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Surgical Technique and Outcome of Extensive Frontal Lobectomy for Treatment of Intracable Non-Lesional Frontal Lobe Epilepsy

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Surgical Technique and Outcome of Extensive Frontal Lobectomy for Treatment of Intracable Non-Lesional Frontal Lobe Epilepsy ORIGINAL ARTICLE doi: 10.2176/nmc.oa.2018-0286 Neurol Med Chir (Tokyo) 60, 17–25, 2020 Online December 5, 2019 Surgical Technique and Outcome of Extensive Frontal Lobectomy for Treatment of Intracable Non-lesional Frontal Lobe Epilepsy Sachiko HIRATA,1 Michiharu MORINO,1 Shunsuke NAKAE,1 and Takahiro MATSUMOTO1 1Department of Neurosurgery, Kumagaya General Hospital, Kumagaya, Saitama, Japan Abstract Although extensive frontal lobectomy (eFL) is a common surgical procedure for intractable frontal lobe epilepsy (FLE), there have been very few reports regarding surgical techniques for eFL. This article pro- vides step-by-step descriptions of our surgical technique for non-lesional FLE. Sixteen patients under- going eFL were included in this study. The goals were to maximize gray matter removal, including the orbital gyrus and subcallosal area, and to spare the primary motor and premotor cortexes and anterior perforated substance. The eFL consists of three steps: (1) positioning, craniotomy, and exposure; (2) lateral frontal lobe resection; and (3), resection of the rectus gyrus and orbital gyrus. Resection ahead of bregma allows preservation of motor and premotor area function. To remove the orbital gyrus preserving anterior perforated substance, it is essential to visualize the olfactory trigone beneath the pia. It is important to observe the surface of the contralateral medial frontal lobe for complete removal of the subcallosal area of the frontal lobe. Thirteen patients (81.25%) became seizure-free and three patients (18.75%) continued to have seizures. None of the patients showed any complications. The eFL is a good surgical technique for the treatment of intractable non-lesional FLE. For treatment of epilepsy by eFL, it is important to resect the non-eloquent area of the frontal lobe as much as possible with preservation of the eloquent cortex. Key words: intractable frontal lobe epilepsy, non-lesional frontal lobe epilepsy, extensive frontal lobectomy Introduction seizure onset zone. Especially, magnetic resonance imaging (MRI) has become the standard modality Frontal lobe epilepsy (FLE) accounts for 20–30% of for presurgical patients. Despite advances in MRI, partial epilepsies.1,2) Approximately 30% of partial MRI-negative FLE (“non-lesional FLE”) accounts for seizure patients suffer from drug-resistant seizures,3) about 30% of neocortical epilepsy cases.6–8) Surgical and patients with drug-resistant epilepsy may resection of an epileptogenic lesion was shown to require surgery. FLE surgery accounts for approxi- be associated with favorable postoperative outcome. mately 10–20% of all epilepsy surgeries, and is the In contrast, despite the advent of advanced imaging second most common type of operation after those techniques, such as interictal and ictal electroen- for temporal lobe epilepsy (TLE).2,4) However, it has cephalography (EEG), long-term video EEG, chronic been reported that the results of surgical treatment intracranial EEG (iEEG), intraoperative electrocorti- for FLE (45–60%) are generally unsatisfactory in cography (ECoG), and positron emission tomography comparison with those for TLE.4–6) One reason for (PET), surgical treatment of non-lesional FLE is one the poor surgical outcomes of FLE is the lack of a of the most challenging areas in epilepsy surgery.5) consistent target organ in FLE in contrast to targeting Frontal lobectomy is a commonly performed of the hippocampus in TLE. Neuroimaging techniques neurosurgical procedure, especially for treating brain have been suggested to be useful for diagnosis of the tumors, such as poorly marginated low-grade glioma, cerebral hemorrhage and contusion. However, the Received November 21, 2018; Accepted August 13, 2019 main purpose of classical frontal lobectomy is to 9) Copyright© 2020 by The Japan Neurosurgical Society This resect the lesion. work is licensed under a Creative Commons Attribution- A different concept is required in treatment of non- NonCommercial-NoDerivatives International License. lesional FLE. This strategy requires resection of the 17 18 S. Hirata et al. non-eloquent frontal lobe area as much as possible Thirty-five patients were diagnosed with non- but should not damage to eloquent area. The most lesional FLE; nine patients were followed up for important goal is to properly resect part of the anterior <1 year (eFL was performed in three patients); eight cingulate gyrus, orbital gyrus, and subcallosal area. patients underwent localized frontal lobectomy However, the importance of resecting these parts has because of the focal epileptogenic zone [one in the not attracted sufficient attention outside of the treat- supplementary motor area (SMA), six in the orbital ment of epilepsy. We call the frontal lobectomy that gyrus, and one in the motor area; multiple subpial includes not only the classical resection area but also transection was performed in this latter case]; two part of the anterior cingulate gyrus, orbital gyrus, patients were suspected to have multifocal epilepsy and subcallosal area “extensive frontal lobectomy” and underwent frontal lobectomy with an additional (eFL). There have been a few reports regarding the procedure (corpus callosotomy, temporal lobectomy). surgical anatomy and technique of eFL. This paper The iEEG was performed in seven patients, two of will present the surgical anatomy and techniques of whom had ictal epileptic discharge at the orbital gyri eFL and show the postoperative seizure outcomes and underwent localized frontal lobectomy. Sixteen in patients undergoing this operation. patients (nine males, seven females) who underwent eFL were included in this study. Data collected Materials and Methods included age at seizure onset and surgery, gender, side of surgery, preoperative MRI, preoperative total Surgical strategy intelligence quotient (TIQ) score, and seizure outcome All patients underwent MRI, single-photon emission (according to the Engel classification) at least 1 year computed tomography (SPECT), sleep activation EEG, after the operation.10) Five and 11 patients had surgery and long-term video EEG as preoperative examina- on the left and right hemispheres, respectively. The tions. It was necessary for diagnosis of non-lesional dominant hemisphere was left in all of these cases. FLE to confirm the typical frontal lobe seizures by The mean age of patients who underwent epilepsy long-term video EEG and the epileptiform discharges surgery was 27.25 years (range 11–45 years, SD beginning from the area of the prefrontal lobe or 9.42), mean age at epilepsy onset was 6.88 years frontal lobe on sleep activation EEG. Patients with (range 3–19 years, SD 5.14), and preoperative mean lesions detected on MRI or SPECT underwent limited TIQ score was 92.08 (range 70–103, SD 13.01). frontal lobectomy. Patients without any lesions on There were no statistically significant differences MRI and SPECT were diagnosed as non-lesional FLE. in characteristics between the patients according Focal resection is performed in non-lesional FLE to the side of surgery (Table 1). patients if long-term video EEG and ECoG reveal a The study protocol was reviewed and approved matched epileptogenic zone. by the Institutional Review Boards of the partici- The iEEG is adopted for FLE patients whose pating institutions. laterality is difficult to identify, who are suspected to have another additional epileptogenic zone or Surgical anatomy and function localized epileptogenic zone in a frontal lobe, such The frontal lobe is the largest area of the brain, and as the temporal lobe. includes about one-third of the whole hemispheric The eFL is adopted in our department for non- lesional patients without localized findings on Table 1 Demographic characteristics and clinical data long-term video EEG and ECoG. of the patients Right FLE Left FLE P-value Patients (n = 11) (n = 5) Operations for FLE were performed in 35 patients Gender at the Department of Neurosurgery, Osaka City Univer- sity Hospital, Osaka, Japan, between April 2000 and Male (%) 54.55 60 0.844 March 2010, in 33 patients at the Department of Age at surgery (yr) 29.64 (3.01) 22 (3.33) 0.151 Neurosurgery, Tokyo Metropolitan Hospital, Tokyo, Age at onset of 7.75 (2.95) 6 (0.41) 0.229 Japan, between April 2010 and March 2017, and in 11 epilepsy (yr) patients at the Department of Neurosurgery, Kumagaya Preoperative TIQ 93.13 (4.36) 90.4 (6.90) 0.656 General Hospital, Saitama, Japan, between April 2017 Seizure free (%) 73 100 0.242 and August 2018 (all operations performed by M.M.). Data are expressed as mean (standard error) unless otherwise Lesions such as brain tumors or cortical dysplasia indicated. Student’s t-test, Wilcoxon rank sum test and localized in the frontal lobe were detected in 44 of Welch’s test were used where appropriate. FLE: frontal lobe the total of 79 patients (56%) on MRI or SPECT. epilepsy, TIQ: total intelligence quotient, yr: years. Neurol Med Chir (Tokyo) 60, January, 2020 Surgical Technique and Outcome of eFL for Non-lesional FLE 19 surface. The lateral surface of the frontal lobe is cerebral artery, such as the lateral striae arteries, the bounded by the central sulcus (rear), by the supe- perforator of the anterior cerebral artery (ACA), such rior hemispheric border (above), and by the sylvian as the recurrent artery of Heubner, and the anterior veins (below). choroidal artery. The anterior perforating arteries The lateral surface is divided by three sulci into supply blood to many important structures in the four gyri (precentral gyrus, superior, middle, and deep brain (e.g., the caudate nucleus, putamen, inferior gyri). The precentral gyrus is bounded in internal capsule, pallidus, and thalamus). The primary front by the precentral sulcus and to the rear by the motor cortex lies along the precentral gyrus, and central sulcus. The superior, middle, and inferior gyri the premotor area lies in front of the precentral are located in front of the precentral gyrus, and are gyrus. The SMA lies in the midline surface of the divided by the superior and inferior frontal sulci.
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