Chapter 109 Temporal Lobe Operations in Intractable Epilepsy
Epilepsy afflicts 0.5% to 1% of the world’s population and incurs an enormous burden of disease-related disability.1 Approximately one third of patients with epilepsy either fail to achieve adequate seizure control with antiepileptic drugs or are unable to tolerate the side effects induced at the doses necessary to do so.2–4 A substantial literature indicates that poorly controlled epilepsy impairs cognition, reduces employment, diminishes psychosocial function and overall quality of life, and increases both risk of sudden death and overall mortality relative to age-matched controls.5–10
Mesial temporal lobe epilepsy (MTLE) is the most common and well-defined focal epilepsy syndrome, and it is also the most likely to be pharmacoresistant.11,12 For a subset of patients with intractable MTLE, anterior temporal lobectomy (ATL) offers the possibility of a seizure-free life with reduced reliance on antiepileptic drugs. ATL has evolved over the past century into a safe and effective procedure that has been validated with class I evidence.13 It is now in widespread use at epilepsy centers throughout the United States and across the developed world, and contemporary surgical series consistently report seizure-free rates of about 70% in MTLE patients.14
The history of surgery for MTLE spans more than a century. Writing in 1898, Jackson and Colman ascribed seizures associated with “tasting movements” and a “dreamy state” to a lesion in the mesial temporal lobe.15 The earliest epilepsy resections excised cortical regions implicated in patients’ seizure semiologies with varying degrees of success, but neocortical removal alone in cases of temporal lobe epilepsy yielded only modest seizure control. In the early 1950s, Penfield et al. used refinements in electroencephalograms (EEGs) and electrocorticography (ECoG) to demonstrate that the mesial limbic structures were central to the pathophysiology of “psychomotor epilepsy.”16 As surgeons identified an increasing number of patients with seizures of mesial temporal origin, interest developed in designing standardized surgical procedures that incorporated resection of the amygdala and hippocampus. Falconer and colleagues17,18 and Morris19 described early versions of procedures that would form the basis for the modern ATL. Niemeyer soon proposed a mesial resection technique that spared the lateral cortex20; this was later adapted by Wieser, Yasargil, and colleagues21–23 and by Olivier,27 and it was the forerunner of the contemporary selective amygdalohippocampectomy (SAH).
The selection of appropriate surgical candidates is paramount to the success of ATL and is discussed in detail in the previous chapter. Briefly, patient selection hinges on the concordance of data from several modalities, including neuroimaging, electrophysiologic recordings, and neuropsychological evaluation that (1) identifies the patient as one with the “surgically remediable syndrome” of MTLE,24 (2) localizes a seizure focus suitable for extirpation, and (3) determines that the benefit gleaned from resecting the implicated epileptogenic zone would outweigh any language or memory deficit likely to be experienced.
The standard en bloc ATL, in which the lateral neocortex and mesial hippocampal structures are removed in a single specimen, was developed in the early 1950s17,18 and employed over the ensuing few decades.25 More recently, two-part resection, in which the lateral and mesial portions are resected separately, has been favored by most surgeons.26–28 What follows is one method of performing the two-part ATL, along with references to other variations.
The procedure is usually performed under general anesthesia, unless ECoG or language mapping are planned. In the former case, nitrous oxide should be discontinued during ECoG but the patient should remain paralyzed with depolarizing muscle relaxants; in the latter, the procedure may be performed while the patient is awake.29,30 When ECoG is planned, perioperative use of anxiolytic medications that might suppress EEG activity (diazepam, midazolam, etc.) should be avoided. The patient is positioned supine on the operating room table with the head turned 90 degrees laterally and is stabilized with three-point fixation. A shoulder roll can be employed to assist with lateral head rotation if necessary. The vertex is lowered approximately 10 degrees below horizontal to minimize frontal lobe retraction later in the procedure. The operative area is shaved with clippers, and the skin is prepared with degreasing solution. We employ a linear incision, starting at the root of the zygoma, approximate 1.5 cm anterior to the tragus (Fig. 109-1). The incision is carried superiorly to the superior temporal line. A gentle anterior curve at the superior aspect of the incision may be employed to increase exposure if necessary. Others use a question mark–shaped incision starting at the same location, curving posteriorly over the auricle, and then curving superiorly and anteriorly toward the hairline.26,29,31,32 The incision is marked, and nonsterile clear plastic adhesive drapes are applied to square off the operative field. The region is then sterilely prepped and draped.
FIGURE 109-1 Incision and craniotomy. We employ a linear incision from the root of the zygoma, approximately 1.5 cm anterior to the tragus, to the superior temporal line. Following incising of the skin and splitting of the temporalis muscle, bur holes are placed just above the zygomatic process and at the superior temporal line. The craniotomy is performed, with attention paid to squaring off the posterior inferior corner to facilitate exposure of the posterior hippocampus.
The skin is anesthetized with 10 to 30 ml of a 50:50 combination of Marcaine 0.5% with epinephrine 1:100,000 and lidocaine 2% with epinephrine 1:100,000. The skin incision is carried out from superior to inferior, with attention paid to preserving the superficial temporal artery if possible. Raney clips are applied for hemostasis. The fascia of the temporalis muscle is incised sharply, and the muscle is then cut parallel to the skin incision with monopolar cautery. The temporalis muscle is retracted with angled cerebellar retractors, exposing the squamous temporal bone and parietal bone.
Two bur holes are placed at either end of the incision, above the zygomatic process, and at the superior temporal line. Using a footplated bit, the craniotomy is carried out, with particular attention paid to squaring off the posteroinferior corner by cutting directly posteriorly above the ear before turning superiorly (Fig. 109-1). Compared to a gentle curve at that corner, a right angle turn facilitates posterior exposure of the hippocampus later in the procedure. The greater sphenoid wing is further trimmed with rongeurs to increase exposure of the temporal pole, and the inferior margin of the craniotomy is similarly trimmed to access the floor of the middle cranial fossa, taking care not to enter the mastoid air cells. Bleeding from the middle meningeal artery is controlled with bipolar cautery.
Prior to durotomy, we square off the exposure with four fresh towels. The dura is sharply incised in a C-shaped fashion based on the sphenoid wing and reflected over the retracted temporalis muscle. This technique exposes the sylvian fissure, inferior frontal gyrus (IFG), superior temporal gyrus (STG), and middle temporal gyrus (MTG) (Fig. 109-2). The cortical surface is inspected for any abnormalities, as well as for the presence of large draining veins such as the Labbé vein or the middle cerebral vein, which must be preserved. The two-step resection then commences, starting with the neocortical block, followed by the mesial block.
FIGURE 109-2 Cortical exposure. The surgeon’s view of the cortical exposure for a left-sided ATL is depicted, performed through the craniotomy shown in Fig. 109-1. A C-shaped durotomy based on the sphenoid wing exposes the IFG, sylvian fissure, STG, and MTG. The planned corticectomy (dashed line) begins in the MTG and extends anteriorly toward the temporal tip and inferiorly toward the floor of the middle fossa. Superior is the bottom aspect of the figure; anterior is the right aspect of the figure.
The first stage of the resection is removal of the neocortical block (Fig. 109-3, stippled region). The temporal pole is visualized at the anteriormost recess of the greater wing of the sphenoid bone by gently lifting the dura and peering down the longitudinal axis of the temporal lobe. The distance from the temporal pole is measured along the length of the MTG. We generally resect about 4 cm of neocortex. In nondominant cases, further posterior extension to 5 or 6 cm may possibly be achievable without significant impact on memory, language, or cognitive function. More generous lateral resections are typically reserved for situations in which there is suspicion of epileptogenicity in the neocortex. In these cases, ECoG and language mapping may be useful to tailor the resection to match the pathophysiology and to avoid postoperative language deficit.29,30,33,34 In most cases of standard MTLE, however, ECoG and large lateral resections are not necessary.28,35 A more sparing approach to the lateral resection was developed by Spencer and colleagues, in which only 3 to 3.5 cm of the temporal tip is removed, leaving the STG intact, regardless of laterality.28,31
FIGURE 109-3 Schematic of resection. The two-part ATL is shown from basal (A), lateral (B), and coronal (C) views. The lateral resection (orange stippled region) includes the MTG and ITG. The posterior extent is generally about 4 cm but may be modified based on anatomic considerations, ECoG, or functional mapping. The lateral specimen includes the MTG, ITG, and part of the fusiform gyrus (FG). The incision plane approaches but does not enter the temporal horn of the lateral ventricle, which lies deep to the MTG. The anteriormost 1.5 to 2 cm of the STG is emptied with subpial dissection. The mesial resection (hatched region) includes the remainder of the FG, PHG, hippocampal formation (HC), and amygdala. AChA, anterior choroidal artery; CN II, optic nerve; CN III, oculomotor nerve; ICA, internal cerebral artery; MCA, middle cerebral artery; PCoA, posterior communicating artery.
The MTG pia is cauterized with bipolar forceps at the specified distance from the temporal pole and is sharply cut. This incision is carried directly inferiorly to the floor of the middle fossa (Figs. 109-2 and 109-3B, dashed line), traversing the MTG and inferior temporal gyrus (ITG), and around the basal surface to include the fusiform (lateral occipitotemporal) gyrus, approaching the collateral sulcus (Fig. 109-3). It is deepened into the white matter of the temporal stem approximately 2 to 3 cm toward the temporal horn of the lateral ventricle, using either bipolar coagulation and suction29,32 or ultrasonic aspiration.26,28,36 Some authors plan a coronal trajectory to enter the ventricle at this point,26,29 but we and others31 prefer to approach but not yet enter the ventricle (Fig. 109-3C). The incision is then carried anteriorly, parallel to the superior border of the MTG, to the temporal pole. The STG is initially left intact to protect the sylvian fissure vessels. The incision is carefully deepened parallel to the plane of the sylvian fissure, and the white matter is aspirated progressively inferiorly in an oblique coronal plane until the inferior incision is encountered. The incision plane is continued anteromedially until the temporal pole, freeing the neocortical specimen. The neocortex and underlying white matter can be sent as the first specimen for analysis. The remaining cuff of the MTG and anteriormost 1.5 to 2 cm of the STG are then aspirated with subpial dissection, maintaining the integrity of the arachnoid plane protecting the sylvian vessels. The neocortical resection is thus completed, leaving only the parahippocampal gyrus (PHG), hippocampus, and amygdala.
Attention is then turned to the mesial temporal structures for the second stage of the procedure (Fig. 109-3, hatched region). Prior to commencing, the microscope is brought into position, and self-retaining retractors are placed. We employ two retractors: one on the STG to gently retract the frontal lobe and the other on the cut coronal surface of the temporal lobe at the level of the MTG. Attention should be paid to minimizing frontal lobe retraction, as the structures immediately deep to the frontal retractor include the external capsule and lentiform nucleus of the basal ganglia.
The mesial contents may be resected as a single piece26 or, as described here, in two separate sections,31 one containing the PHG and hippocampus and the other containing the amygdala. The first step of the mesial resection is identification of the ventricle. The temporal horn of the lateral ventricle runs parallel and deep to the MTG (Fig. 109-3A and C). It can usually be encountered approximately 3 to 4 cm posterior to the temporal pole and about 3.5 cm deep to the surface of the MTG. Its location can be confirmed by studying the preoperative films. At this point in the anterior–posterior dimension, the hippocampal formation comprises the inferomedial wall of the ventricle (Figs. 109-3C and 109-4). The choroidal fissure, defined as the space between the two pial leaflets that form the choroid plexus, comprises the superomedial boundary of the ventricle. Further anteriorly, at the level of the uncus, the amygdala forms the superomesial cap of the ventricle.
FIGURE 109-4 Mesial resection. The surgeon’s view of the remaining mesial structures is depicted following completion of the lateral resection and opening of the temporal horn of the lateral ventricle in a left ATL. The choroid plexus marks the superior aspect of the ventricle, the amygdala marks the anterior extent, and the smooth ventricular surface of the hippocampal formation (HC) is visualized inferomedially, continuing into the cut edge of the PHG. Immediately anterior to the HC, the ventricle curves sharply medially, forming a cleft separating the HC posteriorly from the amygdala anteriorly (see also Fig. 109-5A). Superior is the bottom aspect of the figure; anterior is the right aspect of the figure.
Entry into the ventricle is confirmed by visualizing the smooth ependymal surface, a gush of cerebrospinal fluid, or the emergence of the choroid plexus. The anterior–posterior extent of the ventricle is opened, revealing the smooth shiny ventricular surface of the hippocampus inferomedially, the choroid plexus superiorly, and the amygdala anteriorly (Fig. 109-4). The boundary between the hippocampal formation posteriorly and the amygdala anteriorly is usually demarcated by a cleft of the ventricle near its anterior tip (Figs. 109-4 and 109-5A). This cleft is deepened until the mesial temporal lobe arachnoid membrane is encountered, thereby cleaving the hippocampus and PHG posteriorly from the amygdala anteriorly. This arachnoid membrane is the medial extent of the resection and should never be violated, as the contents of the ambient cistern, including the circle of Willis vessels and cranial nerves, lie beyond it (Fig. 109-3A).
FIGURE 109-5 Preoperative and postoperative MRI. A, Preoperative T2-weighted axial MRI is shown through the level of the midbrain, depicting the cleft (arrowheads) of the temporal horn of the lateral ventricle separating the amygdala anteriorly from the hippocampal formation posteriorly (see also Fig. 109-4). B and C, Postoperative T2-weighted coronal MRI is shown. Anteriorly, at the level of the amygdala and optic chiasm (B), the resection includes all neocortical structures except the STG (asterisk). Posteriorly, at the level of the red nuclei (C), the lateral neocortical structures are spared.
A vertical incision in the hippocampus is performed at its posterior aspect, approximately 2 cm from its head. This incision is carried lateral to medial through the entire width of the hippocampus and PHG. By gently rolling the hippocampus laterally, feeding arteries from the anterior choroidal artery and, more commonly, from the second (crural/ambient) segment of the posterior cerebral artery (PCA) can be identified. These arteries enter through the hippocampal fissure, a small fissure between the dentate gyrus and the subiculum, and typically number three to four. They should be coagulated and sharply divided close to the substance of the hippocampus, taking care not to damage the main arterial trunk.
At this point, the only remaining attachments to the hippocampus and PHG are medial. The lateral and inferior attachments to the hippocampus and PHG were severed during resection of the neocortical block. The vertical hippocampal incision separated them in an anterior–posterior direction. Medially, the fibers of the fimbria leaving the hippocampus can be identified as a thin stream of white matter just inferior to the choroid plexus. These are aspirated along the length of the hippocampus, thus detaching it completely. Superomedially, the choroid plexus may be gently retracted but not coagulated, bearing in mind that the optic tracts and tail of the caudate lie just medial and superior to the choroid plexus. The hippocampus and PHG are then gently rolled off the medial arachnoid membrane and may be sent as an en bloc specimen.
The microscope is then tilted to peer down the long axis of the hippocampus, and the temporal retractor is deepened and lifted slightly. These maneuvers allow improved visibility of the remaining several millimeters of posterior hippocampus. This residual is aspirated with the aid of bipolar cautery. The posterior limit of the hippocampectomy is the point at which the hippocampus begins to curve medially and superiorly, approximately the anterior–posterior level of the quadrigeminal plate.
The second part of the mesial resection is the amygdalectomy. At this point, the amygdala is conspicuous near the temporal pole as the sole remaining mesial structure. The most important consideration for this stage is the superior limit of resection, an imaginary line between the choroidal point (anteriormost extent of the choroid plexus in the choroidal fissure and point of entry of the anterior choroidal artery into the ventricle) and the limen insulae (threshold of the insula and anterior limit of the insula and transition point between the insular and the frontal cortex). This line is roughly approximated by extending an imaginary line parallel and coaxial with the choroid plexus. Venturing superior to this limit risks injury to the globus pallidus. Adjoining structures to the amygdala, such as the white matter of the neocortex and the hippocampus and PHG, have already been removed. The bulbous structure of the amygdala is removed and sent en bloc for analysis, and the remaining contents of the uncus are peeled off the medial arachnoid membrane. The resection is thus completed (Fig. 109-5B and C).
Through the medial arachnoid membrane, the PCA is visible coursing posteriorly around the midbrain, and the oculomotor nerve is seen traveling anteriorly (Fig. 109-6). Bipolar cautery in the vicinity of this arachnoid membrane is therefore not advised. The trochlear nerve may be seen running along and below the edge of the tentorial incisura. After meticulous hemostasis is achieved, the cavity is lined with oxidized cellulose, and the wound is closed in a standard fashion.
FIGURE 109-6 Completed resection. The surgeon’s view of the resection cavity following a completed left ATL. The mesial arachnoid membrane should be preserved to protect the nerves and vessels in the ambient cistern. Through the membrane, the oculomotor nerve (CN III) can be visualized coursing anteriorly, as well as the PCA wrapping around the midbrain. Superior is the bottom aspect of the figure; anterior is the right aspect of the figure.
In patients with a clearly defined unilateral mesial temporal epileptic focus, selective resection of the mesial temporal lobe contents, without the lateral neocortical resection characteristic of a formal ATL, may be a valid option. A variety of procedures for SAH have been developed. These differ in the approach route taken to the mesial structures but are similar in their goal of removing the amygdala, a portion of the uncus, the anterior about 2 cm of hippocampus, and the adjoining PHG.
Niemeyer described the first approach for SAH in the late 1950s,20 soon after Falconer et al. developed the standard ATL.18 In this transcortical transventricular approach, an incision 2 to 3 cm long is made in the MTG, approximately 4 cm posterior to the temporal pole. Dissection through this incision leads to the temporal horn of the lateral ventricle, which lies 3 to 3.5 cm deep to the cortical surface. Upon entering the ventricle, the choroid plexus again provides a helpful landmark as the superomedial boundary of the resection. The PHG is subpially aspirated, and the hippocampus is divided at its anterior and posterior extents in a similar fashion to that described earlier. It can then be mobilized laterally, allowing the irrigating vessels in the hippocampal fissure to be bipolar cauterized and sharply sectioned. Aspiration of the fimbria along the medial aspect of the hippocampus frees the specimen. Removal of the amygdala and subpial aspiration of the uncus anteriorly complete the resection. Advantages of this SAH procedure include its straightforward approach, but an important disadvantage is the difficulty of obtaining an en bloc resection for histologic analysis. Variations to the transcortical transventricular SAH have been described by Olivier, with an entry point in the anterior aspect of the STG rather than the MTG.37
In an attempt to leave the lateral temporal neocortex completely intact, Wieser, Yasargil, and colleagues developed the trans-sylvian approach, a technically demanding procedure that accesses the mesial temporal lobe via a sylvian fissure dissection.21,22 The patient’s head is turned laterally 30 degrees, and the vertex is lowered 20 degrees such that the malar eminence is superior. This position allows a vertical angle of dissection through the sylvian fissure. A pterional craniotomy is performed, approximately 2 cm posterior to the typically described location.38 Following craniotomy and durotomy, the sylvian fissure is opened from the carotid bifurcation to about 2 cm beyond the middle cerebral artery bifurcation. A 1- to 2-cm incision is made in the inferior portion of the circular sulcus of the insula. The amygdala lies just a few millimeters deep to the surface. Opening into the ventricle at this point provides a helpful anatomic point of reference. Moving anteroinferiorly, the amygdala is aspirated and the anterior PHG is subpially resected. Attention is then turned posteroinferiorly to the hippocampus and remainder of PHG. The hippocampus is rotated laterally, and the feeding vessels in the hippocampal fissure are divided, freeing the hippocampus medially. It is detached posteriorly by making a transverse section at the posterior aspect of the peduncles. The hippocampus is thus circumferentially freed and removed with the PHG en bloc. This approach is technically challenging, requiring superior microneurosurgical skill and detailed anatomic knowledge of the region. The theoretical advantage of this technique is its sparing of any injury to the temporal cortex, but damage to the sylvian vessels or instigation of vasospasm is a significant source of morbidity.
Finally, a variety of subtemporal approaches have been described.39–41 Motivation behind their development arose from the desire to leave the lateral neocortex and temporal stem intact. Disadvantages are significant, however, including temporal lobe retraction; risk of injury to venous drainage, including the Labbé vein; and difficulties with surgical orientation. As a result, these approaches are usually reserved for mesial temporal lesionectomies requiring neocortical sparing.