Editorial Opinion
The Reliability of Intraoperative Electrocorticography in Magnetic Resonance Imaging–Negative Temporal Lobe Epilepsy Spikes Mark the Spot Mark Quigg, MD, MSc
The ideal candidate for epilepsy surgery is the patient with medically intractable seizures who has unilateral hippocampal sclerosis and atrophy on magnetic resonance imaging (MRI) with concordant seizures recorded on video electroenRelated article page 702 cephalography. Two randomized trials determined clear advantages of anterior temporal lobectomy (ATL) over the best medical or delayed surgical therapy.1,2 The American Academy of Neurology published guidelines that recommend surgical evaluation for patients with intractable epilepsy.3 However, the nature of epilepsy surgery is changing; the number of patients obtaining surgery has not followed the growth in the number of epilepsy centers in the United States.4 One reason may be that the ideal “slam dunk” patient is rarer; the diagnostic pathway for remaining patients with less obvious lesions is more variable across centers and outcomes are not as good. One important group consists of individuals with MRInegative temporal lobe epilepsy. By definition, these patients have normal MRI findings but otherwise have presurgical findings consistent with an epileptic focus within the mesial structures of the temporal lobe. Outcomes after ATL are less favorable, so interest remains high in determining what presurgical procedures can maximize information, promote seizure-free outcomes, and minimize costs. One procedure is intraoperative electrocorticography (ECoG). Certainly ECoG is nothing new. Penfield5 found that ECoG, in addition to its role in monitoring brain mapping during electrical stimulation, helped confirm the epileptic zone and aided in tailoring resection to the distribution of interictal epileptiform discharges (IEDs). Since then, studies too numerous to cite herein have demonstrated the usefulness of ECoG in the resection of epileptic lesions such as tumors, hippocampal sclerosis, or purely physiological, nonstructural lesions. However, others have pointed out the lack of practicality of ECoG, noting the unreliability of IED when subjected to anesthesia, the inclarity of the significance of drug-activated IED, and the tendency for IED to overestimate the size of the epileptic zone. Burkholder et al6 evaluated the predictive abilities of 2 electrophysiological findings in a retrospective review of patients who underwent ATL for MRI-negative temporal lobe epilepsy. First, they found that if preoperative IED recorded from scalp electrodes was unilateral, seizure-free outcomes occurred in approximately 60% of patients compared with approximately 20% of patients with bilateral IED. Second, in patients for whom IED during ECoG did not stray from the margins of a standard ATL, 65% of patients experijamaneurology.com
enced excellent outcomes compared with 35% of patients in whom IEDs extended beyond the margins of a standard ATL. Both conditions together indicated a seizure remission rate of 71%. Both findings run counter to highly cited studies. For example, the prospective Multicenter Study of Epilepsy Surgery found no value in the consistency of scalp IED in prediction of long-term seizure control.7 An evaluation of ECoG with a similar number of patients as the present study found no correlations among IED location, pathology, and outcome.8 However, the authors point out that their highly homogeneous sample with consistent epileptologists and surgeons may have had an advantage over studies with a variety of focal epilepsies7,8 treated in multicenter consortiums.7 An important addition to their findings was that most of their patients had ECoG recorded both before and after treatment with intraoperative opioids. In contrast to naturally occurring IED, drug-activated IED had no predictive value regarding outcomes. Because drug activation remains a common practice for those who perform ECoG, this particular finding may both account for some of the variability among previous studies and suggest to some that reevaluation is needed regarding the specificity of drug-activated IED. Finally, the mesial vs lateral location of IED on ECoG was not predictive of outcome, a finding that contradicts a similar assessment9 and seems to counter the inference that the volume of distribution of IEDs is predictive. The patient grouping is timely. In the setting of MRInegative temporal lobe epilepsy, the present study supports checking an ECoG as long as an individual has the craniotomy available. Although patients for whom IEDs remain confined to an ATL had nearly twice the rate of seizure freedom than those who did not, the predictions revealed by ECoG may come too late for intervention; the patient is on the table and a craniotomy is performed. However, the knowledge gained from ECoG may guide future counseling on expected outcomes, modulate aggressiveness in tapering anticonvulsants in the postoperative period, or encourage the study of tailored resections based on larger IED volumes. Finally, the present study—a carefully documented case series performed by experts in the field—emphasizes that the ultimate study design, the randomized trial, is a rarity in epilepsy surgery. Given the state of dispersal of patients among many epilepsy centers, it will remain a rarity. To evaluate the conflicts among the present study and its precedents, one way to move forward is to encourage common methods and common means of reporting. Consortiums among centers with use of the National Institutes of HealthJAMA Neurology June 2014 Volume 71, Number 6
Copyright 2014 American Medical Association. All rights reserved.
Downloaded From: http://archneur.jamanetwork.com/ by a Penn State Milton S Hershey Med Ctr User on 05/24/2015
681
Opinion Editorial
Sponsored Common Data Elements as one technique will facilitate either cooperation or meta-analyses that can approach problems with the robustness of multicenter parARTICLE INFORMATION Author Affiliation: Department of Neurology, University of Virginia, Charlottesville. Corresponding Author: Mark Quigg, MD, MSc, Department of Neurology, Box 800394, University of Virginia, Charlottesville, VA 22902 (quigg @virginia.edu). Published Online: April 28, 2014. doi:10.1001/jamaneurol.2014.584. Conflict of Interest Disclosures: None reported. REFERENCES 1. Wiebe S, Blume WT, Girvin JP, Eliasziw M; Effectiveness and Efficiency of Surgery for Temporal Lobe Epilepsy Study Group. A randomized, controlled trial of surgery for temporal-lobe epilepsy. N Engl J Med. 2001;345(5): 311-318. 2. Engel J Jr, McDermott MP, Wiebe S, et al; Early Randomized Surgical Epilepsy Trial (ERSET) Study
682
ticipation. The presurgical evaluation of MRI-negative epilepsy is one field that needs findings ranging beyond the expertise of a single group of health care physicians.
Group. Early surgical therapy for drug-resistant temporal lobe epilepsy: a randomized trial. JAMA. 2012;307(9):922-930. 3. Engel J Jr, Wiebe S, French J, et al; Quality Standards Subcommittee of the American Academy of Neurology; American Epilepsy Society; American Association of Neurological Surgeons. Practice parameter: temporal lobe and localized neocortical resections for epilepsy: report of the Quality Standards Subcommittee of the American Academy of Neurology, in association with the American Epilepsy Society and the American Association of Neurological Surgeons. Neurology. 2003;60(4): 538-547. 4. Englot DJ, Ouyang D, Garcia PA, Barbaro NM, Chang EF. Epilepsy surgery trends in the United States: 1990-2008. Neurology. 2012;78(16): 1200-1206. 5. Jasper HH. Electrocorticography. In: Penfield W, Jasper HH, eds. Epilepsy and the Functional Anatomy of the Human Brain. Boston, MA: Little & Brown; 1954:693-710.
6. Burkholder DB, Sulc V, Hoffman EM, et al. Interictal scalp electroencephalography and intraoperative electrocorticography in magnetic resonance imaging–negative temporal lobe epilepsy surgery [published online April 28, 2014]. JAMA Neurol. doi:10.1001/jamaneurol.2014.585. 7. Spencer SS, Berg AT, Vickrey BG, et al; Multicenter Study of Epilepsy Surgery. Predicting long-term seizure outcome after resective epilepsy surgery: the multicenter study. Neurology. 2005;65 (6):912-918. 8. McBride MC, Binnie CD, Janota I, Polkey CE. Predictive value of intraoperative electrocorticograms in resective epilepsy surgery. Ann Neurol. 1991;30(4):526-532. 9. 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.
JAMA Neurology June 2014 Volume 71, Number 6
Copyright 2014 American Medical Association. All rights reserved.
Downloaded From: http://archneur.jamanetwork.com/ by a Penn State Milton S Hershey Med Ctr User on 05/24/2015
jamaneurology.com
The Reliability of Intraoperative Electrocorticography in Magnetic Resonance Imaging–Negative Temporal Lobe Epilepsy Spikes Mark the Spot Mark Quigg, MD, MSc
The ideal candidate for epilepsy surgery is the patient with medically intractable seizures who has unilateral hippocampal sclerosis and atrophy on magnetic resonance imaging (MRI) with concordant seizures recorded on video electroenRelated article page 702 cephalography. Two randomized trials determined clear advantages of anterior temporal lobectomy (ATL) over the best medical or delayed surgical therapy.1,2 The American Academy of Neurology published guidelines that recommend surgical evaluation for patients with intractable epilepsy.3 However, the nature of epilepsy surgery is changing; the number of patients obtaining surgery has not followed the growth in the number of epilepsy centers in the United States.4 One reason may be that the ideal “slam dunk” patient is rarer; the diagnostic pathway for remaining patients with less obvious lesions is more variable across centers and outcomes are not as good. One important group consists of individuals with MRInegative temporal lobe epilepsy. By definition, these patients have normal MRI findings but otherwise have presurgical findings consistent with an epileptic focus within the mesial structures of the temporal lobe. Outcomes after ATL are less favorable, so interest remains high in determining what presurgical procedures can maximize information, promote seizure-free outcomes, and minimize costs. One procedure is intraoperative electrocorticography (ECoG). Certainly ECoG is nothing new. Penfield5 found that ECoG, in addition to its role in monitoring brain mapping during electrical stimulation, helped confirm the epileptic zone and aided in tailoring resection to the distribution of interictal epileptiform discharges (IEDs). Since then, studies too numerous to cite herein have demonstrated the usefulness of ECoG in the resection of epileptic lesions such as tumors, hippocampal sclerosis, or purely physiological, nonstructural lesions. However, others have pointed out the lack of practicality of ECoG, noting the unreliability of IED when subjected to anesthesia, the inclarity of the significance of drug-activated IED, and the tendency for IED to overestimate the size of the epileptic zone. Burkholder et al6 evaluated the predictive abilities of 2 electrophysiological findings in a retrospective review of patients who underwent ATL for MRI-negative temporal lobe epilepsy. First, they found that if preoperative IED recorded from scalp electrodes was unilateral, seizure-free outcomes occurred in approximately 60% of patients compared with approximately 20% of patients with bilateral IED. Second, in patients for whom IED during ECoG did not stray from the margins of a standard ATL, 65% of patients experijamaneurology.com
enced excellent outcomes compared with 35% of patients in whom IEDs extended beyond the margins of a standard ATL. Both conditions together indicated a seizure remission rate of 71%. Both findings run counter to highly cited studies. For example, the prospective Multicenter Study of Epilepsy Surgery found no value in the consistency of scalp IED in prediction of long-term seizure control.7 An evaluation of ECoG with a similar number of patients as the present study found no correlations among IED location, pathology, and outcome.8 However, the authors point out that their highly homogeneous sample with consistent epileptologists and surgeons may have had an advantage over studies with a variety of focal epilepsies7,8 treated in multicenter consortiums.7 An important addition to their findings was that most of their patients had ECoG recorded both before and after treatment with intraoperative opioids. In contrast to naturally occurring IED, drug-activated IED had no predictive value regarding outcomes. Because drug activation remains a common practice for those who perform ECoG, this particular finding may both account for some of the variability among previous studies and suggest to some that reevaluation is needed regarding the specificity of drug-activated IED. Finally, the mesial vs lateral location of IED on ECoG was not predictive of outcome, a finding that contradicts a similar assessment9 and seems to counter the inference that the volume of distribution of IEDs is predictive. The patient grouping is timely. In the setting of MRInegative temporal lobe epilepsy, the present study supports checking an ECoG as long as an individual has the craniotomy available. Although patients for whom IEDs remain confined to an ATL had nearly twice the rate of seizure freedom than those who did not, the predictions revealed by ECoG may come too late for intervention; the patient is on the table and a craniotomy is performed. However, the knowledge gained from ECoG may guide future counseling on expected outcomes, modulate aggressiveness in tapering anticonvulsants in the postoperative period, or encourage the study of tailored resections based on larger IED volumes. Finally, the present study—a carefully documented case series performed by experts in the field—emphasizes that the ultimate study design, the randomized trial, is a rarity in epilepsy surgery. Given the state of dispersal of patients among many epilepsy centers, it will remain a rarity. To evaluate the conflicts among the present study and its precedents, one way to move forward is to encourage common methods and common means of reporting. Consortiums among centers with use of the National Institutes of HealthJAMA Neurology June 2014 Volume 71, Number 6
Copyright 2014 American Medical Association. All rights reserved.
Downloaded From: http://archneur.jamanetwork.com/ by a Penn State Milton S Hershey Med Ctr User on 05/24/2015
681
Opinion Editorial
Sponsored Common Data Elements as one technique will facilitate either cooperation or meta-analyses that can approach problems with the robustness of multicenter parARTICLE INFORMATION Author Affiliation: Department of Neurology, University of Virginia, Charlottesville. Corresponding Author: Mark Quigg, MD, MSc, Department of Neurology, Box 800394, University of Virginia, Charlottesville, VA 22902 (quigg @virginia.edu). Published Online: April 28, 2014. doi:10.1001/jamaneurol.2014.584. Conflict of Interest Disclosures: None reported. REFERENCES 1. Wiebe S, Blume WT, Girvin JP, Eliasziw M; Effectiveness and Efficiency of Surgery for Temporal Lobe Epilepsy Study Group. A randomized, controlled trial of surgery for temporal-lobe epilepsy. N Engl J Med. 2001;345(5): 311-318. 2. Engel J Jr, McDermott MP, Wiebe S, et al; Early Randomized Surgical Epilepsy Trial (ERSET) Study
682
ticipation. The presurgical evaluation of MRI-negative epilepsy is one field that needs findings ranging beyond the expertise of a single group of health care physicians.
Group. Early surgical therapy for drug-resistant temporal lobe epilepsy: a randomized trial. JAMA. 2012;307(9):922-930. 3. Engel J Jr, Wiebe S, French J, et al; Quality Standards Subcommittee of the American Academy of Neurology; American Epilepsy Society; American Association of Neurological Surgeons. Practice parameter: temporal lobe and localized neocortical resections for epilepsy: report of the Quality Standards Subcommittee of the American Academy of Neurology, in association with the American Epilepsy Society and the American Association of Neurological Surgeons. Neurology. 2003;60(4): 538-547. 4. Englot DJ, Ouyang D, Garcia PA, Barbaro NM, Chang EF. Epilepsy surgery trends in the United States: 1990-2008. Neurology. 2012;78(16): 1200-1206. 5. Jasper HH. Electrocorticography. In: Penfield W, Jasper HH, eds. Epilepsy and the Functional Anatomy of the Human Brain. Boston, MA: Little & Brown; 1954:693-710.
6. Burkholder DB, Sulc V, Hoffman EM, et al. Interictal scalp electroencephalography and intraoperative electrocorticography in magnetic resonance imaging–negative temporal lobe epilepsy surgery [published online April 28, 2014]. JAMA Neurol. doi:10.1001/jamaneurol.2014.585. 7. Spencer SS, Berg AT, Vickrey BG, et al; Multicenter Study of Epilepsy Surgery. Predicting long-term seizure outcome after resective epilepsy surgery: the multicenter study. Neurology. 2005;65 (6):912-918. 8. McBride MC, Binnie CD, Janota I, Polkey CE. Predictive value of intraoperative electrocorticograms in resective epilepsy surgery. Ann Neurol. 1991;30(4):526-532. 9. 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.
JAMA Neurology June 2014 Volume 71, Number 6
Copyright 2014 American Medical Association. All rights reserved.
Downloaded From: http://archneur.jamanetwork.com/ by a Penn State Milton S Hershey Med Ctr User on 05/24/2015
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