1):85–86

    CAS  PubMed  Google Scholar 

  • Bartolomei F, Trébuchon A, Bonini F et al (2016) What is the concordance between the seizure onset zone and the irritative zone? A SEEG quantified study. Clin Neurophysiol 127:1157–1162

    PubMed  Google Scholar 

  • Beniczky S, Lantz G, Rosenzweig I et al (2013) Source localization of rhythmic ictal EEG activity: a study of diagnostic accuracy following STARD criteria. Epilepsia 54:1743–1752

    PubMed  Google Scholar 

  • Blanke O, Lantz G, Seeck M et al (2000) Temporal and spatial determination of EEG-seizure onset in the frequency domain. Clin Neurophysiol 111(5):763–772

    CAS  PubMed  Google Scholar 

  • Boon P, D'Havé M, Vanrumste B et al (2002) Ictal source localization in presurgical patients with refractory epilepsy. J Clin Neurophysiol 19:461–468

    PubMed  Google Scholar 

  • Brodbeck V, Spinelli L, Lascano AM et al (2011) Electroencephalographic source imaging: a prospective study of 152 operated epileptic patients. Brain 134:2887–2897

    PubMed  PubMed Central  Google Scholar 

  • Chassoux F, Devaux B, Landré E et al (2000) Stereoencephalography in focal cortical dysplasia: a 3D approach to delineating the dysplastic cortex. Brain 123:1733–1751

    PubMed  Google Scholar 

  • Duncan JS (2003) Neuroimaging in epilepsy: quality and not just quantity is important: current resources for neuroimaging could be used more efficiently. J Neurol Neurosurg Psychiatry 73:612–613

    Google Scholar 

  • Foldvary N, Klem G, Hammel J et al (2001) The localizing value of ictal EEG in focal epilepsy. Neurology 57:2022–2028

    CAS  PubMed  Google Scholar 

  • Fuchs M, Wagner M, Kastner J (2004) Confidence limits of dipole source reconstruction results. Clin Neurophysiol 115:1442–1451

    PubMed  Google Scholar 

  • Gavaret M, Badier JM, Marquis P et al (2004) Electric source imaging in temporal lobe epilepsy. J Clin Neurophysiol 21:267–282

    PubMed  Google Scholar 

  • Gavaret M, Badier JM, Marquis P et al (2006) Electric source imaging in frontal lobe epilepsy. J Clin Neurophysiol 23:358–370

    PubMed  Google Scholar 

  • Gavaret M, Trébuchon A, Bartolomei F et al (2009) Source localization of scalp-EEG interictal spikes in posterior cortex epilepsies investigated by HR-EEG and SEEG. Epilepsia 50:276–289

    PubMed  Google Scholar 

  • Grinenko O, Li J, Mosher JC, Wang IZ et al (2018) A fingerprint of the epileptogenic zone in human epilepsies. Brain 141(1):117–131

    PubMed  Google Scholar 

  • Guggisberg AG, Dalal SS, Zumer JM et al (2011) Localization of cortico-peripheral coherence with electroencephalography. Neuroimage 57:1348–1357

    PubMed  Google Scholar 

  • Hämäläinen MS, Ilmoniemi RJ (1994) Interpreting measured magnetic fields of the brain: estimation of current distributions. Med Biol Eng Comput 32:35–42

    PubMed  Google Scholar 

  • Jonas J, Vignal JP, Baumann C et al (2011) Effect of hyperventilation on seizure activation: potentiation by antiepileptic drug tapering. J Neurol Neurosurg Psychiatry 82:928–930

    PubMed  Google Scholar 

  • Kahane P, Landré E, Minotti L et al (2006) The Bancaud and Talairach view on the epileptogenic zone: a working hypothesis. Epileptic Disord 8(Suppl 2):S16–26

    PubMed  Google Scholar 

  • Knowlton RC, Razdan SN, Limdi N et al (2009) Effect of epilepsy magnetic source imaging on intracranial electrode placement. Ann Neurol 65:716–723

    PubMed  PubMed Central  Google Scholar 

  • Koessler L, Benhadid A, Maillard L et al (2008) Automatic localization and labeling of EEG sensors (ALLES) in MRI volume. Neuroimage 41:914–923

    CAS  PubMed  Google Scholar 

  • Koessler L, Maillard L, Benhadid A et al (2009) Automated cortical projection of EEG sensors: anatomical correlation via the international 10–10 system. Neuroimage 46:64–72

    CAS  PubMed  Google Scholar 

  • Koessler L, Benar C, Maillard L et al (2010) Source localization of ictal epileptic activity investigated by high resolution EEG and validated by SEEG. Neuroimage 51:642–653

    PubMed  Google Scholar 

  • Koessler L, Cecchin T, Colnat-Coulbois S et al (2015) Catching the invisible: mesial temporal source contribution to simultaneous EEG and SEEG recordings. Brain Topogr 28:5–20

    PubMed  Google Scholar 

  • Koessler L, Colnat-Coulbois S, Cecchin T et al (2017) In-vivo measurements of human brain tissue conductivity using focal electrical current injection through intracerebral multicontact electrodes. Hum Brain Mapp 38(2):974–986

    PubMed  Google Scholar 

  • Koren J, Gritsch G, Pirker S et al (2018) Automatic ictal onset source localization in presurgical epilepsy evaluation. Clin Neurophysiol 129(6):1291–1299

    PubMed  Google Scholar 

  • Kuo CC, Tucker DM, Luu P et al (2018) EEG source imaging of epileptic activity at seizure onset. Epilepsy Res 146:160–171

    PubMed  Google Scholar 

  • Lagarde S, Bonini F, McGonigal A et al (2016) Seizure-onset patterns in focal cortical dysplasia and neurodevelopmental tumors: relationship with surgical prognosis and neuropathologic subtypes. Epilepsia 57:1426–1435

    PubMed  Google Scholar 

  • Lantz G, Michel CM, Seeck M et al (1999) Frequency domain EEG source localization of ictal epileptiform activity in patients with partial complex epilepsy of temporal lobe origin. Clin Neurophysiol 110(1):176–184

    CAS  PubMed  Google Scholar 

  • Lascano AM, Perneger T, Vulliemoz S et al (2016) Yield of MRI, high-density electric source imaging (HD-ESI), SPECT and PET in epilepsy surgery candidates. Clin Neurophysiol 127(1):150–155

    PubMed  Google Scholar 

  • Lantz G, Grave de Peralta R, Spinelli L et al (2003) Epileptic source localization with high density EEG: how many electrodes are needed? Clin Neurophysiol 114:63–69

    CAS  PubMed  Google Scholar 

  • Lüders HO, Najm I, Nair D et al (2006) The epileptogenic zone: general principles. Epileptic Disord 8 Suppl 2:S1–9

    PubMed  Google Scholar 

  • Luria G, Duran D, Visani E (2019) Bayesian multi-dipole modelling in the frequency domain. J Neurosci Methods 312:27–36

    PubMed  Google Scholar 

  • Maillard L, Koessler L, Colnat-Coulbois S et al (2009) Combined SEEG and source localisation study of temporal lobe schizencephaly and polymicrogyria. Clin Neurophysiol 120:1628–1636

    CAS  PubMed  Google Scholar 

  • Maillard LG, Tassi L, Bartolomei F et al (2017) Stereoelectroencephalography and surgical outcome in polymicrogyria-related epilepsy: a multicentric study. Ann Neurol 82(5):781–794

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Michel CM, Lantz G, Spinelli L et al (2004) 128-channel EEG source imaging in epilepsy: clinical yield and localization precision. J Clin Neurophysiol 21:71–83

    PubMed  Google Scholar 

  • Mosher JC, Lewis PS, Leahy RM (1992) Multiple dipole modeling and localization from spatio-temporal MEG data. IEEE Trans Biomed Eng 39:541–557

    CAS  PubMed  Google Scholar 

  • Nemtsas P, Birot G, Pittau F et al (2017) Source localization of ictal epileptic activity based on high-density scalp EEG data. Epilepsia 58(6):1027–1036

    PubMed  Google Scholar 

  • Oostenveld R, Praamstra P (2001) The five percent electrode system for high-resolution EEG and ERP measurements. Clin Neurophysiol 112:713–719

    CAS  PubMed  Google Scholar 

  • Papayannis CE, Consalvo D, Kauffman MA et al (2012) Malformations of cortical development and epilepsy in adult patients. Seizure 21:377–384

    CAS  PubMed  Google Scholar 

  • Pascual-Marqui RD (2002) Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 24(Suppl D):S5–12

    Google Scholar 

  • Pellegrino G, Hedrich T, Chowdhury R et al (2016) Source localization of the seizure onset zone from ictal EEG/MEG data. Hum Brain Mapp 37:2528–2546

    PubMed  Google Scholar 

  • Ramantani G, Koessler L, Colnat-Coulbois S et al (2013) Intracranial evaluation of the epileptogenic zone in regional infrasylvian polymicrogyria. Epilepsia 54:296–304

    PubMed  Google Scholar 

  • Rikir E, Koessler L, Gavaret M et al (2014) Electrical source imaging in cortical malformation-related epilepsy: a prospective EEG-SEEG concordance study. Epilepsia 55:918–932

    PubMed  Google Scholar 

  • Rikir E, Koessler L, Ramantani G, Maillard LG (2017) Added value and limitations of electrical source localization. Epilepsia 58:174–175

    PubMed  Google Scholar 

  • Salado AL, Koessler L, De Mijolla G et al (2018) sEEG is a safe procedure for a comprehensive anatomic exploration of the insula: a retrospective study of 108 procedures representing 254 transopercular insular electrodes. Oper Neurosurg 14:1–8

    Google Scholar 

  • Scherg M (1990) Fundamentals of dipole source potential analysis. In: Grandori F, Hoke M, Romani GL (eds) Auditory evoked magnetic fields and electric potentials (Advance in audiology). Karger, Basel, pp 40–69

    Google Scholar 

  • Seeck M, Koessler L, Bast T et al (2017) The standardized EEG electrode array of the IFCN. Clin Neurophysiol 128:2070–2077

    PubMed  Google Scholar 

  • Sharma P, Scherg M, Pinborg LH et al (2018) Ictal and interictal electric source imaging in pre-surgical evaluation: a prospective study. Eur J Neurol 25(9):1154–1160

    CAS  PubMed  Google Scholar 

  • So N, Gotman J (1990) Changes in seizure activity following anticonvulsant drug withdrawal. Neurology 40:407–413

    CAS  PubMed  Google Scholar 

  • Spencer S, Huh L (2008) Outcomes of epilepsy surgery in adults and children. Lancet Neurol 7:525–537

    PubMed  Google Scholar 

  • Staljanssens W, Strobbe G, Holen RV et al (2017) Seizure onset zone localization from ictal high-density EEG in refractory focal epilepsy. Brain Topogr 30(2):257–271

    PubMed  Google Scholar 

  • Talairach J, Bancaud J (1966) Lesion, “irritative” zone and epileptogenic focus. Confin Neurol 27:91–94

    CAS  PubMed  Google Scholar 

  • Tonini C, Beghi E, Berg AT et al (2004) Predictors of epilepsy surgery outcome: a meta-analysis. Epilepsy Res 62:75–87

    CAS  PubMed  Google Scholar 

  • Trujillo-Barreto NJ, Aubert-Vazquez E, Valdes-Sosa PA (2004) Bayesian model averaging in EEG/MEG imaging. Neuroimage 21:1300–1319

    PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by the French Ministry of Health (PHRC 17-05, 2009).

Funding

Estelle Rikir was supported by a grant from the Medical Council of the CHU of Liège, Belgium.

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Authors and Affiliations

  1. Université de Lorraine, CHRU-Nancy, Service de Neurologie, Nancy, France

    Estelle Rikir, Louis G. Maillard, Chifaou Abdallah, Jean-Pierre Vignal & Laurent Koessler

  2. CHRU Sart-Tilman, Service de Neurologie, Liège, Belgium

    Estelle Rikir

  3. Faculté de Médecine, Université de Liège, Liège, Belgium

    Estelle Rikir

  4. Université de Lorraine, CNRS, CRAN, Nancy, France

    Louis G. Maillard, Jean-Pierre Vignal, Sophie Colnat-Coulbois & Laurent Koessler

  5. AP-HM, Service de Neurophysiologie Clinique, Hôpital de La Timone, Marseille, France

    Martine Gavaret & Fabrice Bartolomei

  6. INSERM UMR 1106, Faculté de Médecine, Institut des Neurosciences Des Systèmes, Marseille, France

    Martine Gavaret & Fabrice Bartolomei

  7. Université de Lorraine, CHRU Nancy, Service de Neurochirurgie, Nancy, France

    Sophie Colnat-Coulbois

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  1. Estelle Rikir
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Rikir, E., Maillard, L.G., Abdallah, C. et al. Respective Contribution of Ictal and Inter-ictal Electrical Source Imaging to Epileptogenic Zone Localization. Brain Topogr 33, 384–402 (2020). https://doi.org/10.1007/s10548-020-00768-3

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