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 in magnetic resonance imaging-negative TLE. Prospective evaluation is needed to clarify the use of ECoG in tailoring temporal lobectomy.

Department of Anesthesiology Mayo Clinic Rochester Minnesota

Department of Neurologic Surgery Mayo Clinic Rochester Minnesota

Department of Neurology Mayo Clinic Rochester Minnesota

Department of Neurology Mayo Clinic Rochester Minnesota2International Clinical Research Center St Anne's University Hospital Brno Czech Republic

Department of Neurology Mayo Clinic Rochester Minnesota7Department of Physiology and Biomedical Engineering Mayo Clinic Rochester Minnesota

Department of Pathology Mayo Clinic Rochester Minnesota

Department of Radiology Mayo Clinic Rochester Minnesota

JAMA Neurol. 2014 Jun;71(6):681-2. doi: 10.1001/jamaneurol.2014.584. PubMed

Zobrazit více v PubMed

Bell ML, Rao S, So EL, et al. Epilepsy surgery outcomes in temporal lobe epilepsy with a normal MRI. Epilepsia. 2009;50(9):2053–2060. PubMed PMC

Berkovic SF, McIntosh AM, Kalnins RM, et al. Preoperative MRI predicts outcome of temporal lobectomy: an actuarial analysis. Neurology. 1995;45(7):1358–1363. PubMed

Bien CG, Szinay M, Wagner J, Clusmann H, Becker AJ, Urbach H. Characteristics and surgical outcomes of patients with refractory magnetic resonance imaging-negative epilepsies. Arch Neurol. 2009;66(12):1491–1499. PubMed

Fong JS, Jehi L, Najm I, Prayson RA, Busch R, Bingaman W. Seizure outcome and its predictors after temporal lobe epilepsy surgery in patients with normal MRI. Epilepsia. 2011;52(8):1393–1401. PubMed

Immonen A, Jutila L, Muraja-Murro A, et al. Long-term epilepsy surgery outcomes in patients with MRI-negative temporal lobe epilepsy. Epilepsia. 2010;51(11):2260–2269. PubMed

Jeha LE, Najm IM, Bingaman WE, et al. Predictors of outcome after temporal lobectomy for the treatment of intractable epilepsy. Neurology. 2006;66(12):1938–1940. PubMed

Radhakrishnan K, So EL, Silbert PL, et al. Predictors of outcome of anterior temporal lobectomy for intractable epilepsy: a multivariate study. Neurology. 1998;51(2):465–471. PubMed

Wieshmann UC, Larkin D, Varma T, Eldridge P. Predictors of outcome after temporal lobectomy for refractory temporal lobe epilepsy. Acta Neurol Scand. 2008;118(5):306–312. PubMed

Jayakar P, Dunoyer C, Dean P, et al. Epilepsy surgery in patients with normal or nonfocal MRI scans: integrative strategies offer long-term seizure relief. Epilepsia. 2008;49(5):758–764. PubMed

Sylaja PN, Radhakrishnan K, Kesavadas C, Sarma PS. Seizure outcome after anterior temporal lobectomy and its predictors in patients with apparent temporal lobe epilepsy and normal MRI. Epilepsia. 2004;45(7):803–808. PubMed

Tatum WO IV, Benbadis SR, Hussain A, et al. Ictal EEG remains the prominent predictor of seizure-free outcome after temporal lobectomy in epileptic patients with normal brain MRI. Seizure. 2008;17(7):631–636. PubMed

Téllez-Zenteno JF, Hernández Ronquillo L, Moien-Afshari F, Wiebe S. Surgical outcomes in lesional and non-lesional epilepsy: a systematic review and meta-analysis. Epilepsy Res. 2010;89(2-3):310–318. PubMed

Tonini C, Beghi E, Berg AT, et al. Predictors of epilepsy surgery outcome: a meta-analysis. Epilepsy Res. 2004;62(1):75–87. PubMed

Steinhoff BJ, So NK, Lim S, Lüders HO. Ictal scalp EEG in temporal lobe epilepsy with unitemporal versus bitemporal interictal epileptiform discharges. Neurology. 1995;45(5):889–896. PubMed

Luther N, Rubens E, Sethi N, et al. The value of intraoperative electrocorticography in surgical decision making for temporal lobe epilepsy with normal MRI. Epilepsia. 2011;52(5):941–948. PubMed PMC

McKhann GM, II, Schoenfeld-McNeill J, Born DE, Haglund MM, Ojemann GA. Intraoperative hippocampal electrocorticography to predict the extent of hippocampal resection in temporal lobe epilepsy surgery. J Neurosurg. 2000;93(1):44–52. PubMed

San-juan D, Tapia CA, González-Aragón MF, Martínez Mayorga A, Staba RJ, Alonso-Vanegas M. The prognostic role of electrocorticography in tailored temporal lobe surgery. Seizure. 2011;20(7):564–569. PubMed

Cascino GD, Trenerry MR, Jack CR, Jr, et al. Electrocorticography and temporal lobe epilepsy: relationship to quantitative MRI and operative outcome. Epilepsia. 1995;36(7):692–696. PubMed

Schwartz TH, Bazil CW, Walczak TS, Chan S, Pedley TA, Goodman RR. The predictive value of intraoperative electrocorticography in resections for limbic epilepsy associated with mesial temporal sclerosis. Neurosurgery. 1997;40(2):302–309. discussion 309-311. PubMed

Tripathi M, Garg A, Gaikwad S, et al. Intra-operative electrocorticography in lesional epilepsy. Epilepsy Res. 2010;89(1):133–141. PubMed

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(6):1179–1185. PubMed PMC

Asano E, Juhász C, Shah A, Sood S, Chugani HT. Role of subdural electrocorticography in prediction of long-term seizure outcome in epilepsy surgery. Brain. 2009;132:1038–1047. pt 4. PubMed PMC

Jack CR., Jr Magnetic resonance imaging. Neuroimaging and anatomy. Neuroimaging Clin N Am. 1995;5(4):597–622. PubMed

Wass CT, Grady RE, Fessler AJ, et al. The effects of remifentanil on epileptiform discharges during intraoperative electrocorticography in patients undergoing epilepsy surgery. Epilepsia. 2001;42(10):1340–1344. PubMed

Cascino GD, So EL, Sharbrough FW, et al. Alfentanil-induced epileptiform activity in patients with partial epilepsy. J Clin Neurophysiol. 1993;10(4):520–525. PubMed

Vale FL, Effio E, Arredondo N, et al. Efficacy of temporal lobe surgery for epilepsy in patients with negative MRI for mesial temporal lobe sclerosis. J Clin Neurosci. 2012;19(1):101–106. PubMed

Hardy SG, Miller JW, Holmes MD, et al. Factors predicting outcome of surgery for intractable epilepsy with pathologically verified mesial temporal sclerosis. Epilepsia. 2003;44(4):565–568. PubMed

Kilpatrick C, O’Brien T, Matkovic Z, Cook M, Kaye A. Preoperative evaluation for temporal lobe surgery. J Clin Neurosci. 2003;10(5):535–539. PubMed

Krendl R, Lurger S, Baumgartner C. Absolute spike frequency predicts surgical outcome in TLE with unilateral hippocampal atrophy. Neurology. 2008;71(6):413–418. PubMed

Lee SK, Kim KK, Hong KS, Kim JY, Chung CK. The lateralizing and surgical prognostic value of a single 2-hour EEG in mesial TLE. Seizure. 2000;9(5):336–339. PubMed

Grønlykke L, Knudsen ML, Høgenhaven H, Moltke FB, Madsen FF, Kjaer TW. Remifentanil-induced spike activity as a diagnostic tool in epilepsy surgery. Acta Neurol Scand. 2008;117(2):90–93. PubMed

Manninen PH, Burke SJ, Wennberg R, Lozano AM, El Beheiry H. Intraoperative localization of an epileptogenic focus with alfentanil and fentanyl. Anesth Analg. 1999;88(5):1101–1106. PubMed

McGuire G, El-Beheiry H, Manninen P, Lozano A, Wennberg R. Activation of electrocorticographic activity with remifentanil and alfentanil during neurosurgical excision of epileptogenic focus. Br J Anaesth. 2003;91(5):651–655. PubMed

Ross J, Kearse LA, Jr, Barlow MK, Houghton KJ, Cosgrove GR. Alfentanil-induced epileptiform activity: a simultaneous surface and depth electroencephalographic study in complex partial epilepsy. Epilepsia. 2001;42(2):220–225. PubMed

Zieglgänsberger W, French ED, Siggins GR, Bloom FE. Opioid peptides may excite hippocampal pyramidal neurons by inhibiting adjacent inhibitory interneurons. Science. 1979;205(4404):415–417. PubMed

Interictal high-frequency oscillations in focal human epilepsy