Clinical utility of intraoperative electrocorticography for epilepsy surgery: A systematic review and meta-analysis.
clinical utility
epilepsy surgery
intraoperative electrocorticography
meta-analysis
Journal
Epilepsia
ISSN: 1528-1167
Titre abrégé: Epilepsia
Pays: United States
ID NLM: 2983306R
Informations de publication
Date de publication:
02 2023
02 2023
Historique:
revised:
16
11
2022
received:
08
09
2022
accepted:
17
11
2022
pubmed:
22
11
2022
medline:
9
2
2023
entrez:
21
11
2022
Statut:
ppublish
Résumé
Despite the widespread use of intraoperative electrocorticography (iECoG) during resective epilepsy surgery, there are conflicting data on its overall efficacy and inability to predict benefit per pathology. Given the heterogeneity of iECoG use in resective epilepsy surgery, it is important to assess the utility of interictal-based iECoG. This individual patient data (IPD) meta-analysis seeks to identify the benefit of iECoG during resective epilepsy surgery in achieving seizure freedom for various pathologies. Embase, Scopus, and PubMed were searched from inception to January 31, 2021 using the following terms: "ecog", "electrocorticography", and "epilepsy". Articles were included if they reported seizure freedom at ≥12-month follow-up in cohorts with and without iECoG for epilepsy surgery. Non-English articles, noncomparative iECoG cohorts, and studies with <10% iECoG use were excluded. This meta-analysis followed the PRISMA 2020 guidelines. The primary outcome was seizure freedom at last follow-up and time to seizure recurrence, if applicable. Forest plots with random effects modeling assessed the relationship between iECoG use and seizure freedom. Cox regression of IPD was performed to identify predictors of longer duration of seizure freedom. Kaplan-Meier curves with log-rank test were created to visualize differences in time to seizure recurrence. Of 7504 articles identified, 18 were included for study-level analysis. iECoG was not associated with higher seizure freedom at the study level (relative risk = 1.09, 95% confidence interval [CI] = 0.96-1.23, p = .19, I
Types de publication
Meta-Analysis
Systematic Review
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
253-265Informations de copyright
© 2022 The Authors. Epilepsia published by Wiley Periodicals LLC on behalf of International League Against Epilepsy.
Références
Dwivedi R, Ramanujam B, Chandra PS, Sapra S, Gulati S, Kalaivani M, et al. Surgery for drug-resistant epilepsy in children. N Engl J Med. 2017;377(17):1639-47. https://doi.org/10.1056/NEJMoa1615335
Engel J, McDermott MP, Wiebe S, Langfitt JT, Stern JM, Dewar S, et al. Early surgical therapy for drug-resistant temporal lobe epilepsy. JAMA. 2012;307(9):922-30. https://doi.org/10.1001/jama.2012.220
Harroud A, Bouthillier A, Weil AG, Nguyen DK. Temporal lobe epilepsy surgery failures: a review. Epilepsy Res Treat. 2012;2012:201651. https://doi.org/10.1155/2012/201651
Nair DR, Mohamed A, Burgess R, Lüders H. A critical review of the different conceptual hypotheses framing human focal epilepsy. Epileptic Disord Int Epilepsy J Videotape. 2004;6(2):77-83.
Penfield W, Jasper H. Epilepsy and the functional anatomy of the human brain. Boston: Little, Brown & Co.; 1954:xv. p. 896.
Yang T, Hakimian S, Schwartz TH. Intraoperative ElectroCorticoGraphy (ECog): indications, techniques, and utility in epilepsy surgery. Epileptic Disord Int Epilepsy J Videotape. 2014;16(3):271-9. https://doi.org/10.1684/epd.2014.0675
Tripathi M, Garg A, Gaikwad S, Bal CS, Chitra S, Prasad K, et al. Intra-operative electrocorticography in lesional epilepsy. Epilepsy Res. 2010;89(1):133-41. https://doi.org/10.1016/j.eplepsyres.2009.12.007
Rassi-Neto A, Ferraz FP, Campos CR, Braga FM. Patients with epileptic seizures and cerebral lesions who underwent lesionectomy restricted to or associated with the adjacent irritative area. Epilepsia. 1999;40(7):856-64. https://doi.org/10.1111/j.1528-1157.1999.tb00791.x
Sugano H, Shimizu H, Sunaga S. Efficacy of intraoperative electrocorticography for assessing seizure outcomes in intractable epilepsy patients with temporal-lobe-mass lesions. Seizure. 2007;16(2):120-7. https://doi.org/10.1016/j.seizure.2006.10.010
Fernández IS, Loddenkemper T. Electrocorticography for seizure foci mapping in epilepsy surgery. J Clin Neurophysiol. 2013;30(6):554-70. https://doi.org/10.1097/01.wnp.0000436898.10125.70
Shah AK, Mittal S. Invasive electroencephalography monitoring: indications and presurgical planning. Ann Indian Acad Neurol. 2014;17(Suppl 1):S89-94. https://doi.org/10.4103/0972-2327.128668
Chassoux F, Devaux B, Landré E, Turak B, Nataf F, Varlet P, et al. Stereoelectroencephalography in focal cortical dysplasia: a 3D approach to delineating the dysplastic cortex. Brain J Neurol. 2000;123(Pt 8):1733-51. https://doi.org/10.1093/brain/123.8.1733
Kacar Bayram A, Yan Q, Isitan C, Rao S, Spencer DD, Alkawadri R. Effect of anesthesia on electrocorticography for localization of epileptic focus: literature review and future directions. Epilepsy Behav. 2021;118:107902. https://doi.org/10.1016/j.yebeh.2021.107902
Palmini A, Gambardella A, Andermann F, Dubeau F, da Costa JC, Olivier A, et al. Intrinsic epileptogenicity of human dysplastic cortex as suggested by corticography and surgical results. Ann Neurol. 1995;37(4):476-87. https://doi.org/10.1002/ana.410370410
Roehri N, Pizzo F, Lagarde S, Lambert I, Nica A, McGonigal A, et al. High-frequency oscillations are not better biomarkers of epileptogenic tissues than spikes. Ann Neurol. 2018;83(1):84-97. https://doi.org/10.1002/ana.25124
Demuru M, Kalitzin S, Zweiphenning W, van Blooijs D, van't Klooster M, van Eijsden P, et al. The value of intra-operative electrographic biomarkers for tailoring during epilepsy surgery: from group-level to patient-level analysis. Sci Rep. 2020;10(1):14654. https://doi.org/10.1038/s41598-020-71359-2
Cuello-Oderiz C, von Ellenrieder N, Sankhe R, Olivier A, Hall J, Dubeau F, et al. Value of ictal and interictal epileptiform discharges and high frequency oscillations for delineating the epileptogenic zone in patients with focal cortical dysplasia. Clin Neurophysiol. 2018;129(6):1311-9. https://doi.org/10.1016/j.clinph.2018.02.003
Lüders HO, Carreño M. General principles of pre-surgical evaluation. In: Lüders HO, editor. Textbook of epilepsy surgery. London: CRC Press; 2008. p. 409-22.
Tanriverdi T, Kemerdere R, Baran O, Sayyahmelli S, Ozlen F, Isler C, et al. Long-term surgical and seizure outcomes of frontal low-grade gliomas. Int J Surg Lond Engl. 2016;33 Pt A:60-4. https://doi.org/10.1016/j.ijsu.2016.07.065
Lesko R, Benova B, Jezdik P, Liby P, Jahodova A, Kudr M, et al. The clinical utility of intraoperative electrocorticography in pediatric epilepsy surgical strategy and planning. J Neurosurg Pediatr. 2020;26(5):533-42. https://doi.org/10.3171/2020.4.PEDS20198
Wong CH, Bleasel A, Wen L, Eberl S, Byth K, Fulham M, et al. Relationship between preoperative hypometabolism and surgical outcome in neocortical epilepsy surgery. Epilepsia. 2012;53(8):1333-40. https://doi.org/10.1111/j.1528-1167.2012.03547.x
Tanriverdi T, Kemerdere R, Baran O, Sayyahmelli S, Ozlen F, Isler C, et al. Long-term surgical and seizure outcomes of frontal low-grade gliomas. Int J Surg. 2016;33:60-4. https://doi.org/10.1016/j.ijsu.2016.07.065
Zhu Q, Liang Y, Fan Z, Liu Y, Zhou C, Zhang H, et al. The utility of intraoperative ECoG in tumor-related epilepsy: systematic review. Clin Neurol Neurosurg. 2022;212:107054. https://doi.org/10.1016/j.clineuro.2021.107054
Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71. https://doi.org/10.1136/bmj.n71
Shlobin NA, Moher D. Commentary: preferred reporting items for systematic reviews and meta-analyses 2020 statement: what neurosurgeons should know. Neurosurgery. 2021;89(5):E267-8. https://doi.org/10.1093/neuros/nyab289
Guyatt GH, Oxman AD, Vist GE, Kunz R, Falck-Ytter Y, Alonso-Coello P, et al. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ. 2008;336(7650):924-6. https://doi.org/10.1136/bmj.39489.470347.AD
Sterne JA, Hernán MA, Reeves BC, Savović J, Berkman ND, Viswanathan M, et al. ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions. BMJ. 2016;355:i4919. https://doi.org/10.1136/bmj.i4919
McHugh ML. Interrater reliability: the kappa statistic. Biochem Med. 2012;22(3):276-82.
van't Klooster MA, Leijten FSS, Huiskamp G, Ronner HE, Baayen JC, van Rijen PC, et al. High frequency oscillations in the intra-operative ECoG to guide epilepsy surgery (“the HFO trial”): study protocol for a randomized controlled trial. Trials. 2015;16:422. https://doi.org/10.1186/s13063-015-0932-6
Schwartz TH, Bazil CW, Walczak TS, Chan S, Pedley TA, Goodman RR. The predictive value of intraoperative electrocorticography in resections for limbic epilepsy associated with mesial temporal sclerosis. Neurosurgery. 1997;40(2):302-9; discussion 309-311. https://doi.org/10.1097/00006123-199702000-00014
Kuruvilla A, Flink R. Intraoperative electrocorticography in epilepsy surgery: useful or not? Seizure. 2003;12(8):577-84. https://doi.org/10.1016/S1059-1311(03)00095-5
Englot DJ, Berger MS, Barbaro NM, Chang EF. Predictors of seizure freedom after resection of supratentorial low-grade gliomas: a review. J Neurosurg. 2011;115(2):240-4. https://doi.org/10.3171/2011.3.JNS1153
Radhakrishnan A, Menon R, Abraham M, Vilanilam G, Sharma S, Thomas B, et al. Predictors of outcome after surgery in 134 children with drug-resistant TLE. Epilepsy Res. 2018;139:150-6. https://doi.org/10.1016/j.eplepsyres.2017.11.020
Luyken C, Blümcke I, Fimmers R, Urbach H, Elger CE, Wiestler OD, et al. The Spectrum of long-term epilepsy-associated tumors: long-term seizure and tumor outcome and neurosurgical aspects. Epilepsia. 2003;44(6):822-30. https://doi.org/10.1046/j.1528-1157.2003.56102.x
Roessler K, Heynold E, Buchfelder M, Stefan H, Hamer HM. Current value of intraoperative electrocorticography (iopECoG). Epilepsy Behav. 2019;91:20-4. https://doi.org/10.1016/j.yebeh.2018.06.053
Berger MS, Ghatan S, Haglund MM, Dobbins J, Ojemann GA. Low-grade gliomas associated with intractable epilepsy: seizure outcome utilizing electrocorticography during tumor resection. J Neurosurg. 1993;79(1):62-9. https://doi.org/10.3171/jns.1993.79.1.0062
Greiner HM, Horn PS, Tenney JR, Arya R, Jain SV, Holland KD, et al. Should spikes on post-resection ECoG guide pediatric epilepsy surgery? Epilepsy Res. 2016;122:73-8. https://doi.org/10.1016/j.eplepsyres.2016.02.011
El Tahry R, Ferrao Santos S, de Tourtchaninoff M, Géraldo Ribeiro Vaz J, Finet P, Raftopoulos C, et al. Post-resection electrocorticography has no added value in epilepsy surgery. Acta Neurol Belg. 2016;116(3):279-85. https://doi.org/10.1007/s13760-016-0641-2
Tran TA, Spencer SS, Marks D, Javidan M, Pacia S, Spencer DD. Significance of spikes recorded on electrocorticography in nonlesional medial temporal lobe epilepsy. Ann Neurol. 1995;38(5):763-70. https://doi.org/10.1002/ana.410380511
Lee KH, Lee YJ, Seo JH, Baumgartner JE, Westerveld M. Epilepsy surgery in children versus adults. J Korean Neurosurg Soc. 2019;62(3):328-35. https://doi.org/10.3340/jkns.2019.0026
Robertson FC, Ullrich NJ, Manley PE, Al-Sayegh H, Ma C, Goumnerova LC. The impact of intraoperative Electrocorticography on seizure outcome after resection of pediatric brain tumors: a cohort study. Neurosurgery. 2019;85(3):375-83. https://doi.org/10.1093/neuros/nyy342
Dash GK, Rathore C, Jeyaraj MK, Wattamwar P, Sarma SP, Radhakrishnan K. Predictors of seizure outcome following resective surgery for drug-resistant epilepsy associated with focal gliosis. J Neurosurg. 2018;130(6):2071-9. https://doi.org/10.3171/2018.3.JNS172949
Gallentine WB, Mikati MA. Intraoperative Electrocorticography and cortical stimulation in children. J Clin Neurophysiol. 2009;26(2):95-108. https://doi.org/10.1097/WNP.0b013e3181a0339d
Peng SJ, Wong TT, Huang CC, Chang H, Hsieh KLC, Tsai ML, et al. Quantitative analysis of intraoperative electrocorticography mirrors histopathology and seizure outcome after epileptic surgery in children. J Formos Med Assoc. 2021;120(7):1500-11. https://doi.org/10.1016/j.jfma.2020.11.001
Sacino MF, Ho CY, Murnick J, Tsuchida T, Magge SN, Keating RF, et al. Intraoperative MRI-guided resection of focal cortical dysplasia in pediatric patients: technique and outcomes. J Neurosurg Pediatr. 2016;17(6):672-8. https://doi.org/10.3171/2015.10.PEDS15512
Roessler K, Sommer B, Grummich P, Coras R, Kasper BS, Hamer HM, et al. Improved resection in lesional temporal lobe epilepsy surgery using neuronavigation and intraoperative MR imaging: Favourable long term surgical and seizure outcome in 88 consecutive cases. Seizure. 2014;23(3):201-7. https://doi.org/10.1016/j.seizure.2013.11.013
Ferrier CH, Aronica E, Leijten FSS, Spliet WGM, van Huffelen AC, van Rijen PC, et al. Electrocorticographic discharge patterns in Glioneuronal tumors and focal cortical dysplasia. Epilepsia. 2006;47(9):1477-86. https://doi.org/10.1111/j.1528-1167.2006.00619.x
Morales Chacón L, Estupiñán B, Lorigados Pedre L, Trápaga Quincoses O, García Maeso I, Sanchez A, et al. Microscopic mild focal cortical dysplasia in temporal lobe dual pathology: An electrocorticography study. Seizure. 2009;18(8):593-600. https://doi.org/10.1016/j.seizure.2009.06.008
Jayakar P, Gotman J, Harvey AS, Palmini A, Tassi L, Schomer D, et al. Diagnostic utility of invasive EEG for epilepsy surgery: indications, modalities, and techniques. Epilepsia. 2016;57(11):1735-47. https://doi.org/10.1111/epi.13515
Macdonald-Laurs E, Maixner WJ, Bailey CA, Barton SM, Mandelstam SA, Yuan-Mou Yang J, et al. One-stage, limited-resection epilepsy surgery for bottom-of-sulcus dysplasia. Neurology. 2021;97(2):e178-90. https://doi.org/10.1212/WNL.0000000000012147
Terra VC, Thomé U, Rosset SS, Funayama SS, dos Santos AC, dos Santos MV, et al. Surgery for focal cortical dysplasia in children using intraoperative mapping. Childs Nerv Syst. 2014;30(11):1839-51. https://doi.org/10.1007/s00381-014-2459-7
Choi SA, Kim KJ. The surgical and cognitive outcomes of focal cortical dysplasia. J Korean Neurosurg Soc. 2019;62(3):321-7. https://doi.org/10.3340/jkns.2019.0005
Wang X, Deng D, Zhou C, Li H, Guan X, Fang L, et al. Focal cortical dysplasia type III related medically refractory epilepsy: MRI findings and potential predictors of surgery outcome. Diagnostics. 2021;11(12):2225. https://doi.org/10.3390/diagnostics11122225
Akeret K, Bellut D, Huppertz HJ, Ramantani G, König K, Serra C, et al. Ultrasonographic features of focal cortical dysplasia and their relevance for epilepsy surgery. Neurosurg Focus. 2018;45(3):E5. https://doi.org/10.3171/2018.6.FOCUS18221
McKhann GM, Schoenfeld-McNeill J, Born DE, Haglund MM, Ojemann GA. Intraoperative hippocampal electrocorticography to predict the extent of hippocampal resection in temporal lobe epilepsy surgery. J Neurosurg. 2000;93(1):44-52. https://doi.org/10.3171/jns.2000.93.1.0044
Benifla M, Bennet-Back O, Shorer Z, Noyman I, Bar-Yosef R, Ekstein D. Temporal lobe surgery for intractable epilepsy in children: what to do with the hippocampus? Seizure. 2017;52:81-8. https://doi.org/10.1016/j.seizure.2017.09.020
Chen X, Sure U, Haag A, Knake S, Fritsch B, Müller HH, et al. Predictive value of electrocorticography in epilepsy patients with unilateral hippocampal sclerosis undergoing selective amygdalohippocampectomy. Neurosurg Rev. 2006;29(2):108-13. https://doi.org/10.1007/s10143-005-0002-8
Crevier-Sorbo G, Brunette-Clément T, Medawar E, Mathieu F, Morgan BR, Hachem LD, et al. A needs assessment of pediatric epilepsy surgery in Haiti. J Neurosurg Pediatr. 2020;27(2):189-95. https://doi.org/10.3171/2020.7.PEDS20256
Kuzniecky R, Baez C, Aranda G, Hidalgo ET, Grover A, Orillac C, et al. Epilepsy surgery in Panama: establishment of a successful hybrid program as a model for small middle-income countries. Epilepsia. 2018;59(11):2137-44. https://doi.org/10.1111/epi.14571
Crevier-Sorbo G, Brunette-Clément T, Medawar E, Mathieu F, Morgan BR, Hachem L, et al. Assessment and treatment of childhood epilepsy in Haiti. Epilepsia Open. 2020;5(2):190-7. https://doi.org/10.1002/epi4.12384
Kobayashi Y, Sato Y, Sugiyama T, Mizutani T. Intraoperative epileptogenic network visualization using gamma oscillation regularity correlation analysis in epilepsy surgery. Surg Neurol Int. 2021;12:254. https://doi.org/10.25259/SNI_298_2021
San-Juan D, Díaz-Nuñez IC, Ojeda-Baldéz M, Barajas-Juárez VA, González-Hernández I, Alonso-Vanegas M, et al. Utility of electrocorticography in the surgical treatment of cavernomas presenting with pharmacoresistant epilepsy. Epileptic Disord Int Epilepsy J Videotape. 2014;16(3):245-60. https://doi.org/10.1684/epd.2014.0674
Weil AG, Le NMD, Jayakar P, Resnick T, Miller I, Fallah A, et al. Medically resistant pediatric insular-opercular/perisylvian epilepsy. Part 2: outcome following resective surgery. J Neurosurg Pediatr. 2016;18(5):523-35. https://doi.org/10.3171/2016.4.PEDS15618
Shan YZ, Fan XT, Meng L, An Y, Xu JK, Zhao GG. Treatment and outcome of epileptogenic temporal cavernous malformations. Chin Med J (Engl). 2015;128(7):909-13. https://doi.org/10.4103/0366-6999.154289
Huang C, Li H, Chen M, Si Y, Lei D. Factors associated with preoperative and postoperative epileptic seizure in patients with cerebral ganglioglioma. Pak J Med Sci. 2014;30(2):245-9.
Englot DJ, Han SJ, Rolston JD, Ivan ME, Kuperman RA, Chang EF, et al. Epilepsy surgery failure in children: a quantitative and qualitative analysis: clinical article. J Neurosurg Pediatr. 2014;14(4):386-95. https://doi.org/10.3171/2014.7.PEDS13658
Santos MV, de Oliveira RS, Machado HR. Approach to cortical dysplasia associated with glial and glioneuronal tumors (FCD type IIIb). Childs Nerv Syst. 2014;30(11):1869-74. https://doi.org/10.1007/s00381-014-2519-z
Qiu B, Ou S, Song T, Hu J, You L, Wang Y, et al. Intraoperative electrocorticography-guided microsurgical management for patients with onset of supratentorial neoplasms manifesting as epilepsy: a review of 65 cases. Epileptic Disord. 2014;16(2):175-84. https://doi.org/10.1684/epd.2014.0662
Yao PS, Zheng SF, Wang F, Kang DZ, Lin YX. Surgery guided with intraoperative electrocorticography in patients with low-grade glioma and refractory seizures. J Neurosurg. 2017;128(3):840-5. https://doi.org/10.3171/2016.11.JNS161296
Huang C, Chen MW, Si Y, Li JM, Zhou D. Factors associated with epileptic seizure of cavernous malformations in the central nervous system in West China. Pak J Med Sci. 2013;29(5):1116-21.
Hu WH, Ge M, Zhang K, Meng FG, Zhang JG. Seizure outcome with surgical management of epileptogenic ganglioglioma: a study of 55 patients. Acta Neurochir. 2012;154(5):855-61. https://doi.org/10.1007/s00701-011-1259-z
Southwell DG, Garcia PA, Berger MS, Barbaro NM, Chang EF. Long-term seizure control outcomes after resection of Gangliogliomas. Neurosurgery. 2012;70(6):1406-14. https://doi.org/10.1227/NEU.0b013e3182500a4c
Gelinas JN, Battison AW, Smith S, Connolly MB, Steinbok P. Electrocorticography and seizure outcomes in children with lesional epilepsy. Childs Nerv Syst. 2011;27(3):381-90. https://doi.org/10.1007/s00381-010-1279-7
San-juan D, Claudia AT, Maricarmen GAF, Adriana MM, Richard JS, Mario AV. The prognostic role of electrocorticography in tailored temporal lobe surgery. Seizure. 2011;20(7):564-9. https://doi.org/10.1016/j.seizure.2011.04.006
Chang EF, Christie C, Sullivan JE, Garcia PA, Tihan T, Gupta N, et al. Seizure control outcomes after resection of dysembryoplastic neuroepithelial tumor in 50 patients: clinical article. J Neurosurg Pediatr. 2010;5(1):123-30. https://doi.org/10.3171/2009.8.PEDS09368
Ogiwara H, Nordli DR, DiPatri AJ, Alden TD, Bowman RM, Tomita T. Pediatric epileptogenic gangliogliomas: seizure outcome and surgical results: clinical article. J Neurosurg Pediatr. 2010;5(3):271-6. https://doi.org/10.3171/2009.10.PEDS09372
Gompel JJV, Rubio J, Cascino GD, Worrell GA, Meyer FB. Electrocorticography-guided resection of temporal cavernoma: is electrocorticography warranted and does it alter the surgical approach?: clinical article. J Neurosurg. 2009;110(6):1179-85. https://doi.org/10.3171/2008.10.JNS08722