TECHNICAL NOTE Surgical strategy to avoid ischemic complications of the pyramidal tract in resective epilepsy surgery of the insula: technical case report Naoki Ikegaya, MD,1,2 Akio Takahashi, MD, PhD,1 Takanobu Kaido, MD, PhD,1 Yuu Kaneko, MD,1 Masaki Iwasaki, MD, PhD,1 Nobutaka Kawahara, MD, PhD,2 and Taisuke Otsuki, MD, PhD1,3 Department of Neurosurgery, Epilepsy Center, National Center of Neurology and Psychiatry (NCNP), Kodaira; 2Department of Neurosurgery, Yokohama City University, Yokohama; and 3Epilepsy Hospital Bethel Japan, Iwanuma, Japan 1 Surgical treatment of the insula is notorious for its high probability of motor complications, particularly when resecting the superoposterior part. Ischemic damage to the pyramidal tract in the corona radiata has been regarded as the cause of these complications, resulting from occlusion of the perforating arteries to the pyramidal tract through the insular cortex. The authors describe a strategy in which a small piece of gray matter is spared at the bottom of the periinsular sulcus, where the perforating arteries pass en route to the pyramidal tract, in order to avoid these complications. This method was successfully applied in 3 patients harboring focal cortical dysplasia in the posterior insula and frontoparietal operculum surrounding the periinsular sulcus. None of the patients developed permanent postoperative motor deficits, and seizure control was achieved in all 3 cases. The method described in this paper can be adopted for functional preservation of the pyramidal tract in the corona radiata when resecting epileptogenic pathologies involving insular and opercular regions. https://thejns.org/doi/abs/10.3171/2017.1.JNS161278 KEY WORDS epilepsy surgery; insula; focal cortical dysplasia; pyramidal tract; periinsular sulcus; surgical technique I nsular resection is becoming a common procedure in epilepsy surgery. However, cortical resection of the insula is notorious for the high probability of motor complications such as hemiplegia, particularly in resection of the superoposterior part.21 In previous studies of patients undergoing insulo-opercular surgeries (635 patients, in total), transient postoperative motor deficit occurred in 17.5% (range 0%–59.0%) and permanent motor deficit in 4.6% (range 0%–16.7%).1–4,7–13,15,17–19,21,22 These complications may be caused by indirect (i.e., ischemic) as well as direct damage to the pyramidal tract. Occlusion of the lenticulostriate arteries (LSAs) is a well-known cause of such ischemic injury. Furthermore, the long insu- lar artery (LIA), a “perforator-like” artery supplying blood to the corona radiata and mostly located in the posterior region of the insula, has been recognized as another important cause of these ischemic complications.16 Lang et al.7 reported that injury to the LIA was associated with postoperative hemiparesis in cases of insular tumor and recommended avoiding damage to arteries arising from M2 branches overlying the posterior insula. Kumabe et al.6 subsequently described not only the LIA, but also the long medullary artery (LMA) from the opercular region as contributors to ischemic complications involving the corona radiata. Furthermore, Tamura et al.14 demonstrated that LIA infarction occurred in the area above the LSA ABBREVIATIONS EEG = electroencephalography; LIA = long insular artery; LMA = long medullary artery; LSA = lenticulostriate artery; SISCOM = subtraction ictal SPECT coregistered to MRI; SPECT = single photon emission computed tomography. SUBMITTED May 18, 2016. ACCEPTED January 5, 2017. INCLUDE WHEN CITING Published online June 9, 2017; DOI: 10.3171/2017.1.JNS161278. ©AANS, 2017 J Neurosurg June 9, 2017 1 N. Ikegaya et al. territory, located between the tip of anterior horn and the top of the superior limb of the insular cleft on the coronal section of MRI. These observations indicate that the LIAs and LMAs supplying blood flow to the corona radiata pass through the posterior part of superior periinsular sulcus. Therefore, to avoid this ischemic complication, we adopted a simple surgical strategy: preserving part of the gray matter at the bottom of the periinsular sulcus where these minute vessels originate to perfuse the pyramidal tract in the corona radiata. This article describes 3 cases of epilepsy surgery in the insulo-opercular region with a discussion of the technical details of our surgical strategy. Methods Surgical planning was undertaken based on our routine presurgical evaluation protocol by means of video-electroencephalography (EEG) monitoring, MRI, FDG-PET, magnetoencephalography, and subtraction ictal single photon emission computed tomography (SPECT) coregistered to MRI (SISCOM). Resective surgery was motivated primarily by the congruence between MRI and SISCOM in our cases. The pyramidal tract within the centrum semiovale was delineated by diffusion tensor imaging, and the spatial relationship with the pathological lesion was investigated. The gray matter at the bottom of the periinsular sulcus closest to the paraventricular part of the pyramidal tract, which was considered to be the area most vulnerable to ischemia, was defined as the area to be preserved. Anatomical landmarks, such as gyral, sulcal, and vascular structures, were precisely identified on MRI to define the resection area. Intracranial EEG monitoring was undertaken using both subdural and depth electrodes, with the latter placed meticulously in and around the target area for confirmation of EEG onset as well as for intraoperative guidance for resection. Both an ultrasonic surgical system and simple suction technique with subpial resection were used during removal. Use of bipolar cautery was avoided if at all possible when removing the insulo-opercular cortex. The bottom of the sulcus, approximately 5 mm in diameter, was not exposed intraoperatively but was instead preserved together with the underlying gray matter structures (Fig. 1). Images from pre- and postoperative MRI studies were used for assessment of lesion volume, as calculated using OsiriX version 6.5 open-source software (www.osirix-viewer.com). Results Three patients were treated using this surgical strategy (Table 1). None of these patients developed permanent neurological deficits after surgery. Significant seizure reduction was achieved in all cases, including total seizure control in 2 cases, despite intentionally leaving a small piece of lesion. In Case 1, intracranial EEG recording demonstrated seizure onset from the upper part of the posterior insula spreading to the supramarginal gyrus. Resection of the frontoparietal operculum and posterior insular cortex was performed while preserving the gray matter at the bottom of the periinsular sulcus (Fig. 2A). In Case 2, intracranial EEG demonstrated onset of ictal 2 J Neurosurg June 9, 2017 discharges from abnormal gray matter at the insula and the frontal operculum surrounding the periinsular sulcus and an abnormal frontal sulcus. Resection of the superior part of the insula and frontal operculum was performed, preserving the gray matter at the bottom of the posterior part of the MRI lesion under which the pyramidal tract passed. Postoperative MRI showed ischemic changes in the centrum semiovale underneath the resected area where the bottom of the periinsular sulcus was totally removed but not underneath the preserved area (Fig. 2B). Transient motor weakness was observed in the patient’s right lower limb for 2 weeks postoperatively. In Case 3, depth electrodes were placed in the central, supramarginal, and superior temporal gyri surrounding the sylvian fissure downward to the posterior part of the insula. Resection of the parietal operculum was performed, preserving the gray matter at the bottom of the periinsular sulcus (Fig. 2C). Postoperative MRI demonstrated that more than 85% of the lesion shown on preoperative imaging was removed in all cases. Complete freedom from seizures was achieved in 2 cases, and more than 50% reduction in seizure frequency was achieved in the other.20 Discussion We described a simple surgical strategy to avoid postoperative ischemic complications involving the pyramidal tract in the corona radiata caused by insular resection, by preserving part of the gray matter at the bottom of the periinsular sulcus, where the minute vessels perfusing the pyramidal tract originate. Our experience shows that a small residual lesion should be considered acceptable in epilepsy surgery in pursuit of achieving satisfactory outcomes for both seizure control and motor function. Postoperative motor complications after insular and/ or opercular resection have been described in patients with brain tumors and vascular disease.1,2,4–8,10–13,15,17,​19,​ 21,22 The chance of permanent motor deficits after insuloopercular surgery has been reported at between 0% and 16.7%.1–4,7–13,15,17–19,21,22 Before Case 1, we experienced 14 cases of epilepsy surgery that included the insula as a part of resection. Postoperative hemiparesis was associated with ischemic complications of the corona radiata in 2 of the 7 cases in which the posterior part of the insula was removed (unpublished data). This fact motivated us to develop the strategy presented in this report. Damage to the LSAs has been reported as the main cause of permanent motor deficits.6,7,21 On the other hand, Lang et al.7 described the clinical importance of preserving the LIA overlying the posterior insula to avoid postoperative motor deficits. Identifying these perforating arteries in the surgical field, however, is quite difficult. There is also an argument that LIA is a subtype of white matter medullary artery.14 Kumabe et al.6 reported that not only the LIA, but also the LMA from the opercular region contribute to the blood supply to the corona radiata. As a matter of fact, however, defining intraoperatively which perforating and/or medullary arteries perfuse the pyramidal tract is difficult.5 We applied a strategy of not preserving any particular vessels, but rather preserving an area of gray matter 6.8% 118 1738 13.4% 492 3664 F 3 M 2 Ant = anterior; dev = deviation; FCD = focal cortical dysplasia; FU = follow-up; GTC = generalized tonic-clonic seizure; histol = histology; inf = inferior; neurol = neurological; operc = operculum; pst = posterior; Sz = seizure; temp = temporal; trans = transient; UE = upper extremity. * ILAE classification. FCD Type Class 1 (2 IIA yrs) Trans motor FCD Type Class 4 (1 weakness IIA yr) (2 wks) None FCD Type Class 1 (5 IIA mos) None 2.0% 190 9325 30 mos GTC, eye dev to rt, bilat blinking, Lt pst insula, supraLt mid-pst temp, Lt pst temp, swallowing, laryngeal constriction marginal gyrus parietal parietal 18 mos 40 mos Tonic Sz of UEs & face (rt > lt), Gray matter surround- Lt frontal pole, Bilat ant-mid breath holding ing lt periinsular & frontal, centemp, froninf frontal sulcus tral, parietal tal pole 5 yrs 19 yrs Lt UE paresthesia, motionless stare Pst upper insula, Rt central Rt mid-pst parietal operc temp 2 mos F 1 Postop Preop MRI Lesion Semiology At Op At Case No. Sex Onset Age TABLE 1. Clinical presentation and outcome in 3 patients at the bottom of the sulcus, through which such arteries may pass to perfuse the corona radiata. We hypothesized that the gray matter at the bottom of the periinsular sulcus closest to the paraventricular part of the pyramidal tract would contribute to its blood supply. This is because ischemic changes to the pyramidal tract caused by insular artery occlusion have been reported to extend from the top of the insular cortex to the deep white matter close to the lateral ventricle.3,14 Our hypothesis was verified in Case 2; that is, ischemia in the centrum semiovale developed underneath the area where the bottom of the periinsular sulcus was totally removed but not underneath the preserved area. We demonstrated that our simple strategy could provide clinically meaningful outcome in some cases for epilepsy surgery in high-risk anatomical locations. Exactly how large a volume of tissue should be preserved to avoid ischemic changes to the pyramidal tract is not yet sufficiently clear. In addition, incomplete resection may result in inadequate seizure control. Our results suggest that smaller residual lesion size leads to better seizure control, supporting the idea that volume reduction of epileptogenic tissue and/or disconnection of the epileptic network within and around the lesion could suppress epileptogenicity sufficiently to allow control by antiepileptic medications. Certainly, the chance of seizure freedom is compromised by preservation of the epileptic tissue in this strategy. Therefore, careful continuation of antiepileptic drugs is important postoperatively. Further case studies with longterm follow-up are necessary to validate our strategy. Scalp EEG FIG. 1. Conceptual schema of the surgical strategy (coronal view). The pyramidal tract and perfusing vessels (dotted lines), including the lenticulostriate artery (LSA), long insular artery (LIA), and long medullary artery (LMA), are illustrated. Gray matter at the bottom of the periinsular sulcus (black area) is preserved to avoid ischemia of the pyramidal tract when resecting insular and opercular cortices (dashed lines). Interictal Ictal Lesion Vol in mm3 Residual Postop Neurol Deficit Histol Sz Outcome* (FU) Resective epilepsy surgery of the insula J Neurosurg June 9, 2017 3 N. Ikegaya et al. FIG. 2. Preoperative (left) and postoperative (right) MR images obtained in Cases 1 (A), 2 (B), and 3 (C). Arrows on preoperative MR images indicate the area of the epileptogenic lesion in each case. Arrowheads on postoperative MR images indicate the preserved area of the insula. The location of the pyramidal tract estimated by diffusion tensor MRI fiber tracking is shown in red-orange. Gray matter at the posterior part of the bottom of the periinsular sulcus was preserved to avoid ischemic complication of the pyramidal tract. In Case 2, postoperative DWI-MRI (lower right in B) shows ischemic changes to the centrum semiovale underneath the anterior insula where the bottom of the periinsular sulcus was totally removed but not underneath the preserved area. Figure is available in color online only. Conclusions We described a surgical technique that was developed in order to avoid ischemic complications at the pyramidal tract in patients undergoing resective epilepsy surgery around the superoposterior part of the insula. That is, we spared a small piece of gray matter at the bottom of the periinsular sulcus, where perfusing vessels to the pyramidal tract originate in passing through the insular cortex. This method was successfully applied in 3 patients harboring focal cortical dysplasia at the insula and frontoparietal operculum surrounding the periinsular sulcus. Acknowledgments We wish to acknowledge Dr. Masayuki Sasaki, Dr. Kenji Sugai, Dr. Eiji Nakagawa, Dr. Takashi Saito, and Dr. Yuuko Motohashi of 4 J Neurosurg June 9, 2017 the National Center of Neurology and Psychiatry (NCNP) for their clinical support. This study was supported in part by an Intramural Research Grant (28-4: Clinical Research for Diagnostic and Therapeutic Innovations in Developmental Disorders) for Neurological and Psychiatric Disorders of NCNP. References 1. Bertalanffy H, Gilsbach JM, Eggert HR, Seeger W: Microsurgery of deep-seated cavernous angiomas: report of 26 cases. Acta Neurochir (Wien) 108:91–99, 1991 2. Duffau H: A personal consecutive series of surgically treated 51 cases of insular WHO Grade II glioma: advances and limitations. J Neurosurg 110:696–708, 2009 3. Finet P, Nguyen DK, Bouthillier A: Vascular consequences of operculoinsular corticectomy for refractory epilepsy. J Neurosurg 122:1293–1298, 2015 Resective epilepsy surgery of the insula 4. 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Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Ikegaya. Study supervision: Iwasaki, Kawahara, Otsuki. Supplemental Information Previous Presentations Parts of this work were presented in poster form at the annual meeting of the American Epilepsy Society, Philadelphia, PA, December 4–8, 2015. Correspondence Naoki Ikegaya, 4-1-1 Ogawahigashimachi, Kodaira, Tokyo 1870031, Japan. email: ikegaya-tuk@umin.ac.jp. J Neurosurg June 9, 2017 5