Tailored multilobar disconnective epilepsy surgery in the posterior quadrant

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OBJECTIVE

Surgical treatment of drug-resistant epilepsy originating from the posterior quadrant (PQ) of the brain often requires large multilobar resections, and disconnective techniques have been advocated to limit the risks associated with extensive tissue removal. Few previous studies have described a tailored temporoparietooccipital (TPO) disconnective approach; only small series with short postoperative follow-ups have been reported. The aim of the present study was to present a tailored approach to multilobar PQ disconnections (MPQDs) for epilepsy and to provide details about selection of patients, presurgical investigations, surgical technique, treatment safety profile, and seizure and cognitive outcome in a large, single-center series of patients with a long-term follow-up.

METHODS

In this retrospective longitudinal study, the authors searched their prospectively collected database for patients who underwent MPQD for drug-resistant epilepsy in the period of 2005–2017. Tailored MPQDs were a posteriori grouped as follows: type I (classic full TPO disconnection), type II (partial TPO disconnection), type III (full temporooccipital [TO] disconnection), and type IV (partial TO disconnection), according to the disconnection plane in the occipitoparietal area. A bivariate statistical analysis was carried out to identify possible predictors of seizure outcome (Engel class I vs classes II–IV) among several presurgical, surgical, and postsurgical variables. Preoperative and postoperative cognitive profiles were also collected and evaluated.

RESULTS

Forty-two consecutive patients (29 males, 24 children) met the inclusion criteria. According to the presurgical evaluation (including stereo-electroencephalography in 13 cases), 12 (28.6%), 24 (57.1%), 2 (4.8%), and 4 (9.5%) patients received a type I, II, III, or IV MPQD, respectively. After a mean follow-up of 80.6 months, 76.2% patients were in Engel class I at last contact; at 6 months and 2 and 5 years postoperatively, Engel class I was recorded in 80.9%, 74.5%, and 73.5% of cases, respectively. Factors significantly associated with seizure freedom were the occipital pattern of seizure semiology and the absence of bilateral interictal epileptiform abnormalities at the EEG (p = 0.02). Severe complications occurred in 4.8% of the patients. The available neuropsychological data revealed postsurgical improvement in verbal domains, whereas nonunivocal outcomes were recorded in the other functions.

CONCLUSIONS

The presented data indicate that the use of careful anatomo-electro-clinical criteria in the presurgical evaluation allows for customizing the extent of surgical disconnections in PQ epilepsies, with excellent results on seizures and an acceptable safety profile.

ABBREVIATIONS AED = antiepileptic drug; DRE = drug-resistant epilepsy; EA = epileptiform abnormality; EEG = electroencephalography; EZ = epileptogenic zone; FCD = focal cortical dysplasia; MPQD = multilobar PQ disconnection; PQ = posterior quadrant; SEEG = stereo-EEG; TO = temporooccipital; TPO = temporoparietooccipital; VEEG = video-EEG.

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Article Information

Correspondence Michele Rizzi: “C. Munari” Center for Epilepsy Surgery, ASST Grande Ospedale Metropolitano Niguarda, Milan, Italy. michele.rizzi@ospedaleniguarda.it.

INCLUDE WHEN CITING Published online April 26, 2019; DOI: 10.3171/2019.1.JNS183103.

Disclosures Dr. Cardinale was a consultant (paid expert testimony) to Renishaw Mayfield, the manufacturer of Neuromate robotic system, until February 2019. Dr. Rizzi is a consultant to WISE Srl, a start-up manufacturing implantable leads for neuromodulation and neuromonitoring.

© AANS, except where prohibited by US copyright law.

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Figures

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    Surgical features of the tailored MPQDs on 3D brain models. The orange lines show the disconnection line on the medial surface of the hemisphere. The red and yellow lines indicate the disconnection on the nondominant and dominant lateral surfaces of the hemisphere, respectively. A and B: Type I MPQD. C and D: Type II MPQD. E and F: Type III MPQD. G and H: Type IV MPQD. Figure is available in color online only.

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    Type I MPQD. This 10-year-old girl had a complicated delivery due to a nuchal cord, with no immediate sequelae. At the age of 6 months, left hemiparesis became evident. A: Preoperative MR images showing diffuse right hemisphere atrophic changes, more prominent in the posterior regions. At 15 months, the patient presented with febrile seizures with clonic movements of the left upper limb, which subsequently disappeared. At 3 years, she started to have daily seizures with abdominal aura, fear, and vegetative symptoms, with limited benefit from carbamazepine and levetiracetam. B: EEG showed right PQ and central EAs, and, during the long-term VEEG monitoring, 2 episodes were recorded, with a right temporal onset and rapid propagation to the ipsilateral occipital and parietal regions. C: Due to partial localizing discordance of this noninvasive phase, SEEG exploration was performed, with coverage of the right PQ and the central region. The electrode arrangement is shown over a pial surface reconstruction (left). SEEG recording of a habitual seizure showed ictal onset in the mesial temporal structures (right), and propagation to the occipital and parietal areas and without involvement of the central region. Accordingly, a complete TPO disconnection was performed. The patient exhibited left upper-limb motor seizures immediately postoperatively, which disappeared completely within 6 months after surgery. She has been seizure free since then, and after 40 months of follow-up, drug tapering has been started. The histopathological diagnosis showed gliosis. D: Postoperative MR images obtained at 6 months. Figure is available in color online only.

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    Type II MPQD. The patient was a right-handed 18-year-old male at the time of referral. Developmental milestones were regularly reached, and he attended secondary school. The patient had been treated for Imerslund-Gräsbeck syndrome since the age of 18 months, when he presented with anemia and convulsions. At the age of 14 years, episodes of loss of contact and gestural automatisms started. Déjà vu auras could also occur. Carbamazepine and valproate were ineffective. EEG revealed EAs at the level of the right temporal region. A: MRI of the brain, showing right hemispheric hypoplasia, more relevant at the level of the temporal lobe, with blurring of the gray matter–white matter interface, and ulegyria of the occipital lobe and of the inferior aspect of the precuneus. Left incomplete hemianopia was also present. B: Long-term VEEG monitoring revealed a right temporal origin of the seizures. C: A right TO disconnection including the posterior precuneus was performed as seen on the postoperative MR images. The patient is seizure free 60 months after surgery, with his AEDs having been withdrawn. Neuropsychological evaluation revealed improvement of both visuospatial and verbal items. Histology showed only unspecific gliosis. Figure is available in color online only.

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    Intraoperative images of a type II MPQD. A: The green line indicates the superficial disconnection plan of a type II MPQD in the dominant hemisphere. B and C: The tentorial free margin (B, arrow) and the falco-tentorial edge (C, arrow) are highlighted. D: Intraventricular view of the splenium of the corpus callosum. Figure is available in color online only.

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    Type III MPQD. The patient was a left-handed 27-year-old male at the time of the referral. His development in utero was complicated by placental insufficiency that required a C-section during the 8th month. The patient completed secondary school with the aid of a special needs teacher, and he was unemployed. He presented with a right inferior limb paresis and right hemianopia. Neuropsychological examination revealed visuospatial memory disturbances. Seizure onset occurred at the age of 8 years with daily episodes starting with fear, followed by a shout, without language disturbances. Carbamazepine was effective for 2 years. The patient’s seizures recurred, and they were characterized by whistling and bitter mouth, followed by loss of contact and oral automatisms. Vigabatrin and valproate were only transiently effective. A: MR images of the brain showed a left hemisphere perinatal injury, more prominent at the level of the temporal and occipital lobes. B: The interictal EAs were recorded by the left temporal and occipital derivations. Long-term VEEG monitoring showed a seizure onset at the level of the left temporal region. C: The patient underwent a complete left TO disconnection as seen on the postoperative MR images. The patient is now seizure free, and drug tapering is ongoing. Histopathological analysis showed the scar of the perinatal injury.

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    Type IV MPQD. This 42-year-old woman was born after a normal pregnancy and delivery. Developmental milestones were regularly reached. The patient was unemployed. Her seizures started at the age of 14 years with a brief loss of contact, without aura. Later, bilateral hand automatisms, with tonic generalization and occasional falls, added to ictal semiology, and speech impairment was present postictally. Carbamazepine, levetiracetam, and zonisamide were ineffective. Neuropsychological examination revealed diffuse language and visuospatial disturbances. A: MRI findings were negative. B: Seizures recorded on long-term VEEG showed a right TO onset, while the interictal EAs were localized bilaterally in the temporal regions. Due to the complexity in EZ localization, a right perisylvian-temporal-occipital SEEG exploration was performed, and a diffuse EZ was defined at the level of the right temporal and basal occipital region. C: A disconnection surgery at this level was subsequently performed. Since both functional MR and SEEG functional mapping failed to disclose a clear dominance for language, and considering the postictal speech impairment presented by the patient, the disconnection spared the posterior portion of the superior temporal gyrus. The patient is seizure free 36 months after surgery, and progressive drug tapering is ongoing. Histopathological analysis revealed only unspecific gliosis. Figure is available in color online only.

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