Pediatric Intraoperative Neurophysiologic Mapping and Monitoring in Brain Surgery.
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 Feb 2024
01 Feb 2024
Historique:
medline:
2
2
2024
pubmed:
2
2
2024
entrez:
2
2
2024
Statut:
ppublish
Résumé
Similar to adults, children undergoing brain surgery can significantly benefit from intraoperative neurophysiologic mapping and monitoring. Although young brains present the advantage of increased plasticity, during procedures in close proximity to eloquent regions, the risk of irreversible neurological compromise remains and can be lowered further by these techniques. More so, pathologies specific to the pediatric population, such as neurodevelopmental lesions, often result in medically refractory epilepsy. Thus, their successful surgical treatment also relies on accurate demarcation and resection of the epileptogenic zone, processes in which intraoperative electrocorticography is often employed. However, stemming from the development and maturation of the central and peripheral nervous systems as the child grows, intraoperative neurophysiologic testing in this population poses methodologic and interpretative challenges even to experienced clinical neurophysiologists. For example, it is difficult to perform awake craniotomies and language testing in the majority of pediatric patients. In addition, children may be more prone to intraoperative seizures and exhibit afterdischarges more frequently during functional mapping using electrical cortical stimulation because of high stimulation thresholds needed to depolarize immature cortex. Moreover, choice of anesthetic regimen and doses may be different in pediatric patients, as is the effect of these drugs on immature brain; these factors add additional complexity in terms of interpretation and analysis of neurophysiologic recordings. Below, we are describing the modalities commonly used during intraoperative neurophysiologic testing in pediatric brain surgery, with emphasis on age-specific clinical indications, methodology, and challenges.
Identifiants
pubmed: 38306217
doi: 10.1097/WNP.0000000000001054
pii: 00004691-202402000-00002
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
96-107Informations de copyright
Copyright © 2024 by the American Clinical Neurophysiology Society.
Déclaration de conflit d'intérêts
The authors have no funding or conflicts of interest to disclose.
Références
Galloway GM, Zamel K. Neurophysiologic intraoperative monitoring in pediatrics. Pediatr Neurol 2011;44:161–170.
Gallentine WB, Mikati MA. Intraoperative electrocorticography and cortical stimulation in children. J Clin Neurophysiol 2009;26:95–108.
Matamala JM, Butler W, Simon MV. Intraoperative neurophysiologic monitoring and mapping in pediatric population. In: Simon MV, ed. Intraoperative neurophysiology: a comprehensive guide to monitoring and mapping. New York: Springer/Demos Medical, 2019; 245–283.
Brody BA, Kinney HC, Kloman AS, Gilles FH. Sequence of central nervous system myelination in human infancy. I. An autopsy study of myelination. J Neuropathol Exp Neurol 1987;46:283–301.
Ratha V, Sampath N, Subramaniam S, Kumar VRR. Technical considerations in awake craniotomy with cortical and subcortical motor mapping in preadolescents: pushing the envelope. Pediatr Neurosurg 2021;56:171–178.
Sala F, Krzan MJ, Deletis V. Intraoperative neurophysiological monitoring in pediatric neurosurgery: why, when, how? Childs Nerv Syst 2002;18:264–287.
Zea Vera A, Aungaroon G, Horn PS, et al. Language and motor function thresholds during pediatric extra-operative electrical cortical stimulation brain mapping. Clin Neurophysiol 2017;128:2087–2093.
Lüders HO, Najm I, Nair D, Widdess-Walsh P, Bingman W. The epileptogenic zone: general principles. Epileptic Disord 2006;8(suppl 2):S1–S9.
Penfield W, Jasper H. Epilepsy and the functional anatomy of the human brain. 1st ed. Boston: Little, Brown, 1954.
Macdonald DB, Pillay N. Intraoperative electrocorticography in temporal lobe epilepsy surgery. Can J Neurol Sci 2000;27(suppl 1):S85–S91; discussion S92–S96.
Greiner HM, Horn PS, Tenney JR, et al. Preresection intraoperative electrocorticography (ECoG) abnormalities predict seizure-onset zone and outcome in pediatric epilepsy surgery. Epilepsia 2016;57:582–589.
Trébuchon A, Chauvel P. Electrical stimulation for seizure induction and functional mapping in stereoelectroencephalography. J Clin Neurophysiol 2016;33:511–521.
Ntsambi-Eba G, Vaz G, Docquier M-A, Van Rijckevorsel K, Raftopoulos C. Patients with refractory epilepsy treated using a modified multiple subpial transection technique. Neurosurgery 2013;72:890–897; discussion 897–898.
Binnie CD, McBride MC, Polkey CE, Sawhney IM, Janota I. Electrocorticography and stimulation. Acta Neurol Scand Suppl 1994;152:74–82.
Lin J, Kwan S. Post-section recruitment of epileptiform discharges in electrocorticography during callosotomy in 48 patients with Lennox–Gastaut syndrome. J Clin Neurosci 2012;19:388–393.
Simon MV. Electrocorticography in nonepilepsy surgery. In: Simon MV, ed. Intraoperative neurophysiology: a comprehensive guide to monitoring and mapping. New York: Springer/Demos Medical, 2019; 208–233.
Simon MV. Intraoperative neurophysiologic sensorimotor mapping and monitoring in supratentorial surgery. J Clin Neurophysiol 2013;30:571–590.
Simon MV. Mapping and monitoring of motor and primary sensory functions. In: Simon MV, ed. Intraoperative neurophysiology: a comprehensive guide to monitoring and mapping. New York: Springer/Demos, 2019; 245–283.
Simon MV, Nuwer MR, Szelenyi A. EEG, ECOG and cortical stimulation techniques. In: Nuwer MR, MacDonald D, eds. Handbook of clinical neurology. Amsterdam: Elsevier, 2022; 10–38.
Simon MV, Eskandar EN, Cole AJ. Intraoperative electrography in epilepsy surgery. In: Simon MV, ed. Intraoperative neurophysiology: a comprehensive guide to monitoring and mapping. New York: Springer/Demos Medical, 2019; 173–207.
Demuru M, Kalitzin S, Zweiphenning W, et al. The value of intraoperative electrographic biomarkers for tailoring during epilepsy surgery: from group level to patient-level analysis. Sci Rep 2020;10:14654.
Motoi H, Miyakoshi M, Abel TJ, et al. Phase-amplitude coupling between interictal high-frequency activity and slow waves in epilepsy surgery. Epilepsia 2018;59:1954–1965.
van 't Klooster MA, van Klink NEC, Leijten FSS, et al. Residual fast ripples in the intraoperative corticogram predict epilepsy surgery outcome. Neurology 2015;85:120–128.
Cepeda C, Levinson S, Nariai H, et al. Pathological high frequency oscillations associate with increased GABA synaptic activity in pediatric epilepsy surgery patients. Neurobiol Dis 2020;134:104618.
Gelinas JN, Battison AW, Smith S, Connolly MB, Steinbok P. Electrocorticography and seizure outcomes in children with lesional epilepsy. Childs Nerv Syst 2011;27:381–390.
Hirsch J, Sainte Rose C, Pierre-Kahn A, Pfister A, Hoppe-Hirsch E. Benign astrocytic and oligodendrocytic tumors of the cerebral hemispheres in children. J Neurosurg 1989;70:568–572.
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;16:120–127.
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;79:62–69.
Hu W, Ge M, Zhang K, Meng F, Zhang J. Seizure outcome with surgical management of epileptogenic ganglioglioma: a study of 55 patients. Acta Neurochir 2012;154:855–861.
Awad IA, Rosenfeld J, Ahl J, Hahn JF, Luders H. Intractable epilepsy and structural lesions of the brain: mapping, resection strategies, and seizure outcome. Epilepsia 1991;32:179–186.
Southwell DG, Garcia PA, Berger MS, Barbaro NM, Chang EF. Long-term seizure control outcomes after resection of gangliogliomas. Neurosurgery 2012;70:1406–1413; discussion 1413–1414.
Wyllie E, Luders H, Morris HH, et al. Clinical outcome after complete or partial cortical resection for intractable epilepsy. Neurology 1987;37:1634–1641.
Qiu B, Ou S, Song T, 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;16:175–184.
Gump WC, Skjei KL, Karkare SN. Seizure control after subtotal lesional resection. Neurosurg Focus 2013;34:E1.
Englot DJ, Berger MS, Barbaro NM, Chang EF. Predictors of seizure freedom after resection of supratentorial low-grade gliomas: a review. J Neurosurg 2011;115:240–244.
Ogiwara H, Nordli DR, DiPatri AJ, Alden TD, Bowman RM, Tomita T. Pediatric epileptogenic gangliogliomas: seizure outcome and surgical results. J Neurosurg Pediatr 2010;5:271–276.
Prayson RA, Estes ML, Morris HH. Coexistence of neoplasia and cortical dysplasia in patients presenting with seizures. Epilepsia 1993;34:609–615.
Prayson RA, Napekoski KM. Composite ganglioglioma/dysembryoplastic neuroepithelial tumor: a clinicopathologic study of 8 cases. Hum Pathol 2012;43:1113–1118.
Yao P, Zheng S, Wang F, Kang D, Lin Y. Surgery guided with intraoperative electrocorticography in patients with low-grade glioma and refractory seizures. J Neurosurg 2018;128:840–845.
Roessler K, Heynold E, Buchfelder M, Stefan H, Hamer HM. Current value of intraoperative electrocorticography (iopECoG). Epilepsy Behav 2018;91:20–24.
Severino M, Geraldo AF, Utz N, et al. Definitions and classification of malformations of cortical development: practical guidelines. Brain 2020;143:2874–2894.
Gröppel G, Dorfer C, Samueli S, et al. Single stage epilepsy surgery in children and adolescents with focal cortical dysplasia type II–prognostic value of the intraoperative electrocorticogram. Clin Neurophysiol 2019;130:20–24.
Terra VC, Thomé U, Rosset SS, et al. Surgery for focal cortical dysplasia in children using intraoperative mapping. Childs Nerv Syst 2014;30:1839–1851.
Tamburrini G, Battaglia D, Albamonte E, et al. Surgery for posterior quadrantic cortical dysplasia: a review. Childs Nerv Syst 2014;30:1859–1868.
Major P, Rakowski S, Simon MV, et al. Are cortical tubers epileptogenic? Epilepsia 2009;50:147–154.
Cusmai R, Chiron C, Curatolo P, Dulac O, Tran-Dinh S. Topographic comparative study of magnetic resonance imaging and electroencephalography in 34 children with tuberous sclerosis. Epilepsia 1990;31:747–755.
Kamimura T, Tohyama J, Oishi M, et al. Magnetoencephalography in patients with tuberous sclerosis and localization-related epilepsy. Epilepsia 2006;47:991–997.
Madhavan D, Weiner HL, Carlson C, Devinsky O, Kuzniecky R. Local epileptogenic networks in tuberous sclerosis complex: a case review. Epilepsy Behav 2007;11:140–146.
Ma TS, Elliott RE, Ruppe V, et al. Electrocorticographic evidence of perituberal cortex epileptogenicity in tuberous sclerosis complex. J Neurosurg Pediatr 2012;10:376–382.
Guerreiro MM, Andermann F, Andermann E, et al. Surgical treatment of epilepsy in tuberous sclerosis: strategic and results in 18 patients. Neurology 1998;51:1263–1269.
Koh S, Jayakar P, Dunoyer C, et al. Epilepsy surgery in children with tuberous sclerosis complex: presurgical evaluation and outcome. Epilepsia 2000;41:1206–1213.
Van Gompel JJ, Rubio J, Cascino GD, Worrell GA, Meyer FB. Electrocorticography-guided resection of temporal cavernoma: is electrocorticography warranted and does it alter the surgical approach? J Neurosurg 2009;110:1179–1185.
Vale FL, Vivas AC, Manwaring J, Schoenberg MR, Benbadis SR. Temporal lobe epilepsy and cavernous malformations: surgical strategies and long-term outcomes. Acta Neurochir 2015;157:1887–1895; discussion 1895.
Wyllie E, Comair YG, Kotagal P, Bulacio J, Bingaman W, Ruggieri P. Seizure outcome after epilepsy surgery in children and adolescents. Ann Neurol 1998;44:740–748.
Mcbride MC, Binnie CD, Janota I, Polkey CE. Predictive value of intraoperative electrocorticograms in resective epilepsy surgery. Ann Neurol 1991;30:526–532.
Greiner HM, Horn PS, Tenney JR, et al. Should spikes on post-resection ECoG guide pediatric epilepsy surgery? Epilepsy Res 2016;122:73–78.
Sommer B, Rampp S, Doerfler A, et al. Investigation of subdural electrode displacement in invasive epilepsy surgery workup using neuronavigation and intraoperative MRI. Neurol Res 2018;40:811–821.
Foldes ST, Munter BT, Appavu BL, Kerrigan JF, Adelson PD. Shift in electrocorticography electrode locations after surgical implantation in children. Epilepsy Res 2020;167:106410.
Nuwer MR, Schuele S. Electrocorticography. In: Schomer D, Lopes da Silva F, eds. Niedermeyer's electroencephalography. 7th ed. New York: Oxford University Press, 2018; 771–780.
El Tahry R, Ferrao Santos S, de Tourtchaninoff M, et al. Post-resection electrocorticography has no added value in epilepsy surgery. Acta Neurol Belg 2016;116:279–285.
Wray CD, McDaniel SS, Saneto RP, Novotny EJ Jr, Ojemann JG. Is postresective intraoperative electrocorticography predictive of seizure outcomes in children? J Neurosurg Pediatr 2012;9:546–551.
Schwartz TH, Bazil CW, Forgione M, Bruce JN, Goodman RR. Do reactive post-resection “injury” spikes exist? Epilepsia 2000;41:1463–1468.
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.
Bindra A, Chouhan RS, Prabhakar H, Dash HH, Chandra PS, Tripathi M. Comparison of the effects of different anesthetic techniques on electrocorticography in patients undergoing epilepsy surgery – a bispectral index guided study. Seizure 2012;21:501–507.
Asano E, Benedek K, Shah A, et al. Is intraoperative electrocorticography reliable in children with intractable neocortical epilepsy? Epilepsia 2004;45:1091–1099.
Smith M, Smith SJ, Scott CA, Harkness WF. Activation of the electrocorticogram by propofol during surgery for epilepsy. Br J Anaesth 1996;76:499–502.
Schneider F, Herzer W, Schroeder HWS, et al. Effects of propofol on electrocorticography in patients with intractable partial epilepsy. J Neurosurg Anesthesiol 2011;23:150–155.
Kjaer TW, Hogenhaven H, Lee AP, et al. Pharmacodynamics of remifentanil. Induced intracranial spike activity in mesial temporal lobe epilepsy. Epilepsy Res 2017;133:41–45.
Ragazzo PC, Galanopoulou AS. Alfentanil-induced activation: a promising tool in the presurgical evaluation of temporal lobe epilepsy patients. Brain Res Brain Res Rev 2000;32:316–327.
Bhaskar N, Thakkar KD, Sharma S, Hrishi AP. Dexmedetomidine for electrocorticography in patients with Lennox–Gastaut syndrome presenting for epilepsy surgery: a case report. A A Pract 2019;13:148–150.
Hufnagel A, Burr W, Elger CE, Nadstawek J, Hefner G. Localization of the epileptic focus during methohexital-induced anesthesia. Epilepsia 1992;33:271–284.
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.
Jayakar P, Alvarez LA, Duchowny MS, Resnick TJ. A safe and effective paradigm to functionally map the cortex in childhood. J Clin Neurophysiol 1992;9:288–293.
Alsallom F, Simon MV. Giant somatosensory evoked potentials in focal epilepsy secondary to glioblastoma multiforme. Neurohospitalist 2023;13:202–203.
Dineen J, Maus DC, Muzyka I, et al. Factors that modify the risk of intraoperative seizures triggered by electrical stimulation during supratentorial functional mapping. Clin Neurophysiol 2019;130:1058–1065.
Simon MV, Cole AJ, Chang EC, et al. An intraoperative multimodal neurophysiologic approach to successful resection of precentral gyrus epileptogenic lesions. Epilepsia 2012;53:e75–e79.