Awake brain surgery for language mapping in pediatric patients: a single-center experience

View More View Less
  • 1 Departments of Neurosurgery,
  • | 2 Neurology,
  • | 3 Pediatrics and Adolescent Medicine, and
  • | 4 Radiology, Medical University of Vienna, Austria
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $515.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $612.00
Print or Print + Online Sign in

OBJECTIVE

The goal of this study was to evaluate the feasibility, benefit, and safety of awake brain surgery (ABS) and intraoperative language mapping in children and adolescents with structural epilepsies. Whereas ABS is an established method to monitor language function in adults intraoperatively, reports of ABS in children are scarce.

METHODS

A retrospective chart review of pediatric patients ≤ 18 years of age who underwent ABS and cortical language mapping for supratentorial tumors and nontumoral epileptogenic lesions between 2008 and 2019 was conducted. The authors evaluated the global intellectual and specific language performance by using detailed neuropsychological testing, the patient’s intraoperative compliance, results of intraoperative language mapping assisted by electrocorticography (ECoG), and postsurgical language development and seizure outcomes. Descriptive statistics were used for this study, with a statistical significance of p < 0.05.

RESULTS

Eleven children (7 boys) with a median age of 13 years (range 10–18 years) underwent ABS for a lesion in close vicinity to cortical language areas as defined by structural and functional MRI (left hemisphere in 9 children, right hemisphere in 2). Patients were neurologically intact but experiencing seizures; these were refractory to therapy in 9 patients. Compliance during the awake phase was high in 10 patients and low in 1 patient. Cortical mapping identified eloquent language areas in 6/10 (60%) patients and was concordant in 3/8 (37.5%), discordant in 3/8 (37.5%), and unclear in 2/8 (25%) patients compared to preoperative functional MRI. Stimulation-induced seizures occurred in 2 patients and could be interrupted easily. ECoG revealed that afterdischarge potentials (ADP) were involved in 5/9 (56%) patients with speech disturbances during stimulation. None of these patients harbored postoperative language dysfunction. Gross-total resection was achieved in 10/11 (91%) patients, and all were seizure free after a median follow-up of 4.3 years. Neuropsychological testing using the Wechsler Intelligence Scale for Children and the verbal learning and memory test showed an overall nonsignificant trend toward an immediate postoperative deterioration followed by an improvement to above preoperative levels after 1 year.

CONCLUSIONS

ABS is a valuable technique in selected pediatric patients with lesions in language areas. An interdisciplinary approach, careful patient selection, extensive preoperative training of patients, and interpretation of intraoperative ADP are pivotal to a successful surgery.

ABBREVIATIONS

ABS = awake brain surgery; ADP = afterdischarge potentials; CBCL = Child Behavior Checklist; DFR = delayed free recall; DNET = dysembryoplastic neuroepithelial tumor; ECoG = electrocorticography; EOR = extent of resection; FCD = focal cortical dysplasia; fMRI = functional MRI; GIA = general intellectual ability; GTR = gross-total resection; IFR = immediate free recall; mMCD = mild malformation of cortical development; SE = strip electrode; STR = subtotal resection; VC = verbal comprehension; VLMT = verbal learning and memory test; VLP = verbal learning performance; WISC = Wechsler Intelligence Scale for Children.

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $515.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $612.00
  • 1

    Penfield W. The cerebral cortex in man. Arch Neurol Psychiatry. 1938;40(3):417442.

  • 2

    Penfield W, Roberts L. Speech and Brain-Mechanisms. Princeton University Press;1959.

  • 3

    Penfield W, Jasper HH. Epilepsy and the Functional Anatomy of the Human Brain. 1st ed. Little;1954.

  • 4

    Surbeck W, Hildebrandt G, Duffau H. The evolution of brain surgery on awake patients. Acta Neurochir (Wien). 2015;157(1):7784.

  • 5

    Berger MS, Ojemann GA. Intraoperative brain mapping techniques in neuro-oncology. Stereotact Funct Neurosurg. 1992;58(1-4):153161.

  • 6

    Duffau H. Contribution of cortical and subcortical electrostimulation in brain glioma surgery: methodological and functional considerations. Neurophysiol Clin. 2007;37(6):373382.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Bartha-Doering L, Kollndorfer K, Kasprian G, et al. Weaker semantic language lateralization associated with better semantic language performance in healthy right-handed children. Brain Behav. 2018;8(11):e01072.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Lux S, Helmstaedter C, Elger CE. Normierungsstudie zum Verbalen Lern- und Merkfähigkeitstest (VLMT). Diagnostica. 1999;45(4):205211.

  • 9

    Wechsler D. Wechsler. Intelligence Scale for Children. 4th ed. Pearson;2003.

  • 10

    Wechsler D. Wechsler. Intelligence Scale for Children. 5th ed. Pearson;2014.

  • 11

    Wieser HG, Blume WT, Fish D, et al. ILAE Commission Report. Proposal for a new classification of outcome with respect to epileptic seizures following epilepsy surgery. Epilepsia. 2001;42(2):282286.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Morshed RA, Young JS, Lee AT, Berger MS, Hervey-Jumper SL. Clinical pearls and methods for intraoperative awake language mapping. Neurosurgery. 2020.

    • Search Google Scholar
    • Export Citation
  • 13

    Nossek E, Matot I, Shahar T, et al. Failed awake craniotomy: a retrospective analysis in 424 patients undergoing craniotomy for brain tumor. J Neurosurg. 2013;118(2):243249.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Nossek E, Matot I, Shahar T, et al. Intraoperative seizures during awake craniotomy: incidence and consequences: analysis of 477 patients. Neurosurgery. 2013;73(1):135140.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Eseonu CI, Rincon-Torroella J, ReFaey K, et al. Awake craniotomy vs craniotomy under general anesthesia for perirolandic gliomas: evaluating perioperative complications and extent of resection. Neurosurgery. 2017;81(3):481489.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Pereira LC, Oliveira KM, L’Abbate GL, Sugai R, Ferreira JA, da Motta LA. Outcome of fully awake craniotomy for lesions near the eloquent cortex: analysis of a prospective surgical series of 79 supratentorial primary brain tumors with long follow-up. Acta Neurochir (Wien). 2009;151(10):12151230.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17

    Balogun JA, Khan OH, Taylor M, et al. Pediatric awake craniotomy and intra-operative stimulation mapping. J Clin Neurosci. 2014;21(11):18911894.

  • 18

    Duffau H, Peggy Gatignol ST, Mandonnet E, Capelle L, Taillandier L. Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with Grade II glioma in the left dominant hemisphere. J Neurosurg. 2008;109(3):461471.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19

    Ritaccio AL, Brunner P, Schalk G. Electrical stimulation mapping of the brain: basic principles and emerging alternatives. J Clin Neurophysiol. 2018;35(2):8697.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Santini B, Talacchi A, Casagrande F, et al. Eligibility criteria and psychological profiles in patient candidates for awake craniotomy: a pilot study. J Neurosurg Anesthesiol. 2012;24(3):209216.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Trevisi G, Roujeau T, Duffau H. Awake surgery for hemispheric low-grade gliomas: oncological, functional and methodological differences between pediatric and adult populations. Childs Nerv Syst. 2016;32(10):18611874.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Delion M, Terminassian A, Lehousse T, et al. Specificities of awake craniotomy and brain mapping in children for resection of supratentorial tumors in the language area. World Neurosurg. 2015;84(6):16451652.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Lohkamp LN, Mottolese C, Szathmari A, et al. Awake brain surgery in children-review of the literature and state-of-the-art. Childs Nerv Syst. 2019;35(11):20712077.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Berger M. The impact of technical adjuncts in the surgical management of cerebral hemispheric low-grade gliomas of childhood. J Neurooncol. 1996;28(2-3):129155.

  • 25

    Klimek M, Verbrugge SJ, Roubos S, van der Most E, Vincent AJ, Klein J. Awake craniotomy for glioblastoma in a 9-year-old child. Anaesthesia. 2004;59(6):607609.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26

    Riquin E, Martin P, Duverger P, Menei P, Delion M. A case of awake craniotomy surgery in an 8-year-old girl. Childs Nerv Syst. 2017;33(7):10391042.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27

    Ojemann SG, Berger MS, Lettich E, Ojemann GA. Localization of language function in children: results of electrical stimulation mapping. J Neurosurg. 2003;98(3):465470.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Herta J, Yildiz E, Marhofer D, et al. Feasibility of intraoperative motor evoked potential monitoring during tethered cord surgery in infants younger than 12 months. Childs Nerv Syst. 2022;38(2):397405.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Murcia D, D’Souza S, Abozeid M, Thompson JA, Djoyum TD, Ormond DR. Investigation of asleep versus awake motor mapping in resective brain surgery. World Neurosurg. 2022;157:e129e136.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Ho A, Khan Y, Fischberg G, Mahato D. Clinical application of brain plasticity in neurosurgery. World Neurosurg. 2021;146:3139.

  • 31

    Roland JL, Griffin N, Hacker CD, et al. Resting-state functional magnetic resonance imaging for surgical planning in pediatric patients: a preliminary experience. J Neurosurg Pediatr. 2017;20(6):583590.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Giussani C, Roux FE, Ojemann J, Sganzerla EP, Pirillo D, Papagno C. Is preoperative functional magnetic resonance imaging reliable for language areas mapping in brain tumor surgery? Review of language functional magnetic resonance imaging and direct cortical stimulation correlation studies. Neurosurgery. 2010;66(1):113120.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Prada F, Del Bene M, Mattei L, et al. Preoperative magnetic resonance and intraoperative ultrasound fusion imaging for real-time neuronavigation in brain tumor surgery. Ultraschall Med. 2015;36(2):174186.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Silva MA, See AP, Essayed WI, Golby AJ, Tie Y. Challenges and techniques for presurgical brain mapping with functional MRI. Neuroimage Clin. 2017;17:794803.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Schmid E, Thomschewski A, Taylor A, et al. Diagnostic accuracy of functional magnetic resonance imaging, Wada test, magnetoencephalography, and functional transcranial Doppler sonography for memory and language outcome after epilepsy surgery: a systematic review. Epilepsia. 2018;59(12):23052317.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Matsumoto R, Nair DR, LaPresto E, et al. Functional connectivity in the human language system: a cortico-cortical evoked potential study. Brain. 2004;127(Pt 10):23162330.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Tamura Y, Ogawa H, Kapeller C, et al. Passive language mapping combining real-time oscillation analysis with cortico-cortical evoked potentials for awake craniotomy. J Neurosurg. 2016;125(6):15801588.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Yamao Y, Suzuki K, Kunieda T, et al. Clinical impact of intraoperative CCEP monitoring in evaluating the dorsal language white matter pathway. Hum Brain Mapp. 2017;38(4):19771991.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Wang Y, Fifer MS, Flinker A, et al. Spatial-temporal functional mapping of language at the bedside with electrocorticography. Neurology. 2016;86(13):11811189.

  • 40

    Aron O, Jonas J, Colnat-Coulbois S, Maillard L. Language mapping using stereo electroencephalography: a review and expert opinion. Front Hum Neurosci. 2021;15:619521.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41

    Gil Robles S, Gelisse P, Vergani F, et al. Discrepancies between preoperative stereoencephalography language stimulation mapping and intraoperative awake mapping during resection of focal cortical dysplasia in eloquent areas. Stereotact Funct Neurosurg. 2008;86(6):382390.

    • Crossref
    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 1220 1220 171
Full Text Views 126 126 7
PDF Downloads 129 129 6
EPUB Downloads 0 0 0