A 360° electronic device for recording high-resolution intraoperative electrocorticography of the brain during awake craniotomy

Restricted access

OBJECTIVE

Epilepsy is common among patients with supratentorial brain tumors; approximately 40%–70% of patients with glioma develop brain tumor–related epilepsy (BTRE). Intraoperative localization of the epileptogenic zone during surgical tumor resection (real-time data) may improve intervention techniques in patients with lesional epilepsy, including BTRE. Accurate localization of the epileptogenic signals requires electrodes with high-density spatial organization that must be placed on the cortical surface during surgery. The authors investigated a 360° high-density ring-shaped cortical electrode assembly device, called the “circular grid,” that allows for simultaneous tumor resection and real-time electrophysiology data recording from the brain surface.

METHODS

The authors collected data from 99 patients who underwent awake craniotomy from January 2008 to December 2018 (29 patients with the circular grid and 70 patients with strip electrodes), of whom 50 patients were matched-pair analyzed (25 patients with the circular grid and 25 patients with strip electrodes). Multiple variables were then retrospectively assessed to determine if utilization of this device provides more accurate real-time data and improves patient outcomes.

RESULTS

Matched-pair analysis showed higher extent of resection (p = 0.03) and a shorter transient motor recovery period during the hospitalization course (by approximately 6.6 days, p ≤ 0.05) in the circular grid patients. Postoperative versus preoperative Karnofsky Performance Scale (KPS) score difference/drop was greater for the strip electrode patients (p = 0.007). No significant difference in postoperative seizures between the 2 groups was present (p = 0.80).

CONCLUSIONS

The circular grid is a safe, feasible tool that grants direct access to the cortical surgical surface for tissue resection while simultaneously monitoring electrical activity. Application of the circular grid to different brain pathologies may improve intraoperative epileptogenic detection accuracy and functional outcomes, while decreasing postoperative complications.

ABBREVIATIONS AD = afterdischarge; ECoG = electrocorticography; EOR = extent of resection; HD = high-density; KPS = Karnofsky Performance Scale; LOS = length of hospital stay.

Article Information

Correspondence Alfredo Quiñones-Hinojosa: Mayo Clinic, Jacksonville, FL. quinones@mayo.edu.

INCLUDE WHEN CITING Published online July 5, 2019; DOI: 10.3171/2019.4.JNS19261.

Disclosures Drs. Tatum, Quiñones-Hinojosa, and ReFaey filed a patent disclosing this device and technology (patent application no. PCT/US2018/039956).

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Left: Diagram showing the circular grid. Right: Diagram showing the modular model of the circular grid.

  • View in gallery

    A 3D reconstruction of a brain image highlighting the spatial organization and dynamic ability of the circular grid. A: Pre-resection recording using the circular grid. B: Simultaneous 360° continuous monitoring during resection of the tumors/lesions. C: Post-resection recording for any residual epileptogenic foci from different sites of the surrounding tumor bed. Figure is available in color online only.

  • View in gallery

    A: Reconstructed brain image showing the fine motor cortex in blue and the lesion in red with the circular grid being used over the lesion for a 360° monitoring. B: Minor corridor corticectomy surrounded by the cortical and subcortical eloquent brain areas. C: ECoG recording with extended time scale showing epileptogenic activity highlighted in blue. D: ECoG showing the detection of epileptiform discharges with an increase in the periodicity in the green region. Figure is available in color online only.

References

  • 1

    Almeida ANMartinez VFeindel W: The first case of invasive EEG monitoring for the surgical treatment of epilepsy: historical significance and context. Epilepsia 46:108210852005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Arechiga NReFaey KRincon-Torroella JChaichana KQuiñones-Hinojosa A: Cortical/subcortical motor mapping for gliomas in Quiñones-Hinojosa A (ed): Video Atlas of Neurosurgery: Contemporary Tumor and Skull Base Surgery. Philadelphia: Elsevier2016Vol 1

    • Search Google Scholar
    • Export Citation
  • 3

    Berger MS: Functional mapping-guided resection of low-grade gliomas. Clin Neurosurg 42:4374521995

  • 4

    Berger MSKincaid JOjemann GALettich E: Brain mapping techniques to maximize resection, safety, and seizure control in children with brain tumors. Neurosurgery 25:7867921989

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Berger MSOjemann GA: Intraoperative brain mapping techniques in neuro-oncology. Stereotact Funct Neurosurg 58:1531611992

  • 6

    Berger MSOjemann GALettich E: Neurophysiological monitoring during astrocytoma surgery. Neurosurg Clin N Am 1:65801990

  • 7

    Blumcke ISpreafico RHaaker GCoras RKobow KBien CG: Histopathological findings in brain tissue obtained during epilepsy surgery. N Engl J Med 377:164816562017

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

    Brunner PRitaccio ALLynch TMEmrich JFWilson JAWilliams JC: A practical procedure for real-time functional mapping of eloquent cortex using electrocorticographic signals in humans. Epilepsy Behav 15:2782862009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Chaichana KLCabrera-Aldana EEJusue-Torres IWijesekera OOlivi ARahman M: When gross total resection of a glioblastoma is possible, how much resection should be achieved? World Neurosurg 82:e257e2652014

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10

    Chaichana KLJusue-Torres ILemos AMGokaslan ACabrera-Aldana EEAshary A: The butterfly effect on glioblastoma: is volumetric extent of resection more effective than biopsy for these tumors? J Neurooncol 120:6256342014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Chaichana KLJusue-Torres INavarro-Ramirez RRaza SMPascual-Gallego MIbrahim A: Establishing percent resection and residual volume thresholds affecting survival and recurrence for patients with newly diagnosed intracranial glioblastoma. Neuro Oncol 16:1131222014

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

    Cho JRKoo DLJoo EYSeo DWHong SCJiruska P: Resection of individually identified high-rate high-frequency oscillations region is associated with favorable outcome in neocortical epilepsy. Epilepsia 55:187218832014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    de Bittencourt PRSandmann MCMoro MSde Araújo JC: Simple, cost-effective technique for portable digital eletrocorticography. Arq Neuropsiquiatr 58 (2B):4244272000

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14

    Engel J Jr: The etiologic classification of epilepsy. Epilepsia 52:119511971205–1209 2011

  • 15

    Eseonu CIEguia FReFaey KGarcia ORodriguez FJChaichana K: Comparative volumetric analysis of the extent of resection of molecularly and histologically distinct low grade gliomas and its role on survival. J Neurooncol 134:65742017

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

    Eseonu CIReFaey KGarcia ORaghuraman GQuinones-Hinojosa A: Volumetric analysis of extent of resection, survival, and surgical outcomes for insular gliomas. World Neurosurg 103:2652742017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Eseonu CIRincon-Torroella JLee YM: ReFaey KTripathi PQuinones-Hinojosa A: Intraoperative seizures in awake craniotomy for perirolandic glioma resections that undergo cortical mapping. J Neurol Surg A Cent Eur Neurosurg 79:2392462018

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18

    Eseonu CIRincon-Torroella JReFaey KLee YMNangiana JVivas-Buitrago T: Awake craniotomy vs craniotomy under general anesthesia for perirolandic gliomas: evaluating perioperative complications and extent of resection. Neurosurgery 81:4814892017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Feyissa AMWorrell GATatum WOMahato DBrinkmann BHRosenfeld SS: High-frequency oscillations in awake patients undergoing brain tumor-related epilepsy surgery. Neurology 90:e1119e11252018

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20

    Formaggio EStorti SFTramontano VCasarin ABertoldo AFiaschi A: Frequency and time-frequency analysis of intraoperative ECoG during awake brain stimulation. Front Neuroeng 6:12013

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

    Haglund MMBerger MSShamseldin MLettich EOjemann GA: Cortical localization of temporal lobe language sites in patients with gliomas. Neurosurgery 34:5675761994

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Hervey-Jumper SLLi JLau DMolinaro AMPerry DWMeng L: Awake craniotomy to maximize glioma resection: methods and technical nuances over a 27-year period. J Neurosurg 123:3253392015

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23

    Kwan PArzimanoglou ABerg ATBrodie MJAllen Hauser WMathern G: Definition of drug resistant epilepsy: consensus proposal by the ad hoc Task Force of the ILAE Commission on Therapeutic Strategies. Epilepsia 51:106910772010

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

    Kwan PBrodie MJ: Early identification of refractory epilepsy. N Engl J Med 342:3143192000

  • 25

    Lara-Velazquez MAl-Kharboosh RJeanneret SVazquez-Ramos CMahato DTavanaiepour D: Advances in brain tumor surgery for glioblastoma in adults. Brain Sci 7:E1662017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Lima GLODezamis ECorns RRigaux-Viode OMoritz-Gasser SRoux A: Surgical resection of incidental diffuse gliomas involving eloquent brain areas. Rationale, functional, epileptological and oncological outcomes. Neurochirurgie 63:2502582017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Louis DNOhgaki HWiestler ODCavenee WKBurger PCJouvet A: The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114:971092007

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

    Marks WJ: Invasive clinical neurophysiology in epilepsy and movement disorders in Aminoff MJ (ed): Aminoff’s Electrodiagnosis in Clinical Neurology ed 6. Philadelphia: Saunders2012

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29

    Merrill DRBikson MJefferys JG: Electrical stimulation of excitable tissue: design of efficacious and safe protocols. J Neurosci Methods 141:1711982005

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

    Mostofa AGPunganuru SRMadala HRAl-Obaide MSrivenugopal KS: The process and regulatory components of inflammation in brain oncogenesis. Biomolecules 7:E342017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Nossek EMatot IShahar TBarzilai ORapoport YGonen T: Intraoperative seizures during awake craniotomy: incidence and consequences: analysis of 477 patients. Neurosurgery 73:1351402013

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

    Ojemann GA: Neurosurgical management of epilepsy: a personal perspective in 1983. Appl Neurophysiol 46:11181983

  • 33

    Quiñones-Hinojosa AOjemann SGSanai NDillon WPBerger MS: Preoperative correlation of intraoperative cortical mapping with magnetic resonance imaging landmarks to predict localization of the Broca area. J Neurosurg 99:3113182003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Sanai NBerger MS: Glioma extent of resection and its impact on patient outcome. Neurosurgery 62:7537662008

  • 35

    Sanai NBerger MS: Mapping the horizon: techniques to optimize tumor resection before and during surgery. Clin Neurosurg 55:14192008

  • 36

    Sanai NBerger MS: Operative techniques for gliomas and the value of extent of resection. Neurotherapeutics 6:4784862009

  • 37

    Sanai NMirzadeh ZBerger MS: Functional outcome after language mapping for glioma resection. N Engl J Med 358:18272008

  • 38

    Sanai NPolley MYMcDermott MWParsa ATBerger MS: An extent of resection threshold for newly diagnosed glioblastomas. J Neurosurg 115:382011

  • 39

    Shorvon SD: The etiologic classification of epilepsy. Epilepsia 52:105210572011

  • 40

    Skirboll SSOjemann GABerger MSLettich EWinn HR: Functional cortex and subcortical white matter located within gliomas. Neurosurgery 38:6786851996

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

    Tamura YOgawa HKapeller CPrueckl RTakeuchi FAnei R: Passive language mapping combining real-time oscillation analysis with cortico-cortical evoked potentials for awake craniotomy. J Neurosurg 125:158015882016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42

    Taplin AMde Pesters ABrunner PHermes DDalfino JCAdamo MA: Intraoperative mapping of expressive language cortex using passive real-time electrocorticography. Epilepsy Behav Case Rep 5:46512016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43

    Tatum WO IVQuinones-Hinojosa A: Onco-epilepsy: more than tumor and seizures. Mayo Clin Proc 93:118111842018

  • 44

    van ’t Klooster MAvan Klink NELeijten FSZelmann RGebbink TAGosselaar PH: Residual fast ripples in the intraoperative corticogram predict epilepsy surgery outcome. Neurology 85:1201282015

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 45

    Vogel RW: Understanding anodal and cathodal stimulation. The ASNM Monitor. December 12017 (https://www.asnm.org/blogpost/1635804/290597/Understanding-Anodal-and-Cathodal-Stimulation) [Accessed May 8 2019]

    • Export Citation
  • 46

    von Koch CSQuinones-Hinojosa AGulati MLyon RPeacock WJYingling CD: Clinical outcome in children undergoing tethered cord release utilizing intraoperative neurophysiological monitoring. Pediatr Neurosurg 37:81862002

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 47

    Voorhies JMCohen-Gadol A: Techniques for placement of grid and strip electrodes for intracranial epilepsy surgery monitoring: pearls and pitfalls. Surg Neurol Int 4:982013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48

    Walker JAQuiñones-Hinojosa ABerger MS: Intraoperative speech mapping in 17 bilingual patients undergoing resection of a mass lesion. Neurosurgery 54:1131182004

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 49

    Wesseling PCapper D: WHO 2016 Classification of gliomas. Neuropathol Appl Neurobiol 44:1391502018

  • 50

    World Health Organization GWH: Epilepsy Fact Sheet. Geneva: WHO2019 (https://www.who.int/news-room/fact-sheets/detail/epilepsy) [Accessed May 9 2019]

    • Search Google Scholar
    • Export Citation
  • 51

    Wyler AROjemann GALettich EWard AA Jr: Subdural strip electrodes for localizing epileptogenic foci. J Neurosurg 60:119512001984

  • 52

    Yuan YPeizhi ZXiang WYanhui LRuofei LShu J: Intraoperative seizures and seizures outcome in patients underwent awake craniotomy. J Neurosurg Sci [epub ahead of print]2016

    • PubMed
    • Search Google Scholar
    • Export Citation

TrendMD

Metrics

Metrics

All Time Past Year Past 30 Days
Abstract Views 1079 1079 356
Full Text Views 240 240 31
PDF Downloads 100 100 3
EPUB Downloads 0 0 0

PubMed

Google Scholar