Interictal scalp electroencephalography and intraoperative electrocorticography inmagnetic resonance imaging-negative temporal lobe epilepsy surgery

David B. Burkholder, Vlastimil Sulc, E. Matthew Hoffman, Gregory D Cascino, Jeffrey W. Britton, Elson L. So, W. Richard Marsh, Fredric B. Meyer, Jamie Van Gompel, Caterina Giannini, C. Thomas Wass, Robert E. Watson, Gregory Alan Worrell

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

IMPORTANCE Scalp electroencephalography (EEG) and intraoperative electrocorticography (ECoG) are routinely used in the evaluation of magnetic resonance imaging-negative= temporal lobe epilepsy (TLE) undergoing standard anterior temporal lobectomy with amygdalohippocampectomy (ATL), but the utility of interictal epileptiform discharge (IED) identification and its role in outcome are poorly defined. OBJECTIVES: To determine whether the following are associated with surgical outcomes in patients with magnetic resonance imaging-negative TLE who underwent standard ATL: (1) unilateral-only IEDs on preoperative scalp EEG; (2) complete resection of tissue generating IEDs on ECoG; (3) complete resection of opioid-induced IEDs recorded on ECoG; and (4) location of IEDs recorded on ECoG. DESIGN, SETTING, AND PARTICIPANTS: Data were gathered through retrospective medical record review at a tertiary referral center. Adult and pediatric patients with TLE who underwent standard ATL between January 1, 1990, and October 15, 2010, were considered for inclusion. Inclusion criteria were magnetic resonance imaging-negative TLE, standard ECoG performed at the time of surgery, and a minimum follow-up of 12 months. Univariate analysis was performed using log-rank time-to-event analysis. Variables reaching significance with log-rank testing were further analyzed using Cox proportional hazards. MAIN OUTCOMES AND MEASURES: Excellent or nonexcellent outcome at time of last follow-up. An excellent outcome was defined as Engel class I and a nonexcellent outcome as Engel classes II through IV. RESULTS Eighty-seven patients met inclusion criteria, with 48 (55%) achieving an excellent outcome following ATL. Unilateral IEDs on scalp EEG (P = .001) and complete resection of brain regions generating IEDs on baseline intraoperative ECoG (P = .02) were associated with excellent outcomes in univariate analysis. Both were associated with excellent outcomes when analyzed with Cox proportional hazards (unilateral-only IEDs, relative risk = 0.31 [95%CI, 0.16-0.64]; complete resection of IEDs on baseline ECoG, relative risk = 0.39 [95%CI, 0.20-0.76]). Overall, 25 of 35 patients (71%) with both unilateral-only IEDs and complete resection of baseline ECoG IEDs had an excellent outcome. CONCLUSIONS AND RELEVANCE: Unilateral-only IEDs on preoperative scalp EEG and complete resection of IEDs on baseline ECoG are associated with better outcomes following standard ATL inmagnetic resonance imaging-negative TLE. Prospective evaluation is needed to clarify the use of ECoG in tailoring temporal lobectomy.

Original languageEnglish (US)
Pages (from-to)702-709
Number of pages8
JournalJAMA Neurology
Volume71
Issue number6
DOIs
StatePublished - 2014

Fingerprint

Temporal Lobe Epilepsy
Scalp
Electroencephalography
Magnetic Resonance Imaging
Anterior Temporal Lobectomy
Electrocorticography
Imaging
Surgery
Tertiary Care Centers
Opioid Analgesics
Medical Records
Inclusion
Pediatrics

ASJC Scopus subject areas

  • Arts and Humanities (miscellaneous)
  • Clinical Neurology

Cite this

Interictal scalp electroencephalography and intraoperative electrocorticography inmagnetic resonance imaging-negative temporal lobe epilepsy surgery. / Burkholder, David B.; Sulc, Vlastimil; Hoffman, E. Matthew; Cascino, Gregory D; Britton, Jeffrey W.; So, Elson L.; Marsh, W. Richard; Meyer, Fredric B.; Van Gompel, Jamie; Giannini, Caterina; Wass, C. Thomas; Watson, Robert E.; Worrell, Gregory Alan.

In: JAMA Neurology, Vol. 71, No. 6, 2014, p. 702-709.

Research output: Contribution to journalArticle

Burkholder, David B. ; Sulc, Vlastimil ; Hoffman, E. Matthew ; Cascino, Gregory D ; Britton, Jeffrey W. ; So, Elson L. ; Marsh, W. Richard ; Meyer, Fredric B. ; Van Gompel, Jamie ; Giannini, Caterina ; Wass, C. Thomas ; Watson, Robert E. ; Worrell, Gregory Alan. / Interictal scalp electroencephalography and intraoperative electrocorticography inmagnetic resonance imaging-negative temporal lobe epilepsy surgery. In: JAMA Neurology. 2014 ; Vol. 71, No. 6. pp. 702-709.
@article{9f3ef9815e794a6d933c9389f46560e7,
title = "Interictal scalp electroencephalography and intraoperative electrocorticography inmagnetic resonance imaging-negative temporal lobe epilepsy surgery",
abstract = "IMPORTANCE Scalp electroencephalography (EEG) and intraoperative electrocorticography (ECoG) are routinely used in the evaluation of magnetic resonance imaging-negative= temporal lobe epilepsy (TLE) undergoing standard anterior temporal lobectomy with amygdalohippocampectomy (ATL), but the utility of interictal epileptiform discharge (IED) identification and its role in outcome are poorly defined. OBJECTIVES: To determine whether the following are associated with surgical outcomes in patients with magnetic resonance imaging-negative TLE who underwent standard ATL: (1) unilateral-only IEDs on preoperative scalp EEG; (2) complete resection of tissue generating IEDs on ECoG; (3) complete resection of opioid-induced IEDs recorded on ECoG; and (4) location of IEDs recorded on ECoG. DESIGN, SETTING, AND PARTICIPANTS: Data were gathered through retrospective medical record review at a tertiary referral center. Adult and pediatric patients with TLE who underwent standard ATL between January 1, 1990, and October 15, 2010, were considered for inclusion. Inclusion criteria were magnetic resonance imaging-negative TLE, standard ECoG performed at the time of surgery, and a minimum follow-up of 12 months. Univariate analysis was performed using log-rank time-to-event analysis. Variables reaching significance with log-rank testing were further analyzed using Cox proportional hazards. MAIN OUTCOMES AND MEASURES: Excellent or nonexcellent outcome at time of last follow-up. An excellent outcome was defined as Engel class I and a nonexcellent outcome as Engel classes II through IV. RESULTS Eighty-seven patients met inclusion criteria, with 48 (55{\%}) achieving an excellent outcome following ATL. Unilateral IEDs on scalp EEG (P = .001) and complete resection of brain regions generating IEDs on baseline intraoperative ECoG (P = .02) were associated with excellent outcomes in univariate analysis. Both were associated with excellent outcomes when analyzed with Cox proportional hazards (unilateral-only IEDs, relative risk = 0.31 [95{\%}CI, 0.16-0.64]; complete resection of IEDs on baseline ECoG, relative risk = 0.39 [95{\%}CI, 0.20-0.76]). Overall, 25 of 35 patients (71{\%}) with both unilateral-only IEDs and complete resection of baseline ECoG IEDs had an excellent outcome. CONCLUSIONS AND RELEVANCE: Unilateral-only IEDs on preoperative scalp EEG and complete resection of IEDs on baseline ECoG are associated with better outcomes following standard ATL inmagnetic resonance imaging-negative TLE. Prospective evaluation is needed to clarify the use of ECoG in tailoring temporal lobectomy.",
author = "Burkholder, {David B.} and Vlastimil Sulc and Hoffman, {E. Matthew} and Cascino, {Gregory D} and Britton, {Jeffrey W.} and So, {Elson L.} and Marsh, {W. Richard} and Meyer, {Fredric B.} and {Van Gompel}, Jamie and Caterina Giannini and Wass, {C. Thomas} and Watson, {Robert E.} and Worrell, {Gregory Alan}",
year = "2014",
doi = "10.1001/jamaneurol.2014.585",
language = "English (US)",
volume = "71",
pages = "702--709",
journal = "JAMA Neurology",
issn = "2168-6149",
publisher = "American Medical Association",
number = "6",

}

TY - JOUR

T1 - Interictal scalp electroencephalography and intraoperative electrocorticography inmagnetic resonance imaging-negative temporal lobe epilepsy surgery

AU - Burkholder, David B.

AU - Sulc, Vlastimil

AU - Hoffman, E. Matthew

AU - Cascino, Gregory D

AU - Britton, Jeffrey W.

AU - So, Elson L.

AU - Marsh, W. Richard

AU - Meyer, Fredric B.

AU - Van Gompel, Jamie

AU - Giannini, Caterina

AU - Wass, C. Thomas

AU - Watson, Robert E.

AU - Worrell, Gregory Alan

PY - 2014

Y1 - 2014

N2 - IMPORTANCE Scalp electroencephalography (EEG) and intraoperative electrocorticography (ECoG) are routinely used in the evaluation of magnetic resonance imaging-negative= temporal lobe epilepsy (TLE) undergoing standard anterior temporal lobectomy with amygdalohippocampectomy (ATL), but the utility of interictal epileptiform discharge (IED) identification and its role in outcome are poorly defined. OBJECTIVES: To determine whether the following are associated with surgical outcomes in patients with magnetic resonance imaging-negative TLE who underwent standard ATL: (1) unilateral-only IEDs on preoperative scalp EEG; (2) complete resection of tissue generating IEDs on ECoG; (3) complete resection of opioid-induced IEDs recorded on ECoG; and (4) location of IEDs recorded on ECoG. DESIGN, SETTING, AND PARTICIPANTS: Data were gathered through retrospective medical record review at a tertiary referral center. Adult and pediatric patients with TLE who underwent standard ATL between January 1, 1990, and October 15, 2010, were considered for inclusion. Inclusion criteria were magnetic resonance imaging-negative TLE, standard ECoG performed at the time of surgery, and a minimum follow-up of 12 months. Univariate analysis was performed using log-rank time-to-event analysis. Variables reaching significance with log-rank testing were further analyzed using Cox proportional hazards. MAIN OUTCOMES AND MEASURES: Excellent or nonexcellent outcome at time of last follow-up. An excellent outcome was defined as Engel class I and a nonexcellent outcome as Engel classes II through IV. RESULTS Eighty-seven patients met inclusion criteria, with 48 (55%) achieving an excellent outcome following ATL. Unilateral IEDs on scalp EEG (P = .001) and complete resection of brain regions generating IEDs on baseline intraoperative ECoG (P = .02) were associated with excellent outcomes in univariate analysis. Both were associated with excellent outcomes when analyzed with Cox proportional hazards (unilateral-only IEDs, relative risk = 0.31 [95%CI, 0.16-0.64]; complete resection of IEDs on baseline ECoG, relative risk = 0.39 [95%CI, 0.20-0.76]). Overall, 25 of 35 patients (71%) with both unilateral-only IEDs and complete resection of baseline ECoG IEDs had an excellent outcome. CONCLUSIONS AND RELEVANCE: Unilateral-only IEDs on preoperative scalp EEG and complete resection of IEDs on baseline ECoG are associated with better outcomes following standard ATL inmagnetic resonance imaging-negative TLE. Prospective evaluation is needed to clarify the use of ECoG in tailoring temporal lobectomy.

AB - IMPORTANCE Scalp electroencephalography (EEG) and intraoperative electrocorticography (ECoG) are routinely used in the evaluation of magnetic resonance imaging-negative= temporal lobe epilepsy (TLE) undergoing standard anterior temporal lobectomy with amygdalohippocampectomy (ATL), but the utility of interictal epileptiform discharge (IED) identification and its role in outcome are poorly defined. OBJECTIVES: To determine whether the following are associated with surgical outcomes in patients with magnetic resonance imaging-negative TLE who underwent standard ATL: (1) unilateral-only IEDs on preoperative scalp EEG; (2) complete resection of tissue generating IEDs on ECoG; (3) complete resection of opioid-induced IEDs recorded on ECoG; and (4) location of IEDs recorded on ECoG. DESIGN, SETTING, AND PARTICIPANTS: Data were gathered through retrospective medical record review at a tertiary referral center. Adult and pediatric patients with TLE who underwent standard ATL between January 1, 1990, and October 15, 2010, were considered for inclusion. Inclusion criteria were magnetic resonance imaging-negative TLE, standard ECoG performed at the time of surgery, and a minimum follow-up of 12 months. Univariate analysis was performed using log-rank time-to-event analysis. Variables reaching significance with log-rank testing were further analyzed using Cox proportional hazards. MAIN OUTCOMES AND MEASURES: Excellent or nonexcellent outcome at time of last follow-up. An excellent outcome was defined as Engel class I and a nonexcellent outcome as Engel classes II through IV. RESULTS Eighty-seven patients met inclusion criteria, with 48 (55%) achieving an excellent outcome following ATL. Unilateral IEDs on scalp EEG (P = .001) and complete resection of brain regions generating IEDs on baseline intraoperative ECoG (P = .02) were associated with excellent outcomes in univariate analysis. Both were associated with excellent outcomes when analyzed with Cox proportional hazards (unilateral-only IEDs, relative risk = 0.31 [95%CI, 0.16-0.64]; complete resection of IEDs on baseline ECoG, relative risk = 0.39 [95%CI, 0.20-0.76]). Overall, 25 of 35 patients (71%) with both unilateral-only IEDs and complete resection of baseline ECoG IEDs had an excellent outcome. CONCLUSIONS AND RELEVANCE: Unilateral-only IEDs on preoperative scalp EEG and complete resection of IEDs on baseline ECoG are associated with better outcomes following standard ATL inmagnetic resonance imaging-negative TLE. Prospective evaluation is needed to clarify the use of ECoG in tailoring temporal lobectomy.

UR - http://www.scopus.com/inward/record.url?scp=84902203120&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84902203120&partnerID=8YFLogxK

U2 - 10.1001/jamaneurol.2014.585

DO - 10.1001/jamaneurol.2014.585

M3 - Article

C2 - 24781216

AN - SCOPUS:84902203120

VL - 71

SP - 702

EP - 709

JO - JAMA Neurology

JF - JAMA Neurology

SN - 2168-6149

IS - 6

ER -