Elsevier

World Neurosurgery

Volume 144, December 2020, Pages e734-e742
World Neurosurgery

Original Article
The Brain is Not Flat: Conformal Electrode Arrays Diminish Complications of Subdural Electrode Implantation, A Series of 117 Cases

https://doi.org/10.1016/j.wneu.2020.09.063Get rights and content

Background

Intracranial recordings are integral to evaluating patients with pharmacoresistant epilepsy whom noninvasive testing fails to localize seizure focus. Although stereo-electroencephalography is the preferred method of intracranial recordings in most centers, subdural electrode (SDE) implantation is necessary in selected cases.

Objective

To identify imaging correlates that predict SDE complications (extra-axial fluid collections [EFCs]), and determine if modifications that diminish stiffness of electrode sheets reduce complications.

Methods

A prospective epilepsy surgery database was used to identify adults undergoing craniotomy for SDE implantation over a 14-year period. EFCs and midline shift were measured via magnetic resonance imaging and computed tomography imaging. Correlation analyses and multivariable logistic regression explored associations between use of conformal arrays, serial order of patients, previous ipsilateral intracranial surgery, midline shift, number of SDEs, and neurologic complications.

Results

A total of 111 consecutive patients (59 female) underwent 117 craniotomies (mean, 115 electrode contacts) for SDE implantation. There were 8 surgical complications, 3 in the first 17 (17.7%). and 5 (after electrode modifications) in a subsequent 100 craniotomies (5.0%). We noted an increase in electrode numbers implanted over time (P < 0.001) and decreased midline shift with conformal grids (ρ = – 0.32; P < 0.001). A multivariable regression showed that midline shift correlated with complications (odds ratio, 2.32; 95% confidence interval, 1.12–4.78; P = 0.023).

Conclusions

Hemorrhagic complications after SDE implantation are difficult to detect because of artifact from electrodes, but predictable by prominent midline shift (>4 mm). Risks inherent to SDE implantation may be minimized using conformal grids. With symptomatic EFCs, a single electrode cable exit site allows hematoma evacuation without terminating intracranial recordings.

Introduction

Intracranial electrophysiology is integral to evaluating patients with epilepsy with poorly defined relationships between lesion and ictal onsets, or no obvious lesion,1, 2, 3, 4, 5 and localizes epileptogenic zone1,2,6,7 in 30%–50% of epilepsy surgery candidates.8,9 Over the last 5 years, there has been a shift from subdural electrodes (SDEs) to stereo-electroencephalography (SEEG) for intracranial evaluation of focal epilepsy. SEEG is safer, faster, and less painful and has better outcomes, particularly to evaluate nonlesional epilepsy.7,10, 11, 12, 13, 14, 15 When the putative focus of epilepsy is proximate to the language, motor, or visual cortex, SDEs may be necessary to ascertain the relative topography of seizure focus relative to the eloquent cortex.7,16, 17, 18, 19, 20, 21, 22, 23 In our practice SDEs are used to evaluate neocortical epilepsy around eloquent language cortex, and in young children, whose skull is too thin to hold anchor bolts for SEEG.

The prevalence of major complications in patients with SDE is difficult to estimate given variability across series and publication bias that results in underreporting adverse outcomes. Large systematic reviews and meta-analyses of adverse events related to SDE placement show a pooled prevalence of around 12%,7,8 with most common adverse events: intracranial hemorrhage (ICH), increased intracranial pressure (ICP), neurologic compromise, and superficial infections around 4.0%, 2.4%, 2.3% and 3.0%, respectively.7 The underlying reason for most of these complications is symptomatic extra-axial fluid/blood collections (sEFCs) causing mass effect, increased ICP, and neurologic compromise. Risk varies between 1% and 17% in large series.1, 2, 3, 4, 5,8,17,24, 25, 26 In such situations, electrodes are removed, extra-axial fluid collection (EFC) evacuated and intracranial electroencephalographic evaluation interrupted or terminated.

We identified imaging characteristics predicting complications in patients who require close observation and early intervention to minimize the impact of complications. We devised techniques to minimize risks by modifying the grid design, implantation technique, and patient management after implantation. We focus on adults who are at greater risk for these complications because they undergo monitoring longer than pediatric patients, because of lower seizure frequencies.

SDEs are platinum-iridium discs embedded within flat silastic sheets.27 They do not reliably conform to the convex surface of the cortex and may promote sEFC accumulation in the potential space between arrays and the concave inner surface of the dura and skull. After complications during the first 3 years, we made relaxing incisions to help them conform to the cortex, coupled with routine dural expansion using bovine xenograft after implantation and used a single exit site for all leads.

Section snippets

Methods

After approval by the local institutional committee for protection of human subjects and informed consent from patients (IRB number HSC-MS-06-0385), a prospective database of adults undergoing SDE implantation for medically refractory epilepsy was compiled. Data from patients undergoing SDE placement by the senior author from November 2004 to October 2017 were compiled, including demographics, number of electrodes, monitoring duration, length of implantation surgery, history of previous

Results

A total of 117 craniotomies were performed in 111 patients: 42 right-sided, 68 left-sided, and 7 bilateral. Six patients returned to the operating room for additional electrodes to be placed during the same hospital stay. The mean patient age was 33.7 years (range, 16–63 years), 59 patients (53%) were female, and there was a mean of 115 electrode contacts (standard deviation, 29.7; range, 60–254), and mean monitoring duration of 8.4 days (standard deviation, 3; range, 1–17). Postimplantation CT

Discussion

Intracranial recording is critical to evaluating patients with intractable epilepsy.1, 2, 3, 4 SDE implantation is simple in concept but fraught with myriad potential complications. We show that hemorrhagic neurologic complications can be anticipated by the degree of shift on postoperative MRI. After modifications in perioperative management, it is possible to minimize risks. Like in other centers, the number of electrodes implanted increases with experience and perhaps with complexity of cases.

Conclusions

The use of conformal subdural grids and routine dural augmentation may reduce complications of SDE implantation. Complications can be anticipated using routine MRI and measuring midline shift. Symptomatic subdural collections may be safely removed without terminating the intracranial evaluation, if appropriate steps are taken to enable this at implantation.

CRediT authorship contribution statement

Brian A. Tong: Formal analysis, Investigation, Software, Data curation, Writing - original draft, Writing - review & editing, Visualization. Yoshua Esquenazi: Investigation, Formal analysis, Data curation, Writing - original draft, Visualization. Jessica Johnson: Formal analysis, Data curation, Project administration. Ping Zhu: Formal analysis, Software, Resources, Validation. Nitin Tandon: Conceptualization, Formal analysis, Investigation, Supervision, Visualization, Validation, Methodology.

References (45)

  • R.L. Sahjpaul et al.

    Dexamethasone for morbidity after subdural electrode insertion–a randomized controlled trial

    Can J Neurol Sci

    (2003)
  • G. Alarcon et al.

    Is it worth pursuing surgery for epilepsy in patients with normal neuroimaging?

    J Neurol Neurosurg Psychiatry

    (2006)
  • H. Yan et al.

    Method of invasive monitoring in epilepsy surgery and seizure freedom and morbidity: a systematic review

    Epilepsia

    (2019)
  • R. Arya et al.

    Adverse events related to extraoperative invasive EEG monitoring with subdural grid electrodes: a systematic review and meta-analysis

    Epilepsia

    (2013)
  • J.A. Bauman et al.

    Multistage epilepsy surgery. Safety, efficacy, and utility of a novel approach in pediatric extratemporal epilepsy

    Neurosurgery

    (2005)
  • N. Tandon et al.

    Analysis of morbidity and outcomes associated with use of subdural grids vs stereoelectroencephalography in patients with intractable epilepsy

    JAMA Neurol

    (2019)
  • D. Taussig et al.

    The contribution of clinical and electrophysiological (EEG and video-SEEG) data in the management of partial epilepsy surgery

  • F. Cardinale et al.

    Stereoelectroencephalography: surgical methodology, safety, and stereotactic application accuracy in 500 procedures

    Neurosurgery

    (2013)
  • J. Gonzalez-Martinez et al.

    Technique, results, and complications related to robot-assisted stereoelectroencephalography

    Neurosurgery

    (2016)
  • E. Behrens et al.

    Surgical and neurological complications in a series of 708 epilepsy surgery procedures

    Neurosurgery

    (1997)
  • T. Blauwblomme et al.

    Adverse events occurring during invasive electroencephalogram recordings in children

    Neurosurgery

    (2011)
  • B.J. Cysyk et al.

    A deep vein thrombosis prevention program for patients undergoing long-term invasive epilepsy monitoring

    J Neurosci Nurs

    (1996)
  • Cited by (15)

    • Event-related phase synchronization propagates rapidly across human ventral visual cortex

      2022, NeuroImage
      Citation Excerpt :

      Electrode Implantation and Data Recording: Data were acquired using either subdural grid electrodes (SDEs; 14 patients) or stereotactically placed depth electrodes (sEEGs; 68 patients). SDEs were subdural platinum-iridium electrodes embedded in a silicone elastomer sheet (PMT Corporation; top-hat design; 3 mm diameter cortical contact), surgically implanted via a craniotomy following previously described methods (Pieters et al., 2013; Tandon, 2012; Tong et al., 2020). sEEGs were implanted using a Robotic Surgical Assistant (ROSA; Medtech, Montpellier, France) (Rollo et al., 2020; Tandon et al., 2019).

    • Spatiotemporally distributed frontotemporal networks for sentence reading

      2023, Proceedings of the National Academy of Sciences of the United States of America
    View all citing articles on Scopus

    Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

    View full text