Stereo-electroencephalography (SEEG)-Guided Surgery in Epilepsy With Cingulate Gyrus Involvement: Electrode Implantation Strategies and Postoperative Seizure Outcome.
Journal
Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society
ISSN: 1537-1603
Titre abrégé: J Clin Neurophysiol
Pays: United States
ID NLM: 8506708
Informations de publication
Date de publication:
01 Sep 2023
01 Sep 2023
Historique:
medline:
4
9
2023
pubmed:
18
3
2023
entrez:
17
3
2023
Statut:
ppublish
Résumé
Surgical treatment of cingulate gyrus epilepsy is associated with good results on seizures despite its rarity and challenging aspects. Invasive EEG monitoring is often mandatory to assess the epileptogenic zone in these patients. To date, only small surgical series have been published, and a consensus about management of these complex cases did not emerge. The authors retrospectively analyzed a large surgical series of patients in whom at least part of the cingulate gyrus was confirmed as included in the epileptogenic zone by means of stereo-electroencephalography and was thus resected. One hundred twenty-seven patients were selected. Stereo-electroencephalography-guided implantation of intracerebral electrodes was performed in the right hemisphere in 62 patients (48.8%) and in the left hemisphere in 44 patients (34.7%), whereas 21 patients (16.5%) underwent bilateral implantations. The median number of implanted electrodes per patient was 13 (interquartile range 12-15). The median number of electrodes targeting the cingulate gyrus was 4 (interquartile range 3-5). The cingulate gyrus was explored bilaterally in 19 patients (15%). Complication rate was 0.8%. A favorable outcome (Engel class I) was obtained in 54.3% of patients, with a median follow-up of 60 months. The chance to obtain seizure freedom increased in cases in whom histologic diagnosis was type-IIb focal cortical dysplasia or tumor (mostly ganglioglioma or dysembryoplastic neuroepithelial tumor) and with male gender. Higher seizure frequency predicted better outcome with a trend toward significance. Our findings suggest that stereo-electroencephalography is a safe and effective methodology in achieving seizure freedom in complex cases of epilepsy with cingulate gyrus involvement.
Identifiants
pubmed: 36930225
doi: 10.1097/WNP.0000000000001000
pii: 00004691-990000000-00080
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
516-528Informations de copyright
Copyright © 2023 by the American Clinical Neurophysiology Society.
Déclaration de conflit d'intérêts
The authors have no funding or conflicts of interest to disclose.
Références
Alkawadri R, So NK, Van Ness PC, Alexopoulos AV. Cingulate epilepsy: report of 3 electroclinical subtypes with surgical outcomes. JAMA Neurol 2013;70:995–1002.
Powell R, Elwes R, Hamandi K, Mullatti N. Cingulate gyrus epilepsy. Pract Neurol 2018;18:447–454.
von Lehe M, Wagner J, Wellmer J, Clusmann H, Kral T. Epilepsy surgery of the cingulate gyrus and the frontomesial cortex. Neurosurgery 2012;70:900–910.
Chou C-C, Lee C-C, Lin CF, et al. Cingulate gyrus epilepsy: semiology, invasive EEG, and surgical approaches. Neurosurg Focus 2020;48:E8.
Kerezoudis P, Singh R, Worrell GA, Van Gompel JJ. Outcomes of cingulate epilepsy surgery: insights from an institutional and patient-level systematic review and meta-analysis. J Neurosurg 2022;137:199–208.
Alkawadri R, Mickey BE, Madden CJ, Van Ness PC. Cingulate gyrus epilepsy. Clinical and behavioral aspects, with surgical outcomes. Arch Neurol 2011;68:381–385.
Bancaud J, Talairach J. Clinical semiology of frontal lobe seizures. In: Chauvel P, Delgado Escueta AV, Halgren E, Bancaud J, eds. Advances in Neurology. Frontal Lobe Seizures and Epilepsies. New York: Raven Press, 1992; 3–58.
Oane I, Barborica A, Chetan F, et al. Cingulate cortex function and multi-modal connectivity mapped using intracranial stimulation. Neuroimage 2020;220:117059.
Jayakar P, Gotman J, Harvey AS, et al. Diagnostic utility of invasive EEG for epilepsy surgery: indications, modalities, and techniques. Epilepsia 2016;57:1735–1747.
Caruana F, Gerbella M, Avanzini P, et al. Motor and emotional behaviours elicited by electrical stimulation of the human cingulate cortex. Brain 2018;141:3035–3051.
Pelliccia V, Avanzini P, Rizzi M, et al. Association between semiology and anatomo-functional localization in patients with cingulate epilepsy. A cohort study. Neurology 2022;98:E2211–E2223.
Colombo N, Tassi L, Deleo F, et al. Focal cortical dysplasia type IIa and IIb: MRI aspects in 118 cases proven by histopathology. Neuroradiology 2012;54:1065–1077.
Cardinale F, Cossu M, Castana L, et al. Stereoelectroencephalography: surgical methodology, safety, and stereotactic application accuracy in 500 procedures. Neurosurgery 2013;72:353–366.
Cardinale F, Pero G, Quilici L, et al. Cerebral angiography for multimodal surgical planning in epilepsy surgery: description of a new three-dimensional technique and literature review. World Neurosurg 2015;84:358–367.
Cardinale F, Rizzi M, Vignati E, et al. Stereoelectroencephalography: retrospective analysis of 742 procedures in a single centre. Brain 2019;142:2688–2704.
Cardinale F, Rizzi M, D'Orio P, et al. A new tool for touch-free patient registration for robot-assisted intracranial surgery: application accuracy from a phantom study and a retrospective surgical series. Neurosurg Focus 2017;42:E8.
Fedorov A, Beichel R, Kalpathy-Cramer J, et al. 3D slicer as an image computing platform for the quantitative imaging network. Magn Reson Imaging 2012;30:1323–1341.
Narizzano M, Arnulfo G, Ricci S, et al. SEEG assistant: a 3D Slicer extension to support epilepsy surgery. BMC Bioinformatics 2017;18:124.
Arnulfo G, Narizzano M, Cardinale F, Fato MM, Palva JM. Automatic segmentation of deep intracerebral electrodes in computed tomography scans. BMC Bioinformatics 2015;16:99–12.
Engel J Jr, Van Ness PC, Rasmussen TB, Ojemann LM. Outcome with respect to epileptic seizures. In: Engel J Jr, ed. Surgical Treatment of the Epilepsies. New York: Raven Press, Ltd., 1993; 609–621.
Grant RL. Converting an odds ratio to a range of plausible relative risks for better communication of research findings. BMJ 2014;348:f7450.
R Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing, 2022. Available at: https://www.R-project.org/ . Accessed September 1, 2022.
Bannur U, Rajshekhar V. Post operative supplementary motor area syndrome: clinical features and outcome. Br J Neurosurg 2000;14:204–210.
Bonini F, McGonigal A, Scavarda D, et al. Predictive factors of surgical outcome in frontal lobe epilepsy explored with stereoelectroencephalography. Neurosurgery 2018;83:217–225.
Jehi LE, Morita-Sherman ME, Love TE, et al. Comparative effectiveness of stereotactic electroencephalography versus subdural grids in epilepsy surgery. Ann Neurol 2021;90:927–939.
Schmidt RF, Wu C, Lang MJ, et al. Complications of subdural and depth electrodes in 269 patients undergoing 317 procedures for invasive monitoring in epilepsy. Epilepsia 2016;57:1697–1708.
Arya R, Mangano FT, Horn PS, Holland KD, Rose DF, Glauser TA. Adverse events related to extraoperative invasive EEG monitoring with subdural grid electrodes: a systematic review and meta-analysis. Epilepsia 2013;54:828–839.
Harput MV, Gonzalez-Lopez P, Türe U. Three-Dimensional reconstruction of the topographical cerebral surface anatomy for presurgical planning with free OsiriX software. Oper Neurosurg 2014;10:426–435.
Nowell M, Rodionov R, Zombori G, et al. Utility of 3D multimodality imaging in the implantation of intracranial electrodes in epilepsy. Epilepsia 2015;56:403–413.
Nowell M, Rodionov R, Zombori G, et al. A pipeline for 3D multimodality image integration and computer-assisted planning in epilepsy surgery. J Vis Exp 2016;111:e53450.
Lo Russo G, Bhatia S, Ojemann JG. Extratemporal localization and eloquent areas. In: Arzimanoglou A, Cross JH, Gaillard WD, et al, eds. Pediatric Epilepsy Surgery. Montrouge: John Libbey & Company Ltd, 2016; 361–379.
Minkin K, Gabrovski K, Sirakov S, et al. Three-dimensional neuronavigation in SEEG-guided epilepsy surgery. Acta Neurochir 2019;161:917–923.
Horsley V. Brain-surgery. BMJ 1886;2:670–675.
Kelly PJ. Stereotactic navigation, Jean Talairach, and I. Neurosurgery 2004;54:454–464.
Hader WJ, Mackay M, Otsubo H, et al. Cortical dysplastic lesions in children with intractable epilepsy: role of complete resection. J Neurosurg 2004;100(suppl 2):110–117.
Fauser S, Bast T, Altenmüller DM, et al. Factors influencing surgical outcome in patients with focal cortical dysplasia. J Neurol Neurosurg Psychiatry 2008;79:103–105.
Fauser S, Essang C, Altenmüller DM, et al. Long-term seizure outcome in 211 patients with focal cortical dysplasia. Epilepsia 2015;56:66–76.
Krsek P, Maton B, Jayakar P, et al. Incomplete resection of focal cortical dysplasia is the main predictor of poor postsurgical outcome. Neurology 2009;72:217–223.
Jin B, Wang J, Zhou J, Wang S, Guan Y, Chen S. A longitudinal study of surgical outcome of pharmacoresistant epilepsy caused by focal cortical dysplasia. J Neurol 2016;263:2403–2410.
Choi SA, Kim SY, Kim H, et al. Surgical outcome and predictive factors of epilepsy surgery in pediatric isolated focal cortical dysplasia. Epilepsy Res 2018;139:54–59.
Choi SA, Kim KJ. Focal cortical dysplasia in pediatric epilepsy. Ann Child Neurol 2019;27:93–104.
Jayalakshmi S, Nanda S, Vooturi S, et al. Focal cortical dysplasia and refractory epilepsy: role of multimodality imaging and outcome of surgery. Am J Neuroradiol 2019;40:892–898.
Rácz A, Becker AJ, Quesada CM, et al. Post-surgical outcome and its determining factors in patients operated on with focal cortical dysplasia type II—a retrospective monocenter study. Front Neurol 2021;12:666056.
Salemdawod A, Wach J, Banat M, et al. Predictors of postoperative long-term seizure outcome in pediatric patients with focal cortical dysplasia type II at a German tertiary epilepsy center. J Neurosurg Pediatr 2022;29:83–91.
Widdess-Walsh P, Jeha L, Nair DR, Kotagal P, Bingaman WE, Najm IM. Subdural electrode analysis in focal cortical dysplasia: predictors of surgical outcome. Neurology 2007;69:660–667.
Cohen-Gadol AA, Ozduman K, Bronen RA, Kim JH, Spencer DD. Long-term outcome after epilepsy surgery for focal cortical dysplasia. J Neurosurg 2004;101:55–65.
Tassi L, Garbelli R, Colombo N, et al. Electroclinical, MRI and surgical outcomes in 100 epileptic patients with type II FCD. Epileptic Disord 2012;14:257–266.
Rao M, Chaturvedi J, Arivazhagan A, et al. Epilepsy surgery for focal cortical dysplasia: seizure and quality of life (QOLIE-89) outcomes. Neurol India 2018;66:1655–1666.
Cardinale F, Revay M, D'Orio P, et al. Surgery for FCD: principles and outcome. In: Chassoux F, Palmini A, eds. Focal Cortical Dysplasias. New Advances for Curing Epilepsy. London, Paris: John Libbey Eurotext, 2022; 203–222.
Lamberink HJ, Otte WM, Blümcke I, et al. Seizure outcome and use of antiepileptic drugs after epilepsy surgery according to histopathological diagnosis: a retrospective multicentre cohort study. Lancet Neurol 2020;19:748–757.
Savic I, Engel J Jr. Sex differences in patients with mesial temporal lobe epilepsy. J Neurol Neurosurg Psychiatry 1998;65:910–912.
Sun Y, Wang X, Che N, et al. Clinical characteristics and epilepsy outcomes following surgery caused by focal cortical dysplasia (Type IIa) in 110 adult epileptic patients. Exp Ther Med 2017;13:2225–2234.
Mazars G. Criteria for identifying cingulate epilepsies. Epilepsia 1970;11:41–47.
Cukiert A, Gronich G, Marino Jr R. Secondary bilateral synchrony associated to a parasagittal tumor. Case report. Arq Neuropsiquiatr 1991;49:333–337.
Enatsu R, Gonzalez-Martinez JA, Bulacio JC, et al. Connections of the limbic network: a corticocortical evoked potentials study. Cortex 2015;62:20–33.
Huppertz H-J, Grimm C, Fauser S, et al. Enhanced visualization of blurred gray-white matter junctions in focal cortical dysplasia by voxel-based 3D MRI analysis. Epilepsy Res 2005;67:35–50.
Wagner J, Weber B, Urbach H, Elger CE, Huppertz H-J. Morphometric MRI analysis improves detection of focal cortical dysplasia type II. Brain 2011;134:2844–2854.
Cardinale F, Francione S, Gennari L, et al. SUrface-PRojected FLuid-attenuation-inversion-recovery analysis: a novel tool for advanced imaging of epilepsy. World Neurosurg 2017;98:715–726.e1.
Jin B, Krishnan B, Adler S, et al. Automated detection of focal cortical dysplasia type II with surface-based magnetic resonance imaging postprocessing and machine learning. Epilepsia 2018;59:982–992.
David B, Kröll-Seger J, Schuch F, et al. External validation of automated focal cortical dysplasia detection using morphometric analysis. Epilepsia 2021;62:1005–1021.
Sun K, Ren Z, Yang D, et al. Voxel-based morphometric MRI post-processing and PET/MRI co-registration reveal subtle abnormalities in cingulate epilepsy. Epilepsy Res 2021;171:106568.