Is intracranial electroencephalography useful for planning resective surgery in intractable epilepsy with ulegyria?

Yutaro Takayama Department of Neurosurgery, National Center Hospital of Neurology and Psychiatry, Kodaira, Tokyo; and
Department of Neurosurgery, Yokohama City University Graduate School of Medicine, Yokohama, Kanagawa, Japan

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Naoki Ikegaya Department of Neurosurgery, Yokohama City University Graduate School of Medicine, Yokohama, Kanagawa, Japan

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Keiya Iijima Department of Neurosurgery, National Center Hospital of Neurology and Psychiatry, Kodaira, Tokyo; and

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Yuiko Kimura Department of Neurosurgery, National Center Hospital of Neurology and Psychiatry, Kodaira, Tokyo; and

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Norihiro Muraoka Department of Neurosurgery, National Center Hospital of Neurology and Psychiatry, Kodaira, Tokyo; and

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Yuu Kaneko Department of Neurosurgery, National Center Hospital of Neurology and Psychiatry, Kodaira, Tokyo; and

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Tetsuya Yamamoto Department of Neurosurgery, Yokohama City University Graduate School of Medicine, Yokohama, Kanagawa, Japan

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Masaki Iwasaki Department of Neurosurgery, National Center Hospital of Neurology and Psychiatry, Kodaira, Tokyo; and

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OBJECTIVE

Intractable epilepsy patients with ulegyria could be candidates for resective surgery. Complete resection of ulegyria in the epileptogenic hemisphere is associated with favorable seizure outcome, although the risk of postoperative functional deficits is higher. The authors evaluated the extent of resection and postsurgical outcomes in epilepsy patients with ulegyria who underwent intracranial electroencephalography (iEEG) monitoring prior to resection to clarify the efficacy of iEEG-guided partial resection of ulegyria.

METHODS

Ten consecutive epilepsy patients with ulegyria (7 males and 3 females, age range at surgery 7–34 years) underwent iEEG prior to resective surgery between 2011 and 2017 with a minimum follow-up of 12 months (range 12–72 months). The diagnosis of ulegyria was based on the typical pattern of cortical atrophy especially at the bottom of the sulcus on MRI. An iEEG study was indicated after comprehensive preoperative evaluations, including high-field MRI, long-term video-EEG, magnetoencephalography, and FDG-PET. The resection planning was based on iEEG analysis. Total lesionectomy was not always performed, as preservation of cortical function was prioritized.

RESULTS

Ulegyria was seen in the occipital and/or parietal lobe in 9 patients and bilaterally in 5 patients. Ictal EEG onset involved the temporal neocortex in 6 patients. Intracranial electrodes were implanted unilaterally in all except 1 patient with bilateral lesions. The extent of MRI lesion was covered by the electrodes. Seizure onset zones (SOZs) and irritative zones (IZs) were identified in all patients. SOZs and IZs were completely resected in 8 patients but were only partially removed in the remaining 2 patients because the eloquent cortices and the epileptogenic zones overlapped. Ulegyria of the epileptogenic side was totally resected in 1 patient. Seizure freedom was achieved in 4 patients, including 3 after partial lesionectomy. Extended resection of the temporal neocortex was performed in 4 patients, although postoperative seizure freedom was achieved only in 1 of these patients. Visual field deficit was seen in 4 patients. Three of 5 patients with bilateral lesions achieved seizure freedom after unilateral resective surgery.

CONCLUSIONS

Intracranial EEG–guided partial lesionectomy provides a reasonable chance of postoperative seizure freedom with a lower risk of functional deficits. Patients with bilateral ulegyria should not be excluded from consideration as surgical candidates.

ABBREVIATIONS

EEG = electroencephalography; IED = interictal epileptiform discharge; iEEG = intracranial EEG; ILAE = International League Against Epilepsy; IZ = irritative zone; MEG = magnetoencephalography; SOZ = seizure onset zone.

OBJECTIVE

Intractable epilepsy patients with ulegyria could be candidates for resective surgery. Complete resection of ulegyria in the epileptogenic hemisphere is associated with favorable seizure outcome, although the risk of postoperative functional deficits is higher. The authors evaluated the extent of resection and postsurgical outcomes in epilepsy patients with ulegyria who underwent intracranial electroencephalography (iEEG) monitoring prior to resection to clarify the efficacy of iEEG-guided partial resection of ulegyria.

METHODS

Ten consecutive epilepsy patients with ulegyria (7 males and 3 females, age range at surgery 7–34 years) underwent iEEG prior to resective surgery between 2011 and 2017 with a minimum follow-up of 12 months (range 12–72 months). The diagnosis of ulegyria was based on the typical pattern of cortical atrophy especially at the bottom of the sulcus on MRI. An iEEG study was indicated after comprehensive preoperative evaluations, including high-field MRI, long-term video-EEG, magnetoencephalography, and FDG-PET. The resection planning was based on iEEG analysis. Total lesionectomy was not always performed, as preservation of cortical function was prioritized.

RESULTS

Ulegyria was seen in the occipital and/or parietal lobe in 9 patients and bilaterally in 5 patients. Ictal EEG onset involved the temporal neocortex in 6 patients. Intracranial electrodes were implanted unilaterally in all except 1 patient with bilateral lesions. The extent of MRI lesion was covered by the electrodes. Seizure onset zones (SOZs) and irritative zones (IZs) were identified in all patients. SOZs and IZs were completely resected in 8 patients but were only partially removed in the remaining 2 patients because the eloquent cortices and the epileptogenic zones overlapped. Ulegyria of the epileptogenic side was totally resected in 1 patient. Seizure freedom was achieved in 4 patients, including 3 after partial lesionectomy. Extended resection of the temporal neocortex was performed in 4 patients, although postoperative seizure freedom was achieved only in 1 of these patients. Visual field deficit was seen in 4 patients. Three of 5 patients with bilateral lesions achieved seizure freedom after unilateral resective surgery.

CONCLUSIONS

Intracranial EEG–guided partial lesionectomy provides a reasonable chance of postoperative seizure freedom with a lower risk of functional deficits. Patients with bilateral ulegyria should not be excluded from consideration as surgical candidates.

In Brief

The authors evaluated the extent of resection and postsurgical outcomes in epilepsy patients with ulegyria who underwent intracranial electroencephalography (iEEG) monitoring prior to resection to clarify the efficacy of iEEG-guided partial resection of ulegyria.

Ulegyria has been sporadically described since the first report in 1899.1 The main cause of ulegyria is hypoxic ischemic brain injury during the perinatal period, but other causes are known, including trauma such as shaken infant syndrome and perinatal hypoglycemia.4,6 Ulegyria, the so-called mushroom-like gyri, appears as typical atrophy of the cortex especially at the bottom of the sulcus on MRI.3,5,9

Ulegyria is frequently associated with epilepsy that tends to be drug resistant and so is a candidate for epilepsy surgery.2,7,8,10 Ulegyria often develops bilaterally in the frontoparietal, occipital, or perisylvian areas because ischemic brain injuries typically occur in the watershed areas.6 Coexistence with hippocampal sclerosis has also been reported. Moreover, the lesion size varies from focal to hemispheric. Therefore, presurgical assessment of drug-resistant epilepsy with ulegyria is complicated, and the optimal surgical strategy for these patients has not been established.3 Complete resection of ulegyria is associated with favorable seizure outcome.8 However, total lesionectomy is occasionally hampered by the close relationship with eloquent areas or by large or bilateral lesions. The effectiveness of partial lesionectomy guided by intracranial electroencephalography (iEEG) is not well understood.

The present study evaluated the extent of resection and postsurgical seizure outcomes in epilepsy patients with ulegyria who underwent iEEG monitoring prior to resection to clarify whether total lesionectomy is necessary and whether iEEG is useful for planning resective surgery in intractable epilepsy with ulegyria.

Methods

Patient Population

A total of 253 patients (264 surgeries) underwent resective epilepsy surgery at our tertiary epilepsy center from 2011 to 2017. Ten patients (7 males and 3 females) were identified who underwent resective surgery for drug-resistant epilepsy with ulegyria and were followed up for at least 12 months after resection. All 10 patients underwent iEEG monitoring prior to resection. Ulegyria was diagnosed by our board-certified radiologists and fulfilled the following MRI criteria: atrophy of the affected gyri located in watershed areas between the territories of the major cerebral arteries, consisting of thin cortex in the deep portion of the sulci with abnormal intensity, whereas the crown of the same gyri had normal thickness and intensity; and subcortical white matter volume loss associated with intensity abnormalities.3,5,9 The study was approved by the ethics committee at the National Center of Neurology and Psychiatry, Tokyo, Japan.

Presurgical Noninvasive Evaluations

All 10 patients underwent comprehensive epilepsy evaluations, including medical interview, neurological and neuropsychological examinations, long-term video-electroencephalography (EEG), MRI, FDG-PET, and magnetoencephalography (MEG). Epilepsy histories were obtained from the patient and, when necessary, his or her relatives, and the semiology of their habitual seizures was confirmed. Scalp EEG was recorded with the standard 10–20 system of electrode placement, including bilateral anterior temporal electrodes. Three-tesla brain MRI was performed, including 3D FLAIR, double inversion recovery, and T1- and T2-weighted imaging. The extent of the MRI lesion was defined in accordance with the MRI criteria.

Intracranial EEG Monitoring

Electrode placement was planned based on the results of noninvasive evaluations. Subdural electrodes were placed around the MRI lesion. Additional depth electrodes were applied when necessary.

Seizure onset zone (SOZ) was defined as an area showing unequivocal iEEG changes during the ictal onset phase. Interictal epileptiform discharges (IEDs) were reviewed, and the area of frequent IEDs was defined as the irritative zone (IZ). Functional mapping with direct electrical cortical stimulation was also performed when necessary. Intracranial EEG findings were reviewed at our presurgical EEG conference attended by board-certified epileptologists.

Surgical Plan

Extent of resection was determined based on the iEEG findings in preference to the extent of the MRI lesion. The ulegyria was totally resected only when epileptic EEG abnormalities co-occurred. Preservation of eloquent cortices was attempted even if they were located within the SOZ and IZ.

Postsurgical Evaluation

All patients were followed up through outpatient visits or postoperative admissions for evaluation. Postsurgical seizure outcome was classified using the International League Against Epilepsy (ILAE) seizure outcome classification.11 EEG, MRI, and neuropsychological tests were performed 12 months after surgery. The relationships between extent of resection and extent of MRI lesion and seizure outcome were investigated.

Results

Clinical Characteristics

Patient age at seizure onset ranged from 2 to 20 years (median 5.5 years). Age at surgery ranged from 7 to 34 years (median 12.5 years). Seven of the 10 patients had a history of perinatal insult, including neonatal hypoglycemia (cases 1–4), vacuum extraction (cases 6 and 7), and trauma due to shaking injury (case 5). The patient in case 10 had anterior temporal ulegyria caused by severe head trauma at the age of 18 years. The remaining 2 patients had a history of Kawasaki disease (case 8) and simple febrile seizure (case 9), which were not related as a cause of ulegyria. No patient had preoperative visual field disturbance. Ulegyria involved the occipital and/or parietal lobe in 9 patients (Table 1). Five patients had ulegyria bilaterally.

TABLE 1.

Clinical characteristics prior to resective surgery

Case No.SexAge at Seizure Onset (yrs)Age at Surgery (yrs)History of Precipitating Neonatal EventLocation of UlegyriaSeizure SemiologySeizure Frequency
1M57HypoglycemiaBilat occipitalVisual aura → tonic3–6/day
2M313HypoglycemiaBilat occipitalHyperkinetic6–7/day
3F810HypoglycemiaBilat POUnclassified aura → tonic3–4/day
4M28HypoglycemiaBilat POVisual aura → IA → automatism5–10/day
5F312Shaking injuryBilat FPOIA3–4/day
6M622Vacuum extractionRt occipitalIA → tonic → sGTCS2–3/wk
7F511Vacuum extractionLt POIA1–2/wk
8M1015NoneRt POVisual aura → IA → automatism0–2/day
9M623NoneLt parietalSensory aura → IA1–2/day
10M2034NoneRt FTIA → automatism2–3/mo

FPO = fronto-parieto-occipital; FT = frontotemporal; IA = impaired awareness; PO = parietooccipital; sGTCS = secondary generalized tonic-clonic seizure.

Focal impaired awareness seizures were seen in 7 patients and were associated with oral or hand automatism in 3 patients; in 1 patient, they evolved to bilateral tonic-clonic seizure. Five patients showed various types of aura: visual illusion in 2 (cases 1 and 8), blindness in 1 (case 4), dysesthesia in 1 (case 9), and unclassified feeling in 1 (case 3).

Presurgical Noninvasive Evaluation

Scalp EEG detected IEDs from the unilateral temporal region in 4 patients, unilateral temporooccipital region in 3, bilateral occipital regions in 1, and unilateral multiple regions in 2 (Table 2). Habitual seizures were recorded during video-EEG monitoring in all patients. Ictal EEG changes started from the temporooccipital region in 3 patients, temporal region in 2, vertex region in 1, frontotemporal region in 1, and the right hemisphere diffusely in 3. Ictal activity involved the temporal region associated with focal impaired awareness seizures in 6 patients, despite the MRI lesion being located in the occipital and/or parietal region. FDG-PET demonstrated hypometabolic area overlapping with the MRI lesion in all patients, although the hypometabolism was detected only in the epileptogenic hemisphere in 2 patients with bilateral ulegyria (cases 2 and 4). Equivalent current dipoles of MEG spikes were estimated unilaterally in 5 patients. The location of the dipoles was consistent with the results of scalp EEG in 4 of these 5 patients.

TABLE 2.

Presurgical noninvasive and invasive evaluation

Scalp EEGIntracranial EEG
Case No.InterictalIctalFDG-PETMEGLocation of ElectrodeIZSOZ
1Lt TOLt TOBilat occipitalLt occipitalLt TOLt medial occipital (cuneus)Lt medial occipital, basal temporal (cuneus-PHG)
2Lt TOLt TOLt occipitalBilat occipitalLt TOCPLt lat & medial occipitalLt lat & medial occipital
3MultifocalVertexBilat POBilat PORt OCPRt medial parietal (SPL)Rt medial parietal (SPL), central
4Bilat occipitalBilat FTRt POBilat FTPRt TOP; lt TOBilat occipitalRt lat & medial PO (cuneus-precuneus); lt medial & basal TO (PCG-LG-PHG)
5Lt TOLt TOLt TO; rt FPOLt occipital; rt POLt TOCPLt basal & lat occipital; lt basal temporal (LG-PHG)Lt basal & lat occipital; lt basal temporal (LG-PHG)
6Rt temporalRt temporalRt FPORt temporalRt TOCPRt lat & medial occipital; rt basal temporal (LG-PHG-FG-ITG)Rt lat & medial occipital; rt basal temporal (LG-PHG-FG-ITG)
7MultifocalRt hemiLt TOLt hemiLt TOCPLt lat & basal TOLt lat & basal TO
8Rt temporalRt hemiRt FTPBilat FPRt TOCPRt lat TO junctionRt lat TO junction
9Lt temporalLt temporalLt PTLt temporalLt TCPLt lat parietal (IPL), STGLt lat parietal (IPL), STG
10Rt temporalRt hemiRt FTRt temporalRt FTRt lat temporal, orbitofrontalRt lat temporal, orbitofrontal

FG = fusiform gyrus; FP = frontoparietal; FTP = fronto-temporo-parietal; hemi = hemispheric; IPL = inferior parietal lobule; ITG = inferior temporal gyrus; lat = lateral; LG = lingual gyrus; OCP = occipito-centro-parietal; PCG = posterior cingulate gyrus; PHG = parahippocampal gyrus; PT = parieto-temporal; SPL = superior parietal lobule; STG = superior temporal gyrus; TCP = temporo-centro-parietal; TO = temporooccipital; TOCP = temporo-occipito-centro-parietal; TOP = temporo-occipito-parietal.

Intracranial EEG Findings

Intracranial electrodes were unilaterally implanted in 9 patients, including 4 with bilateral lesions (cases 1, 2, 3, and 5). The electrodes were placed on the side with the more prominent MRI lesion in these 4 patients, while considering other noninvasive evaluations. Subdural electrodes were placed on the bilateral occipital cortices in the other patient with bilateral lesions (case 4). IEDs were detected in the temporooccipital region in 4 patients (cases 5–8), occipital region in 2 (cases 1 and 2), bilateral occipital regions in 1 (case 4), parietal region in 1 (case 3), parietotemporal region in 1 (case 9), and frontotemporal region in 1 (case 10). Habitual seizures were recorded in all patients. The SOZ was identified in the temporooccipital region in 5 patients (cases 1 and 5–8), occipital region in 1 (case 2), centroparietal region in 1 (case 3), parietotemporal region in 1 (case 9), frontotemporal region in 1 (case 10), and bilateral posterior cortices (left temporooccipital and right parietooccipital) in 1 (case 4). IZs and SOZs were focally localized in all patients, and the location was consistent with the results of scalp EEG in 8 patients (cases 1–6, 8, and 10). Ictal activities were also detected in the temporal region beyond the boundary of the MRI lesion in the 7 patients with occipital and/or parietal ulegyria (cases 1 and 4–9).

Surgical Outcome

The SOZ and IZ were totally removed in the surgical side in 8 patients. Subtotal resection of the SOZ and IZ was performed in the other 2 patients because the iEEG abnormalities extended to the eloquent cortices, the primary somatosensory area in case 3 and the primary visual area in case 5 (Table 3). The MRI lesion was totally resected only in 1 patient (case 8). The mean postsurgical follow-up period was 28 months (range 12–72 months). Four patients achieved seizure freedom (ILAE class 1) at the last follow-up examination, including the patient with total lesionectomy (case 8) (Fig. 1), and 3 of the 9 patients with partial lesionectomy (Figs. 2 and 3). Three of the 5 patients with bilateral lesions obtained seizure freedom. Significant seizure reduction was seen in the other 4 patients (ILAE classes 3 and 4). No meaningful seizure reduction was obtained in 2 patients. Seizure recurrence in those patients was observed within 3 months after resection. Extended resection of the posterior temporal neocortex was performed in 4 patients (cases 5, 7, 8, and 9), although postoperative seizure freedom was achieved only in 1 of these patients. Four patients showed postoperative visual field disturbance, either homonymous hemianopia or lower quadrantanopia.

TABLE 3.

Extent of resection at surgery and postsurgical outcomes

Extent of Resection
Case No.Surgical SideSOZ & IZUlegyriaFollow-Up Duration (mos)Seizure-Free Duration (mos)Postop Seizure FrequencyILAE ClassPostop Complication
1LtTotalPartial2424None1Lower quadrantanopia
2LtTotalPartial3105–6/day5Hemianopia
3RtSubtotal*Partial2222None1None
4RtTotalPartial1313None1None
5LtSubtotalPartial1202–3/wk4None
6RtTotalPartial4001–2/mo4Hemianopia
7LtTotalPartial34010/day5None
8RtTotalTotal1212None1Lower quadrantanopia
9LtTotalPartial1632–3/mo4None
10RtTotalPartial7201–2/yr3None

Primary sensory area was preserved.

Primary visual area was preserved.

FIG. 1.
FIG. 1.

Case 8. Representative patient who achieved seizure freedom after total resection of ulegyria. A: Ictal and/or interictal abnormalities were detected at the red electrode contacts. Extent of the MRI lesion is shown by the white dashed line. Resection containing the SOZ and IZ is shown by the black dashed line. Green dots indicate electrode contacts that did not detect ictal and/or interictal abnormalities. B and C: The MRI lesion was totally removed, and the patient achieved seizure freedom. Figure is available in color online only.

FIG. 2.
FIG. 2.

Case 1. Representative patient who achieved seizure freedom after partial resection of ulegyria. Left: Ictal and/or interictal abnormalities were detected at the red electrode contacts. Extent of occipital ulegyria is shown by the white dashed line. Green dots indicate electrode contacts that did not detect ictal and/or interictal abnormalities. Right: The SOZ and IZ were completely resected. The patient achieved seizure freedom despite incomplete removal of the MRI lesion (white dashed lines). Figure is available in color online only.

FIG. 3.
FIG. 3.

Case 3. Representative patient who achieved seizure freedom after partial resection of the SOZ and ulegyria. A: Ictal and/or interictal abnormalities were detected at the red electrode contacts. Extent of ulegyria is shown by the white dashed line. Resection extent is shown by the black dashed line. The SOZ and IZ were not completely resected because they extended across the central sulcus (white arrowheads). Green dots indicate electrode contacts that did not detect ictal and/or interictal abnormalities. B and C: Partial lesionectomy guided by iEEG was performed. The arrowheads indicate the central sulcus. The anterior part of the ulegyria was removed to preserve the postcentral gyrus. The patient achieved seizure freedom despite incomplete removal of the MRI lesion (white dashed line, C). Figure is available in color online only.

Discussion

Intracranial EEG–guided focal resection surgeries were performed in 10 drug-resistant epilepsy patients with ulegyria, resulting in partial removal of the MRI lesion in 9. Four patients obtained ILAE class 1, and 4 patients had a postoperative visual field deficit. The results indicated that iEEG-guided partial lesionectomy provides a reasonable chance of postoperative seizure freedom with lower risk of functional deficits, although the seizure-free rate is limited compared with total lesionectomy.

Only one previous study considered whether iEEG is useful for resective surgery of ulegyria. Extensive resection of the posterior cortices containing the entire MRI lesion in 10 patients with posterior cortex epilepsy due to ulegyria achieved postoperative seizure freedom in 7, but the SOZ was not completely removed in 4 of 5 patients who underwent preoperative iEEG monitoring.8 Therefore, iEEG was not considered necessary for determining the extent of resection and total lesionectomy of ulegyria was beneficial for seizure relief. Intracranial EEG was only regarded as a step for functional cortical mapping. However, postsurgical visual field deficits appeared in all 10 patients, including 9 with hemianopia. Therefore, extensive resection of the posterior cortices provides a good chance of seizure freedom in compensation for the visual field deficits. Postsurgical seizure outcome was superior to that in our series of patients with occipital ulegyria, but we did not perform extensive resection of the posterior cortices and eventually avoided hemianopia even in the seizure-free patients.

Complete resection of the structural lesion is recommended to achieve a high chance of seizure freedom in epilepsy surgery. In that sense, iEEG may be unnecessary before total lesionectomy, or the surgical indication may be ignored in order to avoid postoperative functional deficits. Certainly, we agree that total lesionectomy without iEEG is the optimal strategy if the lesion is remote from eloquent areas. However, we consider that iEEG is useful in planning focal resective surgery of occipital ulegyria for selected cases, especially if total lesionectomy is expected to cause postoperative functional deficits.

Ulegyria frequently extends to the bilateral hemispheres. Extensive unilateral resection for bilateral perisylvian ulegyria resulted in favorable seizure outcomes.7 Unilateral resection of ulegyria obtained seizure freedom in 4 of 6 patients with bilateral lesions.8 In our study, unilateral resective surgery obtained seizure freedom in 3 of 5 patients with bilateral lesions. Therefore, our results suggest that patients with bilateral ulegyria could be considered as surgical candidates if the epileptogenic zone is estimated in the unilateral hemisphere.

Scalp EEG monitoring is not always useful for the identification of epileptic focus in patients with ulegyria, although none of the patients showed interictal epileptiform discharges.6 Rapid spread of depolarizing activities may cause complexity and misinterpretation of scalp EEG findings. Various seizure symptoms are associated with foci in the frontal, temporal, and parietal cortical regions in patients with occipital ulegyria.3 Such complicated seizure semiology is also caused by rapid spread of ictal activity. The temporal lobe was involved in the ictal EEG onset in 6 of our 9 patients with occipital and/or parietal ulegyria. Our findings suggested rapid propagation of ictal activity toward the temporal lobe from occipital and/or parietal ulegyria. Based on our iEEG study with subdural electrodes placed over the temporooccipital junction, extended resection of the posterior temporal lobe was performed in 4 patients, but postoperative seizure freedom was achieved only in 1. The importance of additional temporal neocortex resection requires further investigation.

The application of iEEG may be helpful for safer and more optimal resection, although the technique still poses problems. The accuracy of electrode implantation is an important point. Precise indwelling of electrodes at predetermined positions is an essential precondition for reliable iEEG analysis. Unfortunately, the present and previous studies of surgery for ulegyria were small. More clinical experience is essential to establish the optimal surgical strategy for epilepsy patients with ulegyria.

Conclusions

Total lesionectomy is not always necessary for seizure freedom in epilepsy surgery in patients with ulegyria. Intracranial EEG–guided partial lesionectomy is a reasonable option, especially if total lesionectomy is expected to cause postoperative functional deficits, although seizure freedom is less likely. Patients with bilateral ulegyria could be considered as surgical candidates if the epileptogenic zone was estimated in the unilateral hemisphere. Rapid propagation of ictal activity toward the temporal lobe from occipital and/or parietal ulegyria was frequently observed. Therefore, the importance of additional temporal neocortex resection should be investigated. Further evaluation including more patients is necessary to establish the efficacy of iEEG-guided resection.

Acknowledgments

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 the National Center of Neurology and Psychiatry.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Iwasaki, Takayama. Acquisition of data: Takayama. Analysis and interpretation of data: Iwasaki, Takayama, Ikegaya, Iijima, Kimura. Drafting the article: Takayama. Critically revising the article: Iwasaki, Takayama, Ikegaya, Yamamoto. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Iwasaki.

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Illustration from Nelson et al. (pp 1516–1526). Artists: Ethan Tyler, Erina He, and Alan Hoofring. Medical Arts, Office of Research Services, National Institutes of Health.

  • FIG. 1.

    Case 8. Representative patient who achieved seizure freedom after total resection of ulegyria. A: Ictal and/or interictal abnormalities were detected at the red electrode contacts. Extent of the MRI lesion is shown by the white dashed line. Resection containing the SOZ and IZ is shown by the black dashed line. Green dots indicate electrode contacts that did not detect ictal and/or interictal abnormalities. B and C: The MRI lesion was totally removed, and the patient achieved seizure freedom. Figure is available in color online only.

  • FIG. 2.

    Case 1. Representative patient who achieved seizure freedom after partial resection of ulegyria. Left: Ictal and/or interictal abnormalities were detected at the red electrode contacts. Extent of occipital ulegyria is shown by the white dashed line. Green dots indicate electrode contacts that did not detect ictal and/or interictal abnormalities. Right: The SOZ and IZ were completely resected. The patient achieved seizure freedom despite incomplete removal of the MRI lesion (white dashed lines). Figure is available in color online only.

  • FIG. 3.

    Case 3. Representative patient who achieved seizure freedom after partial resection of the SOZ and ulegyria. A: Ictal and/or interictal abnormalities were detected at the red electrode contacts. Extent of ulegyria is shown by the white dashed line. Resection extent is shown by the black dashed line. The SOZ and IZ were not completely resected because they extended across the central sulcus (white arrowheads). Green dots indicate electrode contacts that did not detect ictal and/or interictal abnormalities. B and C: Partial lesionectomy guided by iEEG was performed. The arrowheads indicate the central sulcus. The anterior part of the ulegyria was removed to preserve the postcentral gyrus. The patient achieved seizure freedom despite incomplete removal of the MRI lesion (white dashed line, C). Figure is available in color online only.

  • 1

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