Investigating current clinical opinions in stereoelectroencephalography-informed epilepsy surgery.

clinical opinions epilepsy biomarkers epilepsy surgery epileptogenic zone seizure onset zone standardized terminology stereoelectroencephalography

Journal

Epilepsia
ISSN: 1528-1167
Titre abrégé: Epilepsia
Pays: United States
ID NLM: 2983306R

Informations de publication

Date de publication:
03 Aug 2024
Historique:
revised: 11 07 2024
received: 16 02 2024
accepted: 17 07 2024
medline: 4 8 2024
pubmed: 4 8 2024
entrez: 3 8 2024
Statut: aheadofprint

Résumé

Stereoelectroencephalography (SEEG) is increasingly utilized worldwide in epilepsy surgery planning. International guidelines for SEEG terminology and interpretation are yet to be proposed. There are worldwide differences in SEEG definitions, application of features in epilepsy surgery planning, and interpretation of surgical outcomes. This hinders the clinical interpretation of SEEG findings and collaborative research. We aimed to assess the global perspectives on SEEG terminology, differences in the application of presurgical features, and variability in the interpretation of surgery outcome scores, and analyze how clinical expert demographics influenced these opinions. We assessed the practices and opinions of epileptologists with specialized training in SEEG using a survey. Data were qualitatively analyzed, and subgroups were examined based on geographical regions and years of experience. Primary outcomes included opinions on SEEG terminology, features used for epilepsy surgery, and interpretation of outcome scores. Additionally, we conducted a multilevel regression and poststratification analysis to characterize the nonresponders. A total of 321 expert responses from 39 countries were analyzed. We observed substantial differences in terminology, practices, and use of presurgical features across geographical regions and SEEG expertise levels. The majority of experts (220, 68.5%) favored the Lüders epileptogenic zone definition. Experts were divided regarding the seizure onset zone definition, with 179 (55.8%) favoring onset alone and 135 (42.1%) supporting onset and early propagation. In terms of presurgical SEEG features, a clear preference was found for ictal features over interictal features. Seizure onset patterns were identified as the most important features by 265 experts (82.5%). We found similar trends after correcting for nonresponders using regression analysis. This study underscores the need for standardized terminology, interpretation, and outcome assessment in SEEG-informed epilepsy surgery. By highlighting the diverse perspectives and practices in SEEG, this research lays a solid foundation for developing globally accepted terminology and guidelines, advancing the field toward improved communication and standardization in epilepsy surgery.

Identifiants

pubmed: 39096434
doi: 10.1111/epi.18076
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : CIHR
ID : MFE CIHR-IRSC:0633005463
Pays : Canada
Organisme : CIHR
ID : PJT-175056
Pays : Canada
Organisme : Montreal Neurological Institute and Hospital
Organisme : Fonds de Recherche du Québec - Santé

Informations de copyright

© 2024 The Author(s). Epilepsia published by Wiley Periodicals LLC on behalf of International League Against Epilepsy.

Références

Chen Z, Brodie MJ, Liew D, Kwan P. Treatment outcomes in patients with newly diagnosed epilepsy treated with established and new antiepileptic drugs a 30‐year longitudinal cohort study. JAMA Neurol. 2018;75(3):279–286. https://doi.org/10.1001/jamaneurol.2017.3949
Gavvala J, Zafar M, Sinha SR, Kalamangalam G, Schuele S. Stereotactic EEG practices: a survey of United States tertiary referral epilepsy centers. J Clin Neurophysiol. 2022;39(6):474–480. https://doi.org/10.1097/WNP.0000000000000794
Abou‐Al‐Shaar H, Brock AA, Kundu B, Englot DJ, Rolston JD. Increased nationwide use of stereoencephalography for intracranial epilepsy electroencephalography recordings. J Clin Neurosci. 2018;53:132–134. https://doi.org/10.1016/j.jocn.2018.04.064
Frauscher B. Localizing the epileptogenic zone. Curr Opin Neurol. 2020;33(2):198–206. https://doi.org/10.1097/WCO.0000000000000790
Jobst BC, Bartolomei F, Diehl B, Frauscher B, Kahane P, Minotti L, et al. Intracranial EEG in the 21st century. Epilepsy Curr. 2020;20(4):180–188. https://doi.org/10.1177/1535759720934852
Hirsch LJ, Fong MWK, Leitinger M, LaRoche SM, Beniczky S, Abend NS, et al. American clinical neurophysiology Society's standardized critical care EEG terminology: 2021 version. J Clin Neurophysiol. 2021;38(1):1–29. https://doi.org/10.1097/WNP.0000000000000806
Peltola ME, Leitinger M, Halford JJ, Vinayan KP, Kobayashi K, Pressler RM, et al. Routine and sleep EEG: minimum recording standards of the International Federation of Clinical Neurophysiology and the international league against epilepsy. Epilepsia. 2023;64(3):602–618. https://doi.org/10.1111/epi.17448
Talairach J, Bancaud J, Szikla G, Bonis A, Geier S, Vedrenne C. New approach to the neurosurgery of epilepsy. Stereotaxic methodology and therapeutic results. 1. Introduction and history. Neurochirurgie. 1974;20(Suppl 1):1–240.
Rosenow F, Lüders H. Presurgical evaluation of epilepsy. Brain. 2001;124(Pt 9):1683–1700. https://doi.org/10.1093/brain/124.9.1683
Klimes P, Cimbalnik J, Brazdil M, Hall J, Dubeau F, Gotman J, et al. NREM sleep is the state of vigilance that best identifies the epileptogenic zone in the interictal electroencephalogram. Epilepsia. 2019;60(12):2404–2415. https://doi.org/10.1111/epi.16377
Bernabei JM, Li A, Revell A, Bernabei JM, Li A, Revell AY, et al. Quantitative approaches to guide epilepsy surgery from intracranial EEG. Brain. 2023;191:2245–2255. https://doi.org/10.1093/plphys/kiac605
Travnicek V, Klimes P, Cimbalnik J, Halamek J, Jurak P, Brinkmann B, et al. Relative entropy is an easy‐to‐use invasive electroencephalographic biomarker of the epileptogenic zone. Epilepsia. 2023;64(4):962–972. https://doi.org/10.1111/epi.17539
Jacobs J, Wu JY, Perucca P, Zelmann R, Mader M, Dubeau F, et al. Removing high‐frequency oscillations: a prospective multicenter study on seizure outcome. Neurology. 2018;91(11):e1040–e1052. https://doi.org/10.1212/WNL.0000000000006158
Nakatani M, Inouchi M, Daifu‐Kobayashi M, Murai T, Togawa J, Kajikawa S, et al. Ictal direct current shifts contribute to defining the core ictal focus in epilepsy surgery. Brain Commun. 2022;4(5):fcac222.
Grinenko O, Li J, Mosher JC, Wang IZ, Bulacio JC, Gonzalez‐Martinez J, et al. A fingerprint of the epileptogenic zone in human epilepsies. Brain. 2018;141(1):117–131. https://doi.org/10.1093/brain/awx306
Bartolomei F, Chauvel P, Wendling F. Epileptogenicity of brain structures in human temporal lobe epilepsy: a quantified study from intracerebral EEG. Brain. 2008;131(7):1818–1830. https://doi.org/10.1093/brain/awn111
Li A, Huynh C, Fitzgerald Z, Cajigas I, Brusko D, Jagid J, et al. Neural fragility as an EEG marker of the seizure onset zone. Nat Neurosci. 2021;24(10):1465–1474. https://doi.org/10.1038/s41593‐021‐00901‐w
Thomas J, Kahane P, Abdallah C, Avigdor T, Zweiphenning WJEM, Chabardes S, et al. A subpopulation of spikes predicts successful epilepsy surgery outcome. Ann Neurol. 2023;93(3):522–535. https://doi.org/10.1002/ana.26548
Engel JJ. Van Ness PC, Rasmussen TB, Ojemann LM. Outcome with respect to epileptic seizures. Surg Treat Epilepsies. New York: Raven Press, 1993;609–621.
Wieser HG, Blume WT, Fish D, Goldensohn E, Hufnagel A, King D, et al. Proposal for a new classification of outcome with respect to epileptic seizures following epilepsy surgery. Epilepsia. 2001;42(2):282–286. https://doi.org/10.1046/j.1528‐1157.2001.35100.x
Menon RN, Radhakrishnan K. A survey of epilepsy surgery in India. Seizure. 2015;26:1–4. https://doi.org/10.1016/j.seizure.2015.01.005
Lin Y, Hu S, Hao X, Duan L, Wang W, Zhou D, et al. Epilepsy centers in China: current status and ways forward. Epilepsia. 2021;62(11):2640–2650. https://doi.org/10.1111/epi.17058
Kissani N, Nafia S, El Khiat A, Bengamara N, Maiga Y, Sogoba Y, et al. Epilepsy surgery in Africa: state of the art and challenges. Epilepsy Behav. 2021;118:107910. https://doi.org/10.1016/j.yebeh.2021.107910
Aljafen B, Alomar M, Abohamra N, Alanazy M, Al‐Hussain F, Alhumayyd Z, et al. Knowledge of and attitudes toward epilepsy surgery among neurologists in Saudi Arabia. Neurosciences. 2020;25(1):43–49. https://doi.org/10.17712/nsj.2020.1.20190051
Jȩdrzejczak J, Marusic P, Haldre S, Majkowska‐Zwolińska B, Bojinova‐Tchamova V, Mameniskiene R, et al. Current status of epilepsy health care for adult patients from central and eastern European Union countries – a survey of members of the Central Europe epilepsy experts working group. Seizure. 2013;22(6):452–456. https://doi.org/10.1016/j.seizure.2013.03.001
Thuy Le MA, Fong SL, Lim KS, Gunadharma S, Sejahtera DP, Visudtibhan A, et al. Underutilization of epilepsy surgery in ASEAN countries. Seizure. 2019;69:51–56. https://doi.org/10.1016/j.seizure.2019.04.002
Buttle SG, Muir K, Dehnoei S, Webster R, Tu A. Referral practices for epilepsy surgery in pediatric patients: a north American study. Epilepsia. 2022;63(1):86–95. https://doi.org/10.1111/epi.17122
Cockle E, Rayner G, Malpas C, Alpitsis R, Rheims S, O'Brien TJ, et al. An international survey of SEEG cortical stimulation practices. Epilepsia Open. 2023;8(3):1084–1095. https://doi.org/10.1002/epi4.12790
Isnard J, Taussig D, Bartolomei F, Bourdillon P, Catenoix H, Chassoux F, et al. French guidelines on stereoelectroencephalography (SEEG). Neurophysiol Clin. 2018;48(1):5–13. https://doi.org/10.1016/j.neucli.2017.11.005
Burns KEA, Duffett M, Kho ME, Meade MO, Adhikari NKJ, Sinuff T, et al. A guide for the design and conduct of self‐administered surveys of clinicians. C Can Med Assoc J. 2008;179(3):245–252. https://doi.org/10.1503/cmaj.080372
Fahimi M, Barlas F, Thomas R. American Association for Public Opinion Research (AAPOR): a practical guide for surveys based on nonprobability samples. Webinar; 2018. Availbale from: https://www.aapor.org/wp‐content/uploads/2023/01/Webinar‐Feb‐2018_Final.pdf
Jehi L. The epileptogenic zone: concept and definition. Epilepsy Curr. 2018;18(1):12–16.
De Tisi J, Bell GS, Peacock JL, McEvoy AW, Harkness WF, Sander JW, et al. The long‐term outcome of adult epilepsy surgery, patterns of seizure remission, and relapse: a cohort study. Lancet. 2011;378(9800):1388–1395. https://doi.org/10.1016/S0140‐6736(11)60890‐8
Conrad EC, Revell AY, Greenblatt AS, Gallagher RS, Pattnaik AR, Hartmann N, et al. Spike patterns surrounding sleep and seizures localize the seizure‐onset zone in focal epilepsy. Epilepsia. 2023;64(3):754–768. https://doi.org/10.1111/epi.17482
Klimes P, Peter‐Derex L, Hall J, Dubeau F, Frauscher B. Spatio‐temporal spike dynamics predict surgical outcome in adult focal epilepsy. Clin Neurophysiol. 2022;134:88–99. https://doi.org/10.1016/j.clinph.2021.10.023
Shakhatreh L, Foster E, Siriratnam P, Neal A, Carney PW, Jackson GD, et al. Impact of epilepsy surgery on quality of life: systematic review and meta‐analysis. Epilepsia. 2023;64(7):1709–1721.
Jehi L, Yardi R, Chagin K, Tassi L, Russo GL, Worrell G, et al. Development and validation of nomograms to provide individualised predictions of seizure outcomes after epilepsy surgery: a retrospective analysis. Lancet Neurol. 2015;14(3):283–290.

Auteurs

John Thomas (J)

Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.
Department of Biomedical Engineering, Duke Pratt School of Engineering, Durham, North Carolina, USA.

Chifaou Abdallah (C)

Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.

Zhengchen Cai (Z)

Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.

Kassem Jaber (K)

Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.

Jean Gotman (J)

Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.

Sandor Beniczky (S)

Danish Epilepsy Center and Aarhus University Hospital, Aarhus, Denmark.

Birgit Frauscher (B)

Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.
Department of Biomedical Engineering, Duke Pratt School of Engineering, Durham, North Carolina, USA.
Department of Neurology, Duke University Medical Center, Durham, North Carolina, USA.

Classifications MeSH