Epilepsy Surgery for Skull-Base Temporal Lobe Encephaloceles: Should We Spare the Hippocampus from Resection?

The neurosurgical treatment of skull base temporal encephalocele for patients with epilepsy is variable. We describe two adult cases of temporal lobe epilepsy (TLE) with spheno-temporal encephalocele, currently seizure-free for more than two years after anterior temporal lobectomy (ATL) and lesionectomy sparing the hippocampus without long-term intracranial electroencephalogram (EEG) monitoring. Encephaloceles were detected by magnetic resonance imaging (MRI) and confirmed by maxillofacial head computed tomography (CT) scans. Seizures were captured by scalp video-EEG recording. One case underwent intraoperative electrocorticography (ECoG) with pathology demonstrating neuronal heterotopia. We propose that in some patients with skull base temporal encephaloceles, minimal surgical resection of herniated and adjacent temporal cortex (lesionectomy) is sufficient to render seizure freedom. In future cases, where an associated malformation of cortical development is suspected, newer techniques such as minimally invasive EEG monitoring with stereotactic-depth EEG electrodes should be considered to tailor the surrounding margins of the resected epileptogenic zone.


Introduction
An encephalocele refers to the protrusion of brain tissue, meninges, and cerebral spinal fluid (CSF) through a calvarial or skull base defect. Most of these lesions are due to congenital defects, although they can be acquired following trauma, surgery, or infection [1,2]. When associated with temporal lobe seizures, encephaloceles are associated with bony defects in the middle cranial fossa [3,4]. Associated defects have also been localized to the petrosal bone [5,6], cribriform plate [7], and diffusely throughout the skull.
Imaging is often reported to be normal, with the skull-base lesion noted only upon reassessment of initial neuroimaging [3,5,6,8,9]. Magnetic resonance imaging (MRI) and high-resolution CT scan imaging of the skull base allow for identification of these rare lesions and provide critical information  Hippocampus and amygdala were resected in five patients; the samples revealed normal mesial structures (n = 2), gliosis (n = 2), or small focal neuronal loss in CA2 area interpreted as possible mild hippocampal degeneration (n = 1).
Surgical approaches vary depending on seizure type, origin of encephalocele (congenital vs. acquired), location (temporal vs. extra-temporal), the type of brain lesion seen on MRI (with associated signal abnormality vs. none), and concordance of studies (scalp EEG MRI, positron emission tomography (PET) and neuropsychological testing). Most recently, stereotactic-depth EEG electrode implantation was used in one case report of temporal lobectomy and amygdalectomy alone, sparing the hippocampus, with reported seizure freedom [16].

Case Series
We report two cases of temporal lobe encephalocele, one congenital and another traumatic, which were treated with local excision and reparation of the encephalocele. Both cases underwent temporal lobe neocortical resection, sparing the hippocampus. Both patients have remained with Engel class-I surgical outcome (42 months for case 1 and 23 months for case 2). Preoperative MRI ( Figure 1A,B) and maxillofacial CT scan ( Figure 1C) showed a large temporo-sphenoidal encephalocele with a defect in the floor of the middle cranial fossa with herniation of gliotic temporal and frontal opercular tissue into the defect.
AH: amygdalohippocampectomy, ATL: anterior temporal lobectomy, EEG; electroencephalography, F: female, FCD-IC: focal cortical dysplasia, with abnormal radial and tangential cortical amination according to Blumcke's classification, HC: hippocampus, L: left, M: male, Mo: month, MRI: magnetic resonance imaging, NA: not available, R: right, Szs: seizures, T2: Time 2, y: year. * Samples from the base of the encephalocele were obtained from all 12 surgically treated patients. All of these samples showed gliosis and five patients (42%) had mild cortical laminar disorganization. The temporal lobe samples showed gliosis in 11 patients and heterotopic neurons in four patients. Hippocampus and amygdala were resected in five patients; the samples revealed normal mesial structures (n = 2), gliosis (n = 2), or small focal neuronal loss in CA2 area interpreted as possible mild hippocampal degeneration (n = 1).

Case Series
We report two cases of temporal lobe encephalocele, one congenital and another traumatic, which were treated with local excision and reparation of the encephalocele. Both cases underwent temporal lobe neocortical resection, sparing the hippocampus. Both patients have remained with Engel class-I surgical outcome (42 months for case 1 and 23 months for case 2).

Case 1: 24-Year-Old Ambidextrous, Bilingual (English and German) Man with Seizures Since 22 Years of Age. Seizure Semiology: Ictal Expressive Aphasia, Right Forced Head and Eyes Deviation, Lip-Smacking, and Sensation of Fear
Preoperative MRI ( Figure 1A,B) and maxillofacial CT scan ( Figure 1C) showed a large temporosphenoidal encephalocele with a defect in the floor of the middle cranial fossa with herniation of gliotic temporal and frontal opercular tissue into the defect.  Scalp video-EEG monitoring captured five complex partial seizures, localized broadly to the left fronto-temporal channels (T3/T5/O1 and FP1/F3/F7). The ictal pattern was from EEG electrodecremental response, followed by 1.5-2 Hz rhythmic activity then 12-15 Hz low amplitude rhythmic activity (maximally at T5/O1), which is not typical for medial temporal lobe onset seizure but rather for neocortical onset seizure [22] (Figure 2). Electrocardiogram (ECG) correlated with tachycardia up to 120 bpm.
Intraoperative ECoG monitoring with three 2 × 4 grids were used to cover the left frontal operculum, anterior temporal tip containing the dysplastic tissue, and mid-posterior/lateral temporal cortex. One 1 × 8 strip was placed in the inferior medial and anterior temporal lobe. The strip and grid located in the inferior and anterior temporal lobes revealed occasional dysmorphic spikes anteriorly.
Epileptiform discharges were anteriorly located with the temporal pole and possibly the frontal opercular region. There was no evidence of epileptiform discharges coming from the medial-posterior temporal lobe strips.
Surgical approach included the insertion of a lumbar cerebrospinal fluid intrathecal drain, harvest of abdominal fat through a separate incision, left temporal craniotomy and temporal lobectomy with intraoperative electrocorticography, fronto-zygomatic craniotomy, and repair of left sphenonasal encephalocele with microscopic dissection. The ECoG findings allowed for identification of a 3-cm margin from the temporal tip for partial resection.
Scalp video-EEG monitoring captured five complex partial seizures, localized broadly to the left fronto-temporal channels (T3/T5/O1 and FP1/F3/F7). The ictal pattern was from EEG electrodecremental response, followed by 1.5-2 Hz rhythmic activity then 12-15 Hz low amplitude rhythmic activity (maximally at T5/O1), which is not typical for medial temporal lobe onset seizure but rather for neocortical onset seizure [22] (Figure 2). Electrocardiogram (ECG) correlated with tachycardia up to 120 bpm. Intraoperative ECoG monitoring with three 2 × 4 grids were used to cover the left frontal operculum, anterior temporal tip containing the dysplastic tissue, and mid-posterior/lateral temporal cortex. One 1 × 8 strip was placed in the inferior medial and anterior temporal lobe. The strip and grid located in the inferior and anterior temporal lobes revealed occasional dysmorphic spikes anteriorly.
Epileptiform discharges were anteriorly located with the temporal pole and possibly the frontal opercular region. There was no evidence of epileptiform discharges coming from the medialposterior temporal lobe strips.
Surgical approach included the insertion of a lumbar cerebrospinal fluid intrathecal drain, harvest of abdominal fat through a separate incision, left temporal craniotomy and temporal lobectomy with intraoperative electrocorticography, fronto-zygomatic craniotomy, and repair of left sphenonasal encephalocele with microscopic dissection. The ECoG findings allowed for identification of a 3-cm margin from the temporal tip for partial resection.
Surgical pathology of the resected tissue showed benign cerebral parenchyma and focal neuronal heterotropia within the deeper portion of the white matter ( Figure 3). There was no evidence of gliosis or inflammation. There were no abnormal inclusions, myelin-related or metabolic abnormalities, or neoplastic changes. Surgical pathology of the resected tissue showed benign cerebral parenchyma and focal neuronal heterotropia within the deeper portion of the white matter ( Figure 3). There was no evidence of gliosis or inflammation. There were no abnormal inclusions, myelin-related or metabolic abnormalities, or neoplastic changes. Outcome: Seizure frequency prior to surgery was 4-5 times per week. He has remained seizurefree for 42 months since his surgery, during which levetiracetam was discontinued and lacosamide was reduced from 200 mg bid to 100 mg bid. Patient was able to continue his collegiate studies and scored 90th percentile on his Medical College Admission Test (MCAT). Post-operative MRI showed preserved left hippocampus ( Figure 4A) and the left temporal surgical bed ( Figure 4B). The amygdala was resected as well ( Figure 4C). Outcome: Seizure frequency prior to surgery was 4-5 times per week. He has remained seizure-free for 42 months since his surgery, during which levetiracetam was discontinued and lacosamide was reduced from 200 mg bid to 100 mg bid. Patient was able to continue his collegiate studies and scored 90th percentile on his Medical College Admission Test (MCAT). Post-operative MRI showed preserved left hippocampus ( Figure 4A) and the left temporal surgical bed ( Figure 4B). The amygdala was resected as well ( Figure 4C). Outcome: Seizure frequency prior to surgery was 4-5 times per week. He has remained seizurefree for 42 months since his surgery, during which levetiracetam was discontinued and lacosamide was reduced from 200 mg bid to 100 mg bid. Patient was able to continue his collegiate studies and scored 90th percentile on his Medical College Admission Test (MCAT). Post-operative MRI showed preserved left hippocampus ( Figure 4A) and the left temporal surgical bed ( Figure 4B). The amygdala was resected as well ( Figure 4C).

Case 2: 66-Year-Old Right-Handed Man with Intractable Epilepsy since the Age of 43 Years, after He Was Struck on Forehead at Work by a Pump While Pumping Oil from a Compressor. Seizure Semiology Consisted of Dizziness, Starring Off, Lip-Smacking, Excessive Drooling, Right Hand Rolling Movements, and Occasional Bilateral Tonic-Clonic Seizures
Preoperative MRIs in 2009 and 2013 were reported as normal (1.5 Tesla). Preoperative highresolution 3.0 Tesla MRI showed herniated right temporal pole encephalocele ( Figure 5). Both hippocampi appeared normal and symmetric on MRI ( Figure 5C).  Scalp video-EEG monitoring captured nine stereotyped electroclinical seizures (starring off, lipsmacking with occasional right manual automatisms). Ictal onset originated from the right anterior and mid-temporal channels. The electrographic ictal pattern consisted of rhythmic 2-3 Hz activity, suggesting neocortical rather than mesial temporal onset seizure pattern [22] (Figure 6). Scalp video-EEG monitoring captured nine stereotyped electroclinical seizures (starring off, lip-smacking with occasional right manual automatisms). Ictal onset originated from the right anterior and mid-temporal channels. The electrographic ictal pattern consisted of rhythmic 2-3 Hz activity, suggesting neocortical rather than mesial temporal onset seizure pattern [22] (Figure 6). right temporal cortex (arrows).
Scalp video-EEG monitoring captured nine stereotyped electroclinical seizures (starring off, lipsmacking with occasional right manual automatisms). Ictal onset originated from the right anterior and mid-temporal channels. The electrographic ictal pattern consisted of rhythmic 2-3 Hz activity, suggesting neocortical rather than mesial temporal onset seizure pattern [22] (Figure 6). Neuropsychological testing showed relatively intact neuropsychological functioning with some areas of relative weaknesses, including evidence of weaker nonverbal (visual) new learning and memory compared to his auditory (verbal) new learning and memory as well as significant visuoconstructional weaknesses. The absence of any obvious nonverbal (visual) memory impairments provided support for the absence of any right mesial temporal dysfunction and the greater likelihood of seizure control with selective resection of the inferior temporal lobe. Neuropsychological testing showed relatively intact neuropsychological functioning with some areas of relative weaknesses, including evidence of weaker nonverbal (visual) new learning and memory compared to his auditory (verbal) new learning and memory as well as significant visuoconstructional weaknesses. The absence of any obvious nonverbal (visual) memory impairments provided support for the absence of any right mesial temporal dysfunction and the greater likelihood of seizure control with selective resection of the inferior temporal lobe.
Surgical approach included right temporal craniotomy, repair of lateral sphenoid encephalocele with repair of dural defect and rotational temporalis muscle and fascial flap, partial resection of right middle and inferior temporal gyrus for resection of seizure focus, and lumbar drain placement.
To address the seizure focus, the middle and inferior temporal gyri were identified and cauterized. Then, a corticotomy was performed followed by partial resection of the middle and inferior temporal gyri.
Outcome: Seizure occurred several times per month before surgery. He has remained seizure-free for 23 months since surgery. Seizure medications were reduced, during which lamotrigine was reduced from 900 mg to 600 mg daily and pregabalin was switched to gabapentin (from insurance perspective). Patient also has early onset Parkinson's disease and developed insomnia and restless leg syndrome. Clonazepam was added at 1 mg at night. Pathology was not done due to the use of cauterized resection. A post-operative MRI (Figure 7) showed the surgical cavity in the region of the previously noted encephalocele with a small residual fluid collection in the right infra-temporal fossa ( Figure 7B). reduced from 900 mg to 600 mg daily and pregabalin was switched to gabapentin (from insurance perspective). . Patient also has early onset Parkinson's disease and developed insomnia and restless leg syndrome. Clonazepam was added at 1 mg at night. Pathology was not done due to the use of cauterized resection. A post-operative MRI (Figure 7) showed the surgical cavity in the region of the previously noted encephalocele with a small residual fluid collection in the right infra-temporal fossa ( Figure 7B).

Discussion
Meningoencephaloceles can be associated with microscopic congenital malformations. As such, it is important to realize that the meningoencephalocele may be the "the tip of the iceberg" and the diagnosis should lead one to carefully search for evidence of an underlying malformation of cortical development. However, seizure rates and associated cortical congenital abnormalities are probably more uncommon in this rare form of encephaloceles compared to non-skull base encephaloceles (cranial-vault) seen in pediatric patients, which commonly have multifocal cortical abnormalities and generalized epilepsy [23].
The optimal surgical strategy for intractable epilepsy patients with a temporal encephalocele is not well established. Tailored surgery of temporal pole encephaloceles was described by Giulioni et al. [10]. As it has been reported before, local excision (in extra-temporal cases) has a similar chance of seizure freedom as lobectomy (in temporal cases), regardless of the location of the encephalocele (Faulkner). In our review of nearly 44 cases published so far, a conservative surgical approach was seen more often than the larger resection of the anterior temporal lobe, including the amygdala and the hippocampus combined.
We describe here two cases of temporal lobe encephaloceles and related epilepsy in which tailored temporal lobe resection was performed. The left (dominant) hippocampus was preserved in case 1 due to the demanding high cognitive/memory function of a college student, and the right (non-

Discussion
Meningoencephaloceles can be associated with microscopic congenital malformations. As such, it is important to realize that the meningoencephalocele may be the "the tip of the iceberg" and the diagnosis should lead one to carefully search for evidence of an underlying malformation of cortical development. However, seizure rates and associated cortical congenital abnormalities are probably more uncommon in this rare form of encephaloceles compared to non-skull base encephaloceles (cranial-vault) seen in pediatric patients, which commonly have multifocal cortical abnormalities and generalized epilepsy [23].
The optimal surgical strategy for intractable epilepsy patients with a temporal encephalocele is not well established. Tailored surgery of temporal pole encephaloceles was described by Giulioni et al. [10]. As it has been reported before, local excision (in extra-temporal cases) has a similar chance of seizure freedom as lobectomy (in temporal cases), regardless of the location of the encephalocele (Faulkner). In our review of nearly 44 cases published so far, a conservative surgical approach was seen more often than the larger resection of the anterior temporal lobe, including the amygdala and the hippocampus combined.
We describe here two cases of temporal lobe encephaloceles and related epilepsy in which tailored temporal lobe resection was performed. The left (dominant) hippocampus was preserved in case 1 due to the demanding high cognitive/memory function of a college student, and the right (non-dominant) hippocampus was preserved in case 2 due to patient choice and concern of worsening memory in the setting of his advanced age.
In the presence of electrographic or radiographic evidence of wide mesial structure involvement, the approach of ATLAH is reasonable, as shown by Panov et al., who reported four out of six surgical cases of temporal encephaloceles treated with ATLAH. However, two of those six cases were treated, similarly to our cases, with lesionectomy and temporal lobe disconnection. Our cases also illustrate that temporal lobe encephaloceles can be treated successfully with a conservative surgical approach sparing the mesial temporal structures.
The result of post-operative seizure freedom after encephalocele repair with only limited temporal lobe resection, sparing the hippocampus, demonstrates the possibility and the importance of preserving the vital memory function of the hippocampus without jeopardizing post-surgical seizure freedom.
As shown by De Souza et al., most recent advances in stereotactic depth electrode implantation may provide us with better options for intracranial EEG monitoring in future cases, which would allow us to identify the epileptogenic zone more precisely for better outcome