Temporal lobe epilepsy and cavernous malformations: surgical strategies and longterm outcomes Fernando L. Vale, Andrew C. Vivas, Jotham Manwaring, Mike R. Schoenberg & Selim R. Benbadis Acta Neurochirurgica The European Journal of Neurosurgery ISSN 0001-6268 Acta Neurochir DOI 10.1007/s00701-015-2592-4
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Author's personal copy Acta Neurochir DOI 10.1007/s00701-015-2592-4
CLINICAL ARTICLE - FUNCTIONAL
Temporal lobe epilepsy and cavernous malformations: surgical strategies and long-term outcomes Fernando L. Vale 1 & Andrew C. Vivas 1 & Jotham Manwaring 1 & Mike R. Schoenberg 2 & Selim R. Benbadis 3
Received: 22 June 2015 / Accepted: 15 September 2015 # Springer-Verlag Wien 2015
Abstract Objective Cerebral cavernous malformations (CCM) of the temporal lobe often present with seizures. Surgical resection of these lesions can offer durable seizure control. There is, however, no universally accepted methodology for assessing and surgically treating these patients. We propose an algorithm to maximize positive surgical outcomes (seizure control) while minimizing post-surgical neurological deficit. Methods A retrospective review of 34 patients who underwent epilepsy surgery for radiographically proven temporal lobe CCM was conducted. Patients underwent a relatively standard work-up for seizure localization. In patients with mesial temporal lobe epilepsy (MTLE), a complete resection of the epileptogenic zone was performed including amygdalo-hippocampectomy in addition to a lesionectomy if not contraindicated by pre-operative work-up. Patients with neocortical epilepsy underwent intraoperative electrocorticography (ECoG)-guided lesionectomy. Results Seizure-free rate for mesial and neocortical (anterior, lateral, and basal) location was 90 vs. 83 %, respectively. The contents of this manuscript have been partially presented at the 64th Southern Neurosurgical Society annual meeting in Feb/2013 (Sarasota/FL). * Fernando L. Vale
[email protected] 1
Department of Neurosurgery & Brain Repair, Morsani College of Medicine, University of South Florida, Tampa, FL, USA
2
Department of Psychiatry and Behavioral Neurosciences, University of South Florida Morsani College of Medicine, Tampa, FL, USA
3
Department of Neurology, Morsani College of Medicine, University of South Florida, Tampa, FL, USA
Complete resection of the lesion, irrespective of location, was statistically significant for seizure control (p=0.018). There was no difference in seizure control based on disease duration or location (p>0.05). Patients with mesial temporal CCM who presented with MTLE were presumed to also have mesial temporal sclerosis (MTS), or dual pathology. These patients underwent routine resection of the mesial structures. Interestingly, patients who had MTLE and basal (neocortical) lesions who underwent a mesial resection for suspected MTS were found not to have dual pathology. Conclusions Patients with temporal lobe CCM should be offered resection for durable seizure control, prevention of secondary epileptogenic foci, and elimination of hemorrhage risk. The preoperative work-up should follow a team approach. Surgical intervention should include complete lesionectomy in all cases. Intra or extra-operative ECoG for neocortical lesions may be beneficial. Management of mesial temporal CCMs (archicortex) should consider resection of a well-defined epileptogenic zone (including mesial structures) due to high probability of pathologically proven MTS. The use of this treatment algorithm is useful for the education and treatment of these patients. Keywords Epilepsy . Cavernous malformation . Temporal lobe . Pathology
Abbreviations MTLE Mesial temporal lobe epilepsy MTS Mesial temporal sclerosis ECoG Electrocorticography MRI Magnetic resonance imaging CCM Cerebral cavernous malformations
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EC EEG
Engel classification Electroencephalography
allows for maximal resection of diseased brain and improved seizure free outcomes, is desired.
Introduction
Methods
Cerebral cavernous malformations (CCM) and benign brain tumors (BBT) are the most common benign lesions of the intra-axial supratentorial brain. These lesions frequently present with new-onset seizures or chronic epilepsy and are the pathologic substrate in up to 30 % of patients with chronic temporal lobe epilepsy [24, 33, 44]. However, patients with BBT are a difficult population to study given the potential for regrowth and pathologic transformation. In contrast, CCM have a better-defined clinical history and subsequently are a more uniform population to study for outcomes data. Supratentorial CCM most frequently present with seizures, a risk that is estimated to be between 1.5 and 2.4 %/ patient-year [3, 10, 26, 27, 39, 45]. Unfortunately, the term Bbenign brain lesion^ as applied to CCM can be misleading when prognosticating quality of life for patients who develop intractable epilepsy. Patients often develop depression, anxiety, and have immense morbidity associated with their disease [5, 22, 37]. Epilepsy surgery can offer patients long-lasting seizure control [35, 43]. Patients who undergo surgical treatment for medically intractable epilepsy have better outcomes in terms of quality of life compared with medically treated patients, and exhibit marked improvements in psychosocial adaptation [6, 19, 28, 37, 43]. The value of medical management with antiepileptic drugs (AED) is well established, however the risk of spontaneous hemorrhage or generation of secondary epileptogenesis is still a concern. There is enough clinical data that support the benefit of surgical intervention in CCM and epilepsy. Most authors report greater than 80 % seizure control with surgery [17, 26, 38, 45]. It is noteworthy that 10–20 % of all CCM can occur in the temporal lobe [25]. In addition, the temporal lobe is also considered to be more epileptogenic than the rest of the supratentorial compartment [34]. As a consequence, this population is considered a more challenging group for seizure management and long-term control. Despite the benefits of early intervention with a reported rate of 80–90 % seizure control for new-onset or sporadic seizures [17], the timing of surgery has been debated. The purpose of this study is to examine the long-term outcome of patients with CCM and seizures of temporallobe origin. We provide a brief review of the current literature and propose a management strategy to maximize positive surgical outcomes (seizure control) in these patients while minimizing post-surgical neurological deficit. Improved understanding of anatomic and physiologic connections (networks) may allow for better outcomes. Accurate identification of the lesion and the entire epileptogenic zone, which
Since 1998, a prospective database has been maintained for all patients referred to our comprehensive epilepsy center. A retrospective review of 579 patients who presented from 1999–2011 was conducted. Of this group, 34 patients underwent epilepsy surgery for radiographically proven temporal lobe CCM. The data analyzed included sex, age at surgery, side of surgery, pre-operative disease duration, and MRI findings prior to surgery. Patients were then followed post-operatively to assess for post-surgical seizure control and complications. Data collection was approved by the university hospital’s Institutional Review Board (IRB) and was performed in accordance with HIPAA regulations. All patients were evaluated by an attending epileptologist and neurosurgeon, and then reviewed by our institution’s epilepsy board. All patients had a trial of anti-epileptics drugs prior to referral to our center and were considered to suffer from pharmaco-resistant epilepsy. Inclusion criteria were adult patients with radiographically proven temporal CCM, seizures, and a minimum follow-up of 36 months. Patients underwent a relatively standardized preoperative workup prior to surgery that included: (1) high-resolution 1.5-T or 3-T magnetic resonance imaging (MRI) including T2WI or susceptibility-weighted imaging (SWI) sequences, (2) longterm video-EEG monitoring if multiple cavernomas, or if a question of correlation existed, (3) functional MRI (fMRI) for patients with lateral neocortical location to assess speech dominance and location, (4) Wada testing was performed only for patients with mesial lesions or semiology suggestive of MTLE to asses for memory asymmetry, and (5) neuropsychological evaluation for patients with mesial lesions. Operative strategy was based on clinical semiology, electrophysiology, and anatomic location of the CCM. Anterior and lateral neocortical lesions were routinely treated with complete lesionectomy (including hemosiderin-stained brain), if not contraindicated by functional mapping, with the assistance of intra-operative electrocorticography (ECoG). Awake craniotomy with cortical mapping was only performed for temporal lobe lesions in eloquent (speech) cortex. These lesions were removed using the shortest route to the lesion (for deep lesions an intersulcal dissection was preferred). For mesial (archicortex) or basal (neocortical) temporal lobe location, the aim was complete epileptogenic zone resection, if not contraindicated by the pre-operative work-up. Because the latter group usually presented with a clinical semiology and electrophysiology highly suggestive of mesial temporal lobe epilepsy (MTLE), epileptogenic zone resection was defined as total resection of the lesion and
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selective amygdalo-hippocampectomy [12, 40]. Developmental venous anomalies (DVAs) associated with CCM were not resected. Patients were placed on peri-operative IV antibiotics and steroids. Frameless neuronavigation was routinely used for surgery. All resected tissue was sent for histopathological confirmation of diagnosis. MRI was performed in all patients 3 months postoperatively to document the extent of resection and thereafter as necessary. Resection of the CCM and hemosiderin-stained brain was defined as Bcomplete lesionectomy^.
Outcomes Clinical outcomes were based on the Engel modified classification as follows [13]: class I, seizure free or residual aura (EC-I); class II, rare disabling seizures (
