Amygdalohippocampectomy

Background

This article discusses the indications for selective amygdalohippocampectomy (SAH) and the surgical techniques used to perform it.

Epilepsy is a common condition that affects nearly 1% of the world’s population. Although about two thirds of patients with epilepsy achieve good seizure control with antiepileptic medications, the remaining one third have seizures that are resistant to medications and therefore may be considered as candidates for epilepsy surgery. In suitable candidates, surgical therapy is clearly superior to the best medical therapy. ^[1]

Surgery is most often considered and most frequently successful in patients with temporal lobe epilepsy (TLE). Most patients with TLE have seizures that originate from the mesial-basal temporal lobe structures (hippocampus, amygdala, parahippocampal gyrus). Traditionally, the standard surgical treatment has been an en bloc anterior temporal lobectomy (ATL).

ATL involves resection of approximately 3-6 cm of anterior temporal neocortex (depending on language dominance), which permits the surgeon to access and resect mesial structures, including the amygdala and the hippocampus. A modification popularized by the Yale group limits neocortical resection to 3.5 cm from the temporal pole and spares the superior temporal gyrus, obviating the need for language mapping in most cases. ^{[2, 3]}

The primary advantages of ATL are the relatively low morbidity and the good surgical exposure that allows complete resection of mesial structures; this procedure also permits pathologic examination of en bloc specimens. ATL is still commonly used today.

Data from animal models and from pathologic, electrophysiologic, and structural and functional imaging studies support the contention that most temporal lobe epilepsy arises from mesial temporal structures. This suggests the possibility that more targeted mesial temporal resections that spare temporal neocortex (eg, SAH) might provide equally good seizure control and result in fewer neuropsychological sequelae than ATL (see the image below).

In 1958, Niemeyer reported such a procedure, using a small incision in the middle temporal gyrus to access the temporal horn and selectively resect mesial temporal structures. ^[4] Subsequently, Wieser and Yasargil popularized a transsylvian approach and reported outcomes of large numbers of patients who underwent this procedure. ^{[5, 6]} Other techniques, including the subtemporal approach ^[7] and variants of the transcortical approach, have been described. ^[8]

Many individual studies suggest that for patients with well-defined mesial temporal onset seizures, particularly those with the syndrome of hippocampal sclerosis, seizure-free outcomes after SAH are equivalent to outcomes after procedures that involve more extensive temporal neocortical resections. ^{[9, 10, 11, 12, 13, 14]} A systematic review and meta-analysis suggested a slight advantage in seizure-free rates in patients who underwent ATL; however, methodological concerns from combining potentially biased studies have strengthened the call for a randomized controlled trial of SAH versus ATL for treatment of mesial temporal lobe epilepsy. ^{[15, 16, 17]}

Presuming near equivalence in seizure-free outcomes, SAH would be preferred over ATL if it could be clearly demonstrated that the more selective procedure would result in superior postoperative neuropsychological outcomes. Here, the results have been mixed.

Although many studies suggest that SAH can spare some aspects of cognitive function as compared with ATL, ^{[5, 18, 10, 19, 20, 21, 22, 23, 11, 24]} others have reported mixed findings and have not shown the more selective procedure to provide a clear benefit. ^{[25, 26, 27, 28]} SAH can still cause significant verbal memory impairment in some cases of dominant temporal lobe resection, and it does not eliminate the need for careful preoperative evaluation (including assessment of risk to memory function).

Relevant Anatomy

The cerebrum is the largest component of the brain. It is divided into right and left hemispheres. The corpus callosum is the collection of white matter fibers that joins these hemispheres.

Each of the cerebral hemispheres is further divided into 4 lobes: the frontal lobe, the parietal lobe, the temporal lobe, and the occipital lobe. The medial temporal lobe structures are considered by some to be part of the so-called limbic lobe.

The limbic system is a grouping of cortical and subcortical structures involved in memory formation and emotional responses. The limbic system allows for complex interactions between the cortex, the thalamus, the hypothalamus, and the brainstem. The limbic system is not defined by strict anatomic boundaries but incorporates several important structures. The limbic structures conventionally include the amygdala, the hippocampus, the fornix, the mammillary bodies, the cingulate gyrus, and the parahippocampal gyrus.

For more information about the relevant anatomy, see Brain Anatomy.

Indications

Most commonly, suitable candidates for SAH are selected on the basis of the convergence of several lines of evidence implicating unilateral mesial temporal structures as the epileptogenic region. These lines of evidence include the following:

• Compatible ictal semiology and neurologic history

• Magnetic resonance imaging (MRI) showing abnormality in the mesial temporal structures (most commonly, hippocampal atrophy and/or mesial temporal signal change on T2-weighted/fluid-attenuated inversion recovery [FLAIR] sequences); patients with exclusively mesial temporal foreign tissue lesions (eg, low-grade tumor) or neurodevelopmental abnormalities may also be suitable candidates

• Video electroencephalography (EEG) documenting compatible ictal semiology and stereotyped ictal onset on scalp EEG consistent with mesial temporal origin; interictal EEG may reveal concordant unilateral or bilateral (usually predominantly ipsilateral) epileptiform discharges

For patients in whom these lines of evidence do not converge, or for whom some data points are lacking (eg, those with no MRI lesion or with poorly localized ictal onsets on EEG), additional studies may be required, as follows:

• Positron-emission tomography (PET)

• Magnetoencephalography (MEG)

• Ictal single-photon emission computed tomography (SPECT)

Particularly in nonlesional cases, if standard evaluation, supplemented by specialized imaging studies, defines a unilateral temporal lobe onset, intracranial EEG monitoring may be required for distinguishing mesial from temporal neocortical onset so as to determine whether SAH is indicated.

Contraindications

Contraindications to SAH include the following:

• Nonepileptic events

• Idiopathic (primary) generalized epilepsies

• Extratemporal focal epilepsy

• Independent bitemporal onset seizures (in most cases)

• Severe impairment of verbal and visuospatial memory (as demonstrated by neuropsychological testing and intracarotid amytal testing)

• Temporal neocortical epilepsy

• Temporal lobe epilepsy without clear localization to mesial temporal structures

Technical Considerations

Careful attention to surgical technique will lead to better technical results and reduced complication rate.

Best practices

The following measures are recommended in the performance of SAH:

• Navigate from "safe zone" to "safe zone"

• Use neuronavigational guidance frequently, particularly during the early learning curve

• Establish routine way points for surgical image-guided navigation

• The initial subpial dissection should be aimed inferiorly and anteriorly so that the middle fossa floor is encountered first

• Work from the anterior to the posterior uncus, carefully exposing the pia

• Identify the choroid plexus, then the choroidal fissure

• Never extend the resection superior to the choroidal fissure

• "Box out" the region superior to the choroidal fissure with a flat self-retaining retractor to prevent inadvertent injury

• Use 2 retractors, one on the choroid plexus retracting superiorly to prevent injury superior to the fissure and the other in the ventricle to expose the posterior pes hippocampi

• Work posteriorly to mobilize the hippocampus from the fissure, then divide the pes hippocampi posteriorly to coincide with the anteroposterior location of the collicular plate on axial guidance MRI

• Dissect the parahippocampal gyrus from posterior to anterior to liberate the pes

• Carefully mobilize the pes hippocampi based on the hippocampal fissure, avoiding injury to any perforating arteries

• Obtain absolute hemostasis.

• Line the medial pial boundary with thrombin-soaked gelatin sponge (eg, Gelfoam) and oxidized cellulose fabric on the resection bed proper

Complication prevention

Potential complications include the following:

• Hemorrhage

• Infarction (commonly of deep penetrating vessels, leading to lacunar stroke)

• Infection

• Failure of neuronavigation protocols, leading to inaccurate resection

• Incomplete resection

• Variable contralateral homonymous superior quadrant visual field defect, from injury to the Meyer loop (usually asymptomatic)

• Memory impairment ^[29]

• Transient dysnomia

• Mood changes

Intraoperative complications can be minimized by strict adherence to timeout procedures, careful patient positioning, and careful visual identification of landmarks coupled with repeated reconfirmation of stereotactic findings. Attention to careful patient selection and preoperative testing can minimize the risk to memory and the chances of mood disturbances and can maximize efficacy by excluding inappropriate patients.

An image-based frameless intraoperative guidance system is employed. Magnetic resonance imaging (MRI) with fiducial placement is performed just before the operation. Anesthesia

Routine general anesthesia with endotracheal intubation is indicated. Antibiotics are administered. To minimize intraoperative brain shift, mannitol is avoided.

The patient is placed in the supine position, with the head rotated 90º to the opposite side and parallel to the floor. The head is held in position in a 3-pin fixateur.

Approach Considerations

Various approaches to selective amygdalohippocampectomy (SAH) have been developed. ^[30] Of these, the transcortical approach will be described in some detail (see the video below). Additional comments will be made about alternative approaches (eg, transsylvian and subtemporal).

Transcortical Approach

Scalp fiducials are registered, and the planned entry point is marked on the scalp, along with planned bone flap and scalp incisions. The scalp is prepared, draped, and infiltrated with lidocaine 1%, bupivacaine 0.25%, and epinephrine.

A linear scalp incision is performed. The temporalis fascia is incised, separated from the periosteum, and retracted laterally. A neuronavigation system is used to determine the location of the temporal craniotomy. The dura is opened and flapped inferiorly.

The neuronavigation system is used to estimate the distance from the temporal pole and then to plan an entry point in the middle temporal gyrus in a section that is free of cortical vessels. The entry point should be no greater than 3.5 cm from temporal pole (dominant temporal lobe). A 1.5-2 cm cortical incision is planned. The cortical surface is opened with a bipolar cautery (see the image below).

Guided by neuronavigation, dissection is performed toward the temporal pole. When the temporal horn is entered, 2 self-retaining brain retractors are set up to optimize the view of the intraventricular anatomy (see the image below).

The following key structures are identified:

• Dural floor of the middle fossa

• Pial boundary overlying the suprasellar cistern (carotid artery, third cranial nerve)

• Uncus of the temporal lobe

• Medial prominence of the hippocampus

• Choroid plexus

• Choroidal fissure

Resection of the parahippocampal gyrus is performed, beginning with subpial resection of the uncus and then proceeding medially and posteriorly. Neuronavigational confirmation is frequently obtained at this stage. To avoid injuring the posterior cerebral artery, third cranial nerve, or cerebral peduncle, the mesial pial border must be strictly preserved.

After parahippocampal gyrus resection, the hippocampus is mobilized laterally into the resection cavity. Hippocampal resection proceeds from anterior to posterior, with care taken to identify and preserve the anterior choroidal artery. The resection is extended posteriorly to the level of the tectal plate on axial navigation magnetic resonance imaging (MRI). Neuronavigation is used to confirm the completeness of the resection.

The resection cavity is inspected, and hemostasis is achieved. Brain retractors are removed, and the dura is closed. The bone flap is plated. The temporalis muscle is reapproximated, and the scalp is closed in layers to the skin with reabsorbable sutures.

After completion of anesthesia, a neurologic examination is performed. A postoperative computed tomography (CT) scan of the head is obtained. Antiepileptic medications are continued.

The patient is monitored overnight in a neurological intensive care unit (ICU). The postoperative hospital stay is generally 3-4 days.

Transsylvian Approach

The transsylvian approach to SAH is approach was popularized by Wieser and Yasargil. ^{[6, 31, 32]} Its advantages include the following:

• It avoids injury to the temporal neocortex and underlying white matter, which are traversed in the transcortical approach

• It allows en bloc resections

The disadvantages are as follows:

• It is technically difficult

• It affords only limited surgical exposure

• Exposure of sylvian vessels poses a risk of vascular injury or vasospasm ^[33]

• It results in transection of the temporal stem

Subtemporal Approach

The advantages of the subtemporal approach to SAH include the following ^[7] :

• It largely avoids injury to the Meyer loop (visual field defect)

• It might produce fewer neuropsychological sequelae ^{[21, 34]} (the available data are insufficient to establish whether this is so)

The disadvantages are as follows:

• It may necessitate excessive retraction of the temporal lobe

• It may result in injury to the vein of Labbe

• It may necessitate removal of the zygomatic process