Preoperative Evaluation

Invasive Investigations

When noninvasive investigations alone fail to correctly define the EZ, and/or when the EZ (or the anatomic lesion) is suspected to involve highly functional regions, invasive recording with intracranial electrodes is indicated. In many centers, subdural electrodes (arranged in strips or grids and placed through bur holes or craniotomy) are employed. In our center, stereotactic placement of intracerebral electrodes (stereoelectroencephalography, or SEEG) is preferred as the invasive EEG monitoring technique of choice, and it is required in approximately 30% of cases operated on. For each patient, the strategy of intracerebral electrode placement is tailored according to previously acquired clinical, electrical, and anatomic data. Examples of customized SEEG explorations are shown in Figs. 111-1 and 111-2. The technical details of this methodology have been reported elsewhere.¹²

FIGURE 111-1 Example of an SEEG exploration. Coverage with intracerebral electrodes includes the right frontal and temporal lobes, as well as the rolandic and insular cortex. A brain cortical surface reconstruction of the lateral (A) and mesial (B) aspects of the right hemisphere was obtained from the 3D T1-weighted MRI structural images. (FreeSurfer software, http://surfer.nmr.mgh.harvard.edu.) Black spots, labeled by lowercase letters, indicate the surface impact points of each intracerebral electrode. C to H, Blended images of 3D T1-weighted MRI and coregistered postimplantation volumetric computed tomography, where single contacts of intracerebral electrodes are easily recognizable: electrodes b and l (C), electrode i (D), electrode t (E), electrode s (F), and a sagittal slice showing several contacts of different electrodes (G). H, The rectangular insert is magnified, where intracortical insular contacts of electrodes t, x, and r are shown.

FIGURE 111-2 Example of an SEEG exploration. Coverage with intracerebral electrodes includes the right temporal, occipital, and parietal lobes. A brain cortical surface reconstruction of the lateral (A) and mesial (B) aspects of the right hemisphere was obtained from the 3D T1-weighted MRI structural images. (FreeSurfer software, http://surfer.nmr.mgh.harvard.edu.) Black spots, labeled by lowercase letters, indicate the surface impact points of each intracerebral electrode. C to H, Blended images of 3D T1-weighted MRI and coregistered postimplantation volumetric computed tomography, where single contacts of intracerebral electrodes are easily recognizable: electrode d and intrahippocampal contacts of electrode c (C), electrode p (D), electrode y (E), electrode o (F), and MRI slices coplanar with electrode k (G and H).

This method can reveal that in some cases the ictal discharges do not respect the anatomic limits of a single cerebral lobe, therefore allowing the diagnosis of multilobar epilepsy. This has been the case in 42% of the patients operated on after SEEG recording in our center. However, only 10% of cases evaluated by noninvasive investigations received a multilobar resection.

Surgical Decision-Making

The larger the epileptogenic cortex that needs to be removed, the harder the compromise that must be reached between the desire to cure each patient and the fear of creating new neurologic or neuropsychologic damage. The well-known concept of critical mass¹³ does apply to epilepsy surgery, and the decision on the extent of the EZ in multilobar partial epilepsies raises several particular diagnostic and therapeutic problems. In surgical planning, several questions can be considered that have no standard solutions and could have different answers depending on the characteristic of each patient and the attitude, feeling, and experience of the epilepsy surgery team. These issues concern the criteria for identifying the actual epileptogenic cortex. For instance, the following are challenging and not yet fully addressed questions: Should only the cortical areas that are affected by the ictal discharges at the onset of the seizures be removed? How long is the ictal onset? If the initial clinical symptom occurs several seconds after the onset of the electrical discharge, is removal of the symptomatogenic cortex mandatory,¹⁴ or will removal of only the initially affected cortical region be sufficient? What is the risk of removing the entire epileptogenic cortex? What kind of neurologic or neuropsychologic deficits can be induced? Are all of them predictable?

Anesthetic Considerations

Resective surgery for treatment of focal epilepsy does not require anesthetic approaches substantially differing from those commonly employed in other intracranial procedures. In our center, resections are performed under general anesthesia, with the patient positioned according to the site of surgery. Prophylactic antibiotics (1-2 g of cephamezine given intravenously) are given at anesthesia induction. Candidates for surgical treatment of severe partial epilepsy are commonly in optimal physical condition, and their interictal intracranial pressure (ICP) is not elevated.¹⁵ Careful anesthesiologic management (mostly hyperventilation, diuretics, or barbiturates) can be helpful when the volume of the exposed brain suddenly increases. This transitory increase in ICP may suggest the occurrence of an epileptic seizure,¹⁶ the clinical symptoms of which are masked by anesthesia. Except for this infrequent, transitory, and easily controlled incident, no other major intraoperative complications are usually expected in epileptic patients.

Surgical Technique

As compared to classic approaches for unilobar epilepsies, those adopted for multilobar excisions are tailored according to the site and extension of the region involved in the procedure. The supine position is usually preferred even when surgery is performed on the posterior portions of the hemisphere, with the operating table being tilted and the head rotated to obtain comfortable access to the surgical field. The prone position is used mainly when surgery involves the mesial aspects of the parietal or occipital lobes. Both skin incision and bone flap are designed to fully expose the region to be removed, as well as the surrounding cortical areas. In some instances, when a two-step procedure is likely, the surgeon must take into account the possible subsequent step when fashioning skin and bone flaps. In patients who have been previously evaluated by SEEG, the tracks of electrodes can be easily identified on the bone surface, and they are used as landmarks to plan the extent of the bone flap. While opening the dura mater, if an SEEG has been previously performed, care should be taken to separate the adhesions between the inner aspect of the dura and the cortical surface at the electrode entry points. Once the dura is opened, it is useful to match the vascular surgical anatomy with the stereoscopic angiograms obtained preoperatively, which provide an exquisite three-dimensional (3D) view of the sulcal and gyral pattern of the region.¹⁷ Careful inspection of the exposed cortex enables the surgeon to identify the entry points of intracerebral electrodes, which are used to draw the borders of resection (Fig. 111-3).

FIGURE 111-3 A, The tracks left by the multilead electrodes of a previous SEEG at the cortical entry point are still clearly visible at surgery several months after their removal. B, Before starting cortical excision, lettered paper tags are used to mark every electrode’s entry point to correctly draw the planned resection on the cortical surface.

Neuronavigation is helpful in optimizing accuracy and safety of the procedure, and it is routinely employed in our center. Once a volumetric T1-weighted MRI sequence is obtained preoperatively and entered into the neuronavigational module, different anatomic and functional elements can be incorporated in the plan of navigation, including the volume of the lesion as it appears in other MRI sequences, the electrodes trajectories of a previous SEEG, and the volume of cortical areas activated at functional MRI, as well as those of major subcortical bundles detected at diffusion tensor imaging (DTI) fiber tracking.

With the aid of the surgical microscope, resection is accomplished according to a few simple rules:

Like hemispherectomy, which has progressively evolved into hemispherotomy (described later) to minimize the risks of hydrocephalus, hemosiderosis, and intraoperative blood losses, extended multilobar resections may be replaced with disconnective techniques. In our experience, disconnections have been particularly helpful in procedures involving the posterior quadrant of the hemisphere, when the EZ extends to the temporal, occipital, and parietal lobes. In these cases, we can employ a pure disconnective technique (Fig. 111-4) or otherwise combine resection with disconnection.¹⁸ Unlike other authors, when combining the two techniques, we prefer to remove the occipital and parietal lobes and to disconnect the temporal lobe, which may exert a sort of “push-up” effect if left in place, thus limiting residual brain dislocation into the resulting surgical cavity. Like other disconnective techniques, posterior hemispheric disconnections are not indicated if evolutive pathologies are suspected. A drawback of disconnective approaches is the limited availability of resected tissue, which may prevent a reliable etiologic diagnosis and restrict the access of basic scientists to pathologic specimens.

FIGURE 111-4 Postoperative sagittal T1-weighted MRI, showing the plane of disconnection isolating a large focal cortical dysplasia of the posterior quadrant of the right hemisphere, including the whole temporal lobe, from both the ipsilateral central and frontal lobes and the contralateral hemisphere.

At dural closure, intravenous phenytoin (10-15 mg per kilogram of body weight) is administered over a 20-minute period. At the end of surgery, the patient is moved to the intensive care unit (ICU) and anesthesia is progressively tapered. Habitual oral antiepileptic medicaments are given as soon as the patient can safely swallow.

The anatomofunctional basis of morbidity in multilobar resections does not differ substantially from that of unilobar resections, and it strictly depends on the site of surgery. Morbidity may include transient motor impairment, akinesia and mutism after removal of the supplementary motor area,¹⁹ transient speech disturbances following resections involving the neocortex of the dominant temporal lobe, and contralateral superior quadrantoanopia in anterior temporal lobectomies. The risk of larger contralateral visual field defects is higher following resections in the posterior portion of the hemisphere. When removal is contiguous to the rolandic region, the risk of motor–sensory impairment is usually increased, and functional mapping by either intracerebral electrical stimulations at SEEG or functional MRI or intraoperative cortical and subcortical electrophysiologic evaluation is helpful to minimize the chances of unwanted postoperative deficits.

Results on seizures of multilobar surgery are far less gratifying if compared to other unilobar resections, either in our or in other centers^18,20–26 (Tables 111-1 to 111-3). Slightly better results are observed in multilobar resections, including the temporal lobe. However, it must be stressed that, despite a complex epileptologic situation that could hardly be improved by further drug regimens, a substantial number of patients can be cured or improved (Engel’s²⁷ classes I-III, approximately 80% in our series) by surgical treatment.

Table 111-1 Results on Seizures in Unilobar Resections^∗

Ia+c, completely seizure-free patients.

∗ Results are according to Engel’s (1987) classification.²⁷

Table 111-2 Results on Seizures in Multilobar Resections^∗

Table 111-3 Literature Reporting Seizure Outcome in Multilobar Resections (Publication Period 1998-2008)

Illustrative Case

This 15-year-old girl received repeated surgery (at 2.4 and 13 months of age) for a complex cardiac malformation, following several hypoxic–anoxic episodes that had occurred since birth.

At 4 years of age, she started presenting with seizures, which became drug resistant despite different pharmacologic attempts. When she was referred to our center at 15 years of age, her seizures were clinically characterized by nonlateralized blurred vision, head and eye deviation toward the left side, loss of contact, and inconstant late oroalimentary automatisms. No peri-ictal speech disturbances were reported. Abrupt ictal falls with no prodromic symptoms were also described. Seizures frequency was three to four episodes daily.

Neurologic examination was normal, with a revised Wechsler Intelligence Scale for Children score of 73 (verbal score 79, performance score 71).

Scalp video-EEG disclosed slower background activity on the right hemisphere and interictal slow waves and spike and waves on the right temporo-occipital regions. Ictal EEG showed an early low-voltage fast activity on the right posterior leads, with late spread to the homologous contralateral regions. Brain MRI documented two separate lesions of possible ischemic nature in the right hemisphere, involving the basal occipital and the rolandic regions (Fig. 111-5A). SEEG investigation was performed to evaluate the relationships between the occipital anatomic lesion and the EZ, which could be suspected to involve also the parietal and temporal lobes on the basis of the electroclinical findings (Fig. 111-5B). No electroclinical data indicated the need to sample the rolandic lesion by intracerebral electrodes. Electroclinical correlations obtained during SEEG recordings localized the EZ in the inferior half of the occipital lobe (electrodes l and v) and in the posterior mesiobasal aspect of the temporal lobe (electrodes f and e) (Fig. 111-5C). Surgical resection of the EZ was performed (Fig. 111-5D), and histologic examination documented gliotic changes in the excised tissue corresponding to the MRI lesion. The patient was left with an expected and anticipated complete left-sided hemianopia, and she is seizure free since surgery after 3 years of follow-up.

FIGURE 111-5 Illustrative case. A, Brain MRI (coronal and sagittal sections, T2-weighted FLAIR sequences) showing two separate mainly hyperintense lesions in the right rolandic region (open arrows) and in the basal aspect of the ipsilateral occipital lobe (closed arrows). Electroclinical noninvasive findings suggested a right occipitoparietotemporal localization of the EZ. B, Stereotactic scheme of the SEEG exploration, with lateral and frontal views of the skull. Dashed areas indicate the site of the lesions imported from the MRI coregistered with stereotactic angiography. The 16 stereotactically implanted intracerebral electrodes are indicated by letters. Explored structures were, from lateral to mesial, d, inferior temporal, fusiform, and parahippocampal gyri; e, inferior temporal and fusiform gyri; c, middle temporal gyrus, posterior hippocampus, and parahippocampal gyrus; f, inferior temporal and parahippocampal gyri; w, posterior part of the superior temporal gyrus; l, inferior occipital gyrus, occipital lesion, and lingual gyrus; v, middle occipital gyrus, lesion, and calcarine cortex; z, angular and posterior cingulated gyri; s, supramarginal and postcentral cingulated gyri; p, inferior parietal lobule and precuneus; n, supramarginal gyrus and precuneus; x, superior parietal lobule, precuneus, and posterior cingulate gyrus. C, Ictal SEEG. The recorded spontaneous seizure showed a sequence of polyspikes well localized in the lingual gyrus and inferior calcarine cortex, followed by a low-voltage fast activity (arrow) on the same leads, and, with a delay of about 500 msec, the involvement of the fusiform and parahippocampal gyri. The ictal discharge spreading to other structures appeared less prominent. The clinical symptomatology was characterized by (1) an oculocephalic deviation toward the left, grimacing; (2) a further rotation of the head to the left; (3) the patient calling her mother and (4) raising a dystonic left arm; and finally (5) a rotation of the trunk to the left. No speech disturbance was observed in the postictal period. D, Postoperative brain MRI (sagittal T1-weighted inversion recovery sequences), showing resection of the mesiobasal and dorsolateral portions of the right occipital lobe, as well as of the posterior mesiobasal cortex of the temporal lobe. Coll, collateral; Cx, cortex; iOg, inferior occipital gyrus; mOg, middle occipital gyrus; O, occipital; Parahipp, parahippocampal; iPl, inferior parietal lobule; sPl, superior parietal lobule; Supramarg, supramarginal; iTg: inferior temporal gyrus; mTg, middle temporal gyrus; sTg, superior temporal gyrus.