The Paramedian Supracerebellar-Transtentorial

J Neurosurg 116:773–791, 2012

The paramedian supracerebellar-transtentorial approach to the entire length of the mediobasal temporal region: an anatomical and clinical study Laboratory investigation

Uğur Türe, M.D.,1 Mehmet Volkan Harput, M.D.,1 Ahmet Hilmi Kaya, M.D.,1 Praveen Baimedi, M.D.,1 Zeynep Firat, Ph.D.,1 Hatice Türe, M.D.,2 and Canan Aykut Bingöl, M.D.3 Departments of 1Neurosurgery, 2Anesthesiology, and 3Neurology, Yeditepe University School of Medicine, İstanbul, Turkey

Object. The exploration of lesions in the mediobasal temporal region (MTR) has challenged generations of neurosurgeons to achieve an appropriate approach. To address this challenge, the extensive use of the paramedian supracerebellar-transtentorial (PST) approach to expose the entire length of the MTR, as well as the fusiform gyrus, was investigated. Methods. The authors studied the microsurgical aspects of the PST approach in 20 cadaver brains and 5 cadaver heads under the operating microscope. They evaluated the features, advantages, difficulties, and limitations of the PST approach and refined the surgical technique. They then used the PST approach in 15 patients with large intrinsic MTR tumors (6 patients), tumor in the posterior fusiform gyrus with mediobasal temporal epilepsy (MTE) (1 patient), cavernous malformations in the posterior MTR including the fusiform gyrus (2 patients), or intractable MTE with hippocampal sclerosis (6 patients) from December 2007 to May 2010. Patients ranged in age from 11 to 63 years (mean 35.2 years), and in 9 patients (60%) the lesion was located on the left side. Results. In all patients with neuroepithelial tumors or cavernous malformations, the lesions were completely and safely resected. In all patients with intractable MTE with hippocampal sclerosis, the anterior two-thirds of the parahippocampal gyrus and hippocampus, as well as the amygdala, were removed selectively through the PST approach. There was no surgical morbidity or mortality in this series. Three patients (20%) with high-grade neuroepithelial tumors underwent postoperative radiotherapy and chemotherapy but needed a second surgery for recurrence during the follow-up period. In all patients with MTE, antiepileptic medication could be decreased to a single drug at lower doses, and no seizure activity has occurred until this point. Conclusions. The PST approach provides the surgeon precise anatomical orientation when exposing the entire length of the MTR, as well as the fusiform gyrus, for removing any lesion. This is a novel technique especially for removing tumors involving the entire MTR in a single session without damaging neighboring neural or vascular structures. This approach can also be a viable alternative for selective removal of the parahippocampal gyrus, hippocampus, and amygdala in patients with MTE due to hippocampal sclerosis. (http://thejns.org/doi/abs/10.3171/2011.12.JNS11791)

Key Words • amygdala • fusiform gyrus • hippocampus • mediobasal temporal region • parahippocampal gyrus • paramedian supracerebellar-transtentorial • semisitting position • diagnostic and operative techniques • skull base

he MTR is actually part of the limbic lobe and in- anteriorly by the lesser wing of the sphenoid bone; and cludes 2 main portions, the paralimbic areas (meso- laterally by the rhinal and collateral sulci. The posterior cortex) and the limbic areas (corticoid and allocor- border of the MTR is the isthmus of the cingulate gyrus tex).T The paralimbic areas consist of the temporal pole and and the tip of the cuneus, which is the junction between the parahippocampal gyrus, and the limbic areas consist the parietooccipital and calcarine sulci.6,7,31,34,52,58,61,64,65 The of the amygdala, piriform cortex, and the retrocommis- temporal and occipital neocortical structures cover the sural part of the hippocampal formation.23,24 The MTR is MTR and are therefore significant obstacles to surgery of roughly limited medially by the lateral wall of the cav- the MTR. The need to incise, resect, or retract the tem- ernous sinus and the carotid, crural, and ambient cisterns; poral or occipital lobes during surgery of the MTR is a controversial issue.1,3,4,8–10,12,13,15,20,26,27,29,30,33,35–38,42–48,50,57–59,67 Abbreviations used in this paper: EEG = electroencephalography; This enclosed and extended localization near these highly MTE = mediobasal temporal epilepsy; MTR = mediobasal temporal significant structures renders the MTR a difficult surgical region; PST = paramedian supracerebellar-transtentorial; ROI = area in some respects. This location necessitates the least region of interest; TEE = transesophageal echocardiography. traumatic approach without the risk of injury to overlying

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Unauthenticated | Downloaded 10/09/21 06:20 AM UTC U. Türe et al. structures, and extended localization may require more after obtaining institutional board review approval, we than single-session surgery when a lesion involves the en- used the PST approach in 15 patients in the semisitting tire length of the MTR. position. Six (40%) had large tumors involving the entire Various approaches to the MTR include the anteri- MTR, 1 (6.7%) had a lesion in the posterior fusiform gy- or,9,48,60,63 lateral,5,12,30,32,37,45,52 and posterior,15,28,46,56,57,61,62,66 rus with MTE, 2 (13.3%) had cavernous malformations, which have been introduced with different variations. In and 6 (40%) had drug-resistant MTE due to hippocampal reviewing these approaches carefully, one notes that the sclerosis. All patients were treated at our institution be- approaches deemed “less invasive” are restricted to only tween December 2007 and May 2010 by the senior au- 1 or 2 portions of the MTR. For example, the lateral trans- thor (U.T.). The mean patient age was 35.2 years (range cortical or transsulcal approaches are mainly restricted to 11–63 years). Eight (53.3%) were male, and 7 (46.7%) the anterior and middle portions of the MTR,27,30,32 and were female. Each patient suffered from seizures with a the small petrosal approach is restricted to the middle duration of symptoms ranging from 10 days to 21 years. portion.52 Although the pterional-transsylvian approach Preoperative radiological examinations included plain is appropriate for large tumors of the MTR, it is restricted radiographs, MR images, MR angiograms, and 3-planar to the anterior and middle portions of the MTR for pa- CT scans, along with the use of bone windows and 3D tients with MTE.60–63 The supratentorial infraoccipital reconstruction. Neuropsychological tests and a visual approach,46 the lateral occipital subtemporal approach,57 field study were done preoperatively and 2 months after and the supracerebellar transtentorial approach (E. de surgery, except for 1 patient in whom these tests were not 28,56,66 Oliveira, personal communication, 2008) are mainly possible because she was severely confused and disori- restricted to the posterior portion of the MTR. Selective ented in the preoperative period (Case 3). Detailed infor- handling of the MTR has also been used for lesions ex- mation about these patients is summarized in Table 1. tending posteriorly, which is appropriate but necessitates Presurgical evaluation was done for patients with staged surgery and requires a combination of 2 different MTE due to hippocampal sclerosis who had no response approaches: the pterional-transsylvian approach to the to at least 2 antiepileptic drugs. Patients were included anterior part and the posterior interhemispheric approach 62 if they had unilateral hippocampal sclerosis documented to the posterior part of the MTR. with high-resolution 3-T MR images (Achieva, Philips). In this manuscript, we describe a novel approach to Hippocampal sclerosis was defined as atrophy of the the entire length of the MTR, selectively, with its ana- amygdala-hippocampus-parahippocampal complex on tomical basis, namely, the paramedian supracerebellar- T1-weighted images and/or increased signal or disruption transtentorial approach. This approach was first defined of the internal architecture of the mediobasal temporal in cadaveric studies and then used in clinical application. structures on T2-weighted or FLAIR images. All patients with MTE were evaluated using video- EEG monitoring with electrode placement according to Methods the Extended International 10–20 System, with additional Microsurgical Anatomical Study anterior temporal electrodes designated T1 and T2 and sphenoidal electrodes (128-channel, Telefactor Beehive). Twenty brain specimens obtained from routine au- At least 3 seizures were recorded in each patient. Seizure topsies and an additional 5 cadaver heads were used for semiology and ictal and interictal EEG findings were used the microsurgical anatomical study of the PST approach for lateralization and localization. All patients underwent by the senior author (U.T.). The brains were fixed in a FDG-PET/CT scanning (Achieva, Philips). Neuropsycho- 10% formaldehyde solution for a minimum of 2 months. logical tests were also done in all patients. Patients with The detailed anatomy of this region was studied through concordant neuroradiological imaging (both MR imaging the fiber dissection technique, which has been described and PET CT) and neuropsychological test results were es- previously,16,17,19,53,54 and the surgical landmarks of the pecially selected as candidates for this surgical approach. MTR and fusiform gyrus were investigated. In the formalin-fixed cadaver heads, the bilateral internal carotid Patients who had suspected involvement of temporal neo- and vertebral arteries as well as the jugular veins were cortical or extratemporal areas as the source of seizures dissected at the neck and then were cannulated. After sa- were excluded. Intraoperative corticography with sub- line irrigation to wash out any residual luminal clots, the dural strip electrodes and hippocampal depth electrodes arteries and veins were perfused with red and blue sili- was done in all patients to confirm epileptogenic areas. cone, respectively. The microsurgical aspects of the PST Neuroradiological Study. Before surgery and 2–3 approach were carried out under the operating micro- months afterward, all patients underwent imaging using a scope at × 6 to × 25. Particular attention was paid to the 3-T MR imaging unit (Achieva, Philips) with an 8-channel relationships between the MTR and the vital neural and sensitivity encoding (SENSE) head coil. Postcontrast T1- vascular structures. The features, indications, advantages, weighted 3D turbo field echo was acquired in the sagittal and limitations of the PST approach were investigated plane (TR 8.5 msec, TE 4 msec, slice thickness 1 mm). and compared with other previously described surgical Diffusion tensor images were acquired using single-shot approaches. spin echo echo planar imaging (TR 10,000 msec, TE 53 msec, EPI factor 67, slice thickness 2.5 mm, gap 0 mm). Clinical Material Sixteen diffusion directions at b = 800 seconds/mm2 were Based on our microsurgical anatomical study and acquired in addition to b = 0 images. The acquisition time

774 J Neurosurg / Volume 116 / April 2012 Unauthenticated | Downloaded 10/09/21 06:20 AM UTC Paramedian supracerebellar-transtentorial approach Outcome recurrent tumor recurrent recurrent tumor; died of recurrent tumor 30 mos after op 1st gery tumor recurrent for no deficit no deficit; no seizure; CBZ 600 mg/d no deficit no deficit no deficit200LTG mg/dor seizure no deficit; reop 9 mos postop for no deficit or seizure; CBZ 600 mg/d no deficit or seizure; CBZ 600 mg/d no deficit or seizure; CBZ 800 mg/d no deficit1200 or seizure; VPA mg/d no new deficit no deficit no deficit;13 mosreop postop for no deficit; reop 28 mos after sur- no deficit

Therapy† Histopathology/Adjuvant Histopathology/Adjuvant Grade II ma Grade II + chemotherapy hippocampal sclerosis cavernous malformation cavernous diffuse astrocytoma WHO pleomorphic xanthoastrocyto- hippocampal sclerosis anaplastic astrocytoma Grade III/chemotherapy hippocampal sclerosis hippocampal sclerosis hippocampal sclerosis hippocampal sclerosis glioblastoma WHO Grade IV/ chemotherapy malformation cavernous glioblastoma Grade IV/radio- Grade glioblastoma + chemotherapy IV/radio- Grade glioblastoma diffuse astrocytoma Grade II

Excision sel-AH total macroscopic total macroscopic total sel-AH macroscopic total sel-AH sel-AH sel-AH sel-AH total macroscopic total macroscopic macroscopic macroscopic total macroscopic total total macroscopic

+ posterior Op Approach lt-sided PST lt-sided PST rt-sided PST lt-sided PST rt-sided PST lt-sided PST lt-sided PST lt-sided PST rt-sided PST rt-sided PST lt-sided PST lt-sided PST lt-sided PST rt-sided PST rt-sided PST interhemispheric

Neuroradiological Diagnosis hippocampal gyrus & fusiform gyri of the MTR form gyrus gyri tumor of MTR of the MTR of the MTR + posterior & middle portions of the cingulate gy- lt-sided MTS lt-sided posterior lesion of para- rt-sided tumor parahippocampal of lt-sided MTS rt-sided tumor along entire length lt-sided MTS lt-sided MTS lt-sided MTS rt-sided MTS lt-sided fusiform-parahippocampal rt-sided posterior lesion of fusi- gyrus lt-sided tumor along entire length rt-sided tumor along entire length fusiform posterior in tumor lt-sided rt-sided tumor along entire length rus

+ radiotherapy 3 yrs prior; rt mg/d, OXC 600mg/d, OXC 1000 mg/d, VPA mg/d LEV 3000 400 mg/d, TPM mg/d,200 LTG CBZwk); 900 mg/d, LEV 3000 mg/d, VPA mg/d 1000 CBZ 1000mo); mg/d, LEV 3000 mg/d mo); DPH 400mo); mg/d, LEV 3000 mg/d CLZmo); 2 mg/d, LEV 300 2500 mg/d, LTG mg/d, ZNS 400 mg/d monitored another at institution; due to tumor growth, she came to our institution; neurologically intact neurologically intact disoriented, noncooperative, confused, was & had lt hemiparesis lt had & Symptoms, Neurological Signs, & Medication & Signs, Neurological Symptoms, 20-yr Hx of seizures 400 (2–8 times/mo); LTG 8-mo Hx of seizures 1-mo Hx of seizures 17-yr Hx of intractable17-yr seizures (3–4 times/wk); mg/d Hx of 7-mo seizures 20-yr Hx of intractable seizures (4–5 times/ history21-yr of intractable seizures times/ (1–2 18-yr history of intractable seizures (3–4 times/ history11-yr of intractable seizures times/ (1–2 gyrus glioblastoma frontal superior posterior resection hemiparesis 8-mo Hx of seizures generalized seizure 10 days prior days admission/generalized to seizure 10 1-yr Hx of seizures & rt-sided MTR tumor; 20-day Hx of seizures; 400 VPA mg/d 1-mo Hx of seizures & lt hemiparesis; patient

Sex Age (yrs), 11, M 37, F 37, 37, F 37, 31, M 31, 21, M 12, M 12, 26, M 56, F 24, F 24, 40, F 29, F 44, M 55, M 42, M 42, 63, F Grades are based on the WHO grading system. CBZ = carbamazepine; CLZ = clonazepam; DPH = diphenylhydantoin; Hx = history; LEV = levetiracetam; = lamotrigine; LTG MTS = mediobasal temporal sclerosis; = oxcarbazepine; OXC sel-AH = 11 12 13 14 15 10 5 6 7 8 9 1 2 3 4 No.

Case selective amygdalohippocampectomy; TPM = topiramate; = valproic VPA acid; ZNS = zonisamide. † * TABLE 1: Characteristics 1: TABLE of patients who underwent surgery through the PST approach*

J Neurosurg / Volume 116 / April 2012 775 Unauthenticated | Downloaded 10/09/21 06:20 AM UTC U. Türe et al. was about 6 minutes. Sixty slices were taken for whole- the MTR into superior and inferior parts, as the anterior brain coverage from the vertex to the foramen magnum. calcarine sulcus separates these structures naturally. The All data were transferred to the MR imaging system’s superior portion (parahippocampocingulate) is separated Release 2.6 Level 3 workstation (Achieva, Philips). The from the cingulate gyrus by the isthmus cinguli. The fiber tracking software was used to generate 3D diffu- superior portion contains the gyri Andrea Retzii, gyrus sion tensor tractography, which allows virtual dissection fasciolaris, and the fasciola cinerea. The isthmus cinguli of white matter pathways. The directional color-coding forms the transition between the posterosuperior parahip- of the fiber tracts in fractional anisotropy maps was as pocampal gyrus and the posterior cingulate gyrus behind follows: red for left- to right-oriented fibers, blue for cra- and below the splenium of the corpus callosum. The infe- niocaudal-oriented fibers, and green for anteroposterior- rior portion (parahippocampolingual) is connected with oriented fibers. For tracking the white matter fibers, the the anterior lingual gyrus, and an imaginary line between ROI method was applied. These fibers are generated from the preoccipital notch and the tip of the cuneus forms the multiple ROIs placed on color-coded fiber pathways.18 The posterior border of the MTR. The lingual (medial oc- fibers of the anterior commissure (ac, red), uncinate fas- cipitotemporal) gyrus is demarcated from the fusiform ciculus (unc, green), posterior thalamic peduncle includ- (lateral occipitotemporal) gyrus by the posterior portion ing the optic radiation (or, yellow), and the frontooccipital of the collateral sulcus, and from the cuneus by the calca- fasciculus (fof, blue) were generated. A T1-weighted 3D rine sulcus. The intralingual sulcus separates the lingual turbo field echo sequence was used for the background gyrus into 3 portions: superior, inferior, and anterior. The anatomical structure. anterior portion, which we call the parahippocampolin- The frontooccipital fasciculus connects the occipital gual gyrus, belongs to the posterior portion of the MTR, and frontal lobes.54 To define this tract, the first ROI was while the superior and inferior portions belong to the oc- defined in the frontal lobe and the second in the occipi- cipital lobe. The collateral sulcus forms the lateral margin tal lobe on the fiber pathways in the coronal plane. The of the posterior portion of the MTR (Fig. 1). anterior commissure connects the anterior and ventral The MTR is deeply enclosed and is close to highly temporal lobes of the 2 hemispheres. For tracking the fi- vital neural and vascular structures. These are the optic bers of the anterior commissure, 2 ROIs were defined 10 tract and the lateral geniculate body; the oculomotor and mm away from the left and right sides at the point where trochlear nerves; the midbrain; the internal carotid, the the anterior commissure is seen in the midsagittal plane. anterior choroidal, and posterior cerebral arteries; the The uncinate fasciculus connects the anterior temporal basal vein of Rosenthal and its tributary medially; and lobe with the medial and lateral orbitofrontal cortex. To the sublentiform portion of the internal capsule. This por- set the uncinate fasciculus, the first ROI was defined in tion of the internal capsule includes the frontopontine, the anterior temporal lobe white matter, and the second temporopontine, and occipitopontine fibers; the inferior was defined around the white matter of the anterior basal thalamic peduncle; and the posterior thalamic peduncle, portion of the frontal lobe in the coronal plane. The op- which includes the optic radiation (Appendix). By using tic radiation connects the lateral geniculate body to the the fiber dissection technique, these significant anatomi- occipital cortex. The first ROI was outlined on the oc- cal structures of the temporal lobe and their relations to cipital visual cortex in the coronal plane, the second ROI the surrounding formations can be seen (Figs. 2 and 3). was defined on the lateral geniculate body in the sagittal The visual cortex (Brodmann areas 17–19) is located pos- plane, and the third was defined on the optic tract in the terior to the MTR, and the basal language area in the fu- coronal plane.2 siform gyrus is located lateral to the MTR. The features, advantages, and limitations of the PST Anesthesiology Considerations. All patients were ex- approach were investigated, and we found that the ap- amined preoperatively by a cardiologist and were evalu- proach is feasible for exposing the entire length of the ated using transthoracic echocardiography to exclude MTR as well as the fusiform gyrus, even with cadaver anyone with atrial or ventricular septal defects, as these specimens (Figs. 4–7). defects contraindicate the use of the semisitting position. Surgical Technique Results Microsurgical Anatomical Study Preparing and Positioning. In the operating room, antiembolic stockings and a pneumatic sequential com- The MTR is separated into 3 portions: the anterior, pression device are applied to the patient’s legs to prevent middle, and posterior portions. The anterior portion starts deep venous thrombosis. After endotracheal intubation, from the piriform cortex and extends to the tip of the un- the patient undergoes placement of a TEE probe to moni- cus. The temporal incisura and the rhinal and collateral tor for possible air embolism. Before the positioning, a sulci form the lateral border of the anterior portion. This “bubble test” with the Valsalva maneuver is done to fur- portion consists of the amygdala, uncus, and head of the ther evaluate for any possible shunting from the right to parahippocampal gyrus and hippocampus.5 The middle the left atrium. This bubble test is crucial because trans- portion extends to the collicular level of the midbrain. thoracic echocardiography, which is done in the preop- The collateral sulcus is the lateral border of the middle erative period, may miss atrial or ventricular septal de- portion of the MTR. The posterior portion extends poste- fects, and it is imperative to confirm that there are no such riorly from this level. We divided the posterior portion of defects. Transesophageal echocardiography provides de-

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fixation of the headholder. Flexing the leg to increase the intraabdominal pressure can also help to increase venous blood return to the heart. Hyperextension or hyperflexion of the leg must be avoided to prevent nerve damage. In the preoperative period, the patient should be examined to delineate the normal range of motion. To preserve the intravascular volume of the patient in this semisitting position, we avoid the use of diuretics. Also, we did not use positive end expiratory pressure in our series. Avoiding spontaneous ventilation is also important to prevent air embolism. Incision. A vertical, linear paramedian incision is made. It passes through the midpoint of an imaginary line between the external occipital protuberance and the mas- Fig. 1. The inferolateral view of the left cerebral hemisphere in a toid process. The incision extends one-third above and cadaver brain showing portions of the MTR, which are separated by two-thirds below the superior nuchal line (Fig. 8B). De- dotted lines. The arrows indicate posterior extensions of the parahip- pending on the patient’s skin thickness and muscle mass, pocampal gyrus to the isthmus of the cingulum (superior) and to the lin- the incision may be extended superiorly and inferiorly, gual gyrus (inferior). No exact border shows where the MTR ends. The but a 12-cm incision is generally sufficient for exposure. asterisk indicates the tip of the cuneus. Abbreviations with white letters denote the sulci and fissures. A = anterior portion of the mediotemporal The occipital artery is usually encountered twice, initial- region; cas = calcarine sulcus; cas-a = anterior calcarine sulcus; cc-s = ly superficial to the occipital belly of the occipitofron- splenium of the corpus callosum; cig = cingulate gyrus; cos = collateral talis muscle, and later while dissecting the suboccipital sulcus; cp = cerebral peduncle; cun = cuneus; fg = fusiform gyrus; ils = muscles. Next, we split the occipital belly of the frontooc- inferior lingual sulcus; ist = isthmus cinguli; lg-a = anterior lingual gyrus; cipital muscle, and the suboccipital muscles are separated lg-i = inferior lingual gyrus; lg-s = superior lingual gyrus; lgb = lateral with electrocautery in line with the incision. The occipital geniculate body; M = middle portion of the mediotemporal region; ots = artery beneath the splenius capitis muscle should be co- occipitotemporal sulcus; P = posterior portion of the mediobasal tem- agulated and divided. The muscle mass is retracted using poral region; pc = piriform cortex; pon = preoccipital notch; pos = parietooccipital sulcus; rs = rhinal sulcus; s = subiculum; sups = subparietal 2 Whitlenar retractors, one curved superiorly and the oth- sulcus; tp = temporal pole; u = uncus; us = uncal sulcus; II = optic nerve. er straight inferiorly. The external occipital protuberance should be exposed medially and the asterion laterally to allow sufficient exposure for subperiosteal dissection. tailed real-time information about the heart, great vessels, There is no need to expose the foramen magnum region. and every air bubble entering the blood circulation during surgery. Thus, it is possible to detect air inflow at an early Craniotomy. Three bur holes are then made. The first stage and prevent any complications with appropriate ma- is placed in line with the skin incision and 2 cm above the neuvers (Fig. 8A and B). superior nuchal line, as this is the most superior aspect With the patient in the supine position, the skull of the exposure. The second hole is placed just lateral to clamp of the Mayfield-Kees 3-point fixation device is the external occipital protuberance right over the trans- applied to the head. One skull pin is fixed to the mas- verse sinus just lateral to the confluence of sinuses, and toid process of the contralateral side, and 2 pins are fixed the third hole is placed on the asterion (corresponding ap- to the ipsilateral frontal and parietal regions. While the proximately just medial to the junction of the transverse surgeon holds the patient’s head securely, silicone cush- and sigmoid sinuses). A dural dissector is then passed to ions and large soft pillows are placed to position the pa- separate the dura and the transverse sinus from the bone, tient’s legs approximately 90° to the torso with the knees and the bone flap is turned with the craniotome, which flexed 90°. The seat section of the operating table should extends one-third above the transverse sinus and two- be parallel to the ground and the back section tilted up thirds below the transverse sinus. Placing the craniotomy approximately 25°. This smaller degree of tilt helps pre- well above the transverse sinus helps in 2 ways: the ex- vent complications associated with air embolism and pre- act location of the transverse sinus varies, and the transverse sinus sometimes needs to be pulled up depending serves the surgeon’s comfort when the operating table is on the tentorial angle. We try not to expose the mastoid elevated and the surgeon’s armrest is used. This modifi- air cells and, irrespective of opening air cells, we apply cation recreates the semisitting position. After the patient bone wax to the bone edges to prevent a CSF leak. With is in the desired position, the Mayfield crossbar adaptor this exposure, we usually have approximately 6 cm of is fitted to the accessory rail of the back section of the bone exposed in the mediolateral plane and 5 cm in the operating table to allow changes in the degree of eleva- superoinferior plane. This space is necessary to achieve tion of the back without having to go under the drapes to a wide mediolateral corridor, which allows excellent vi- disconnect the Mayfield system during surgery. The pa- sualization and enough room for maneuvering during the tient’s head is then fixed in a neutral-straight position with operation (Fig. 8C). moderate flexion. Extreme flexion of the head must be avoided, especially in elderly patients. When positioning Dural Opening. At this stage, the operating micro- the patient’s head, the surgeon flexes the neck as neces- scope is introduced. It is critical to mention that we use a sary to increase the intracranial venous pressure during surgical microscope with a 300-mm objective lens with-

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Fig. 2. Four different formalin-fixed cadaveric brain specimens are shown in various angles. By using the fiber dissection technique, some of the significant anatomical structures of the temporal lobe and their relations with the surrounding formations are demonstrated. A: Lateral view of the left cerebral hemisphere. The superior longitudinal fasciculus (slf), uncinate fasciculus (uf), occipitofrontal fasciculus (of), sagittal stratum (sas), corona radiata (cr), and putamen (pu) are revealed. B: Left superolateral view of a cadaver brain after axial section through the foramen of Monro showing the lateral extensions of fibers of the anterior commissure (ac) to the temporal pole (tp) (anteriorly) and the sagittal stratum (sas) (posteriorly). C: The inferior view of the left hemisphere in a cadaver brain specimen shows the inferior thalamic peduncle (itp) and the posterior thalamic peduncle (ptp), which includes the optic radiation at the roof of the temporal horn. D: In the anterior view of a coronal section of a cadaveric brain at the level of the foramen of Monro, the right internal capsula (ic) is revealed after dissection of the putamen (pu), the globus pallidus (gp), and caudate nucleus (cn) on the same side. Dissecting the fibers at the right side of the pons (po) reveals the transverse pontine fibers (trpf) and the frontopontine fibers (fpf). Abbreviations with white letters denote the sulci and fissures. alic = anterior limb of the internal capsule; alv = atrial portion of the lateral ventricle; ap = ansa peduncularis; aps = anterior periinsular sulcus; c = claustrum; cc = corpus callosum; cc-s = splenium of the corpus callosum; cer = cerebellum; cos = collateral sulcus; cp = cerebral peduncle; f = fornix; f-c = column of the fornix; f-cr = crus of the fornix; fg = fusiform gyrus; fma = forceps major (radiation of the corpus callosum); gic = genu of the internal capsule; h = hippocampus; i = insula; ips = inferior periinsular sulcus; lgb = lateral geniculate body; mb = mamillary body; mgb = medial geniculate body; ocp = occipital pole; ot = optic tract; pg-a = anterior portion of the parahippocampal gyrus; plic = posterior limb of the internal capsule; pt = pulvinar of the thalamus; sf = sylvian fissure; slic = sublentiform portion of the internal capsule; sn = substantia nigra; sps = superior periinsular sulcus; th = thalamus; T1 = superior temporal gyrus; T2 = middle temporal gyrus; T3 = inferior temporal gyrus; I = olfactory nerve; II = optic nerve. out autofocus and zoom functions (OPMI 1 FC, Zeiss). transverse sinus. This opening is parallel to the transverse The counterweight-balanced microscope stand is con- sinus in the center of the exposure. At the ends of the trolled with a pistol-grip hand switch and mouth switch exposure, the dural incision curves up closer to the trans- (Contraves).62 We make 2 openings in the dura. The first verse sinus. It is important to open the dura wide from is a transverse opening about 15 mm long placed right the midline to the lateral aspect of the opening to create over the lower aspect of the craniotomy to access the cis- a wide mediolateral corridor. This corridor allows visual- terna magna. Cerebrospinal fluid is then released to relax ization of the supracerebellar space to work between the the posterior fossa and allow the supracerebellar infraten- tentorial draining veins without sacrificing them. This torial corridor to open. A cottonoid is left here, allowing wide corridor also allows visualization of the medial tem- access to the cisterna magna to release more CSF as nec- poral structures beyond the “napkin ring” formed by the essary. The transverse and occipital sinuses should not midbrain medially and the petrous ridge laterally. be opened. Before the second incision, a micro-Doppler When the surgeon approaches the transverse sinus probe (Mizuho America, Inc.) is used to confirm the exact during the second dural opening, a small, inadvertent location and extension of the transverse sinus. A curvilin- opening may appear in the transverse sinus, which might ear opening in the dura is made about 15 mm below the lead to air inflow to the blood circulation. Thus, we alert

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Fig. 3. A: In a formalin-fixed cadaveric brain specimen, the left hemisphere was almost totally dissected away by using the fiber dissection technique; the MTR and all portions of the internal capsule were preserved. B: Further dissection was done, and the left-sided internal capsule, diencephalon, brainstem, and cerebellum (cer) were also removed. The left MTR has been preserved. Abbreviations with white letters denote the sulci and fissures. ab = amygdaloid body; ac = anterior commissure; ahi = alveus of the hippocampus; alic = anterior limb of the internal capsule; alv = atrial portion of the lateral ventricle; ap = ansa peduncularis; cc-b = body of the corpus callosum; cc-s = splenium of the corpus callosum; cig = cingulate gyrus; cos = collateral sulcus; cv = cerebellar vermis; f-b = body of the fornix; f-c = column of the fornix; f-cr = crus of the fornix; fi = fimbria; fm = foramen of Monro; fma = forceps major (radiation of the corpus callosum); lg = lingual gyrus; m = midbrain; pg = parahippocampal gyrus; plic = posterior limb of the internal capsule; po = pons; sa = subcallosal area; slic = sublentiform portion of the internal capsule; sp = septum pellucidum; th = thalamus. our anesthesia team to watch for that phenomenon. After cistern all the way to the lateral aspect of the ambient the dural opening, adhesions of arachnoid villi are com- cistern. monly found from the most posterosuperior aspect of During dissection of the arachnoid to uncover am- the cerebellum to the dura. We release these arachnoid bient and quadrigeminal cisterns, care must be taken villi adhesions, a maneuver that opens the supracerebellar to identify the trochlear nerve. The trochlear nerve ad- operative corridor. After it is opened, the dura is placed vances between the posterior cerebral artery and superior over the transverse sinus. At this point, the patency of the cerebellar artery after emerging from the dorsal aspect of transverse sinus is checked again with a micro-Doppler the crus cerebri. Before tentorial opening, the trochlear probe to make sure that tenting of the dura did not com- nerve should be followed until it pierces the tentorium. promise flow. Although the trochlear nerve remains below the trajec- Exploring the Supracerebellar Space. The superior (tentorial) surface of the cerebellum is dissected from the tentorium (Fig. 8D). The supracerebellar space is then explored, and special attention is paid to understand any venous variations. Generally, 1 small vein in the supracerebellar paramedian region drains to the tentorium. In our first 4 patients (26.7%), we sacrificed these veins to allow a sufficient working space. Although there were no clinical or radiological problems with this sacrifice, in the remaining 11 patients (73.3%) we preserved these veins even if there were multiple ones. We were able to mobilize the veins and modify the tentorial incision according to the venous variations to open enough space. The surgeon must not sacrifice the lateral petrosal vein or the tentorial veins around the midline, which are the main veins draining the posterior fossa. Dissection is carried forward to open the posterior Fig. 4. The left paramedian sagittal section through the hippocampal aspect of the quadrigeminal cistern and the ambient cis- formation of a formalin-fixed cadaveric head is shown. The figure shows the paramedian supracerebellar transtentorial approach for selective tern and to identify the superior cerebellar artery, the amygdalohippocampectomy. The arrow indicates the route of the surgi- trochlear nerve, the pineal gland, the vein of Galen, and cal approach. Abbreviations with white letters denote sulci and fissures. the basal vein of Rosenthal. The inferior colliculus, the ab = amygdaloid body; ac = anterior commissure; cer = cerebellum; most important landmark during surgery, is identified. To chp = choroid plexus; cos = collateral sulcus; cr = corona radiata; hi = take advantage of the mediolateral corridor, the arach- hippocampus; ocp = occipital pole; pu = putamen; slic = sublentiform noid should be opened medially from the quadrigeminal portion of the internal capsule; te = tentorium; trs = transverse sinus.

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Fig. 5. A: The superior view of a cadaver brain reveals the MTR on both sides to show their relationship to the ventricles and the surrounding vascular structures. The dotted lines designate the portions of the hippocampal formation from the superior view that correspond to portions of the MTR. B: After resection of the remaining temporal lobe, the middle fossa is revealed. The tentorium was dissected away to demonstrate how the middle fossa relates to the cerebellum, midbrain, and anterior fossa. The head of the hippocampus sits on the lateral wall of the cavernous sinus at the medial border of the middle fossa. A1 = precommunicating (first) segment of the anterior cerebral artery; ab = amygdaloid body; af = anterior fossa; alv = atrial portion of the lateral ventricle; ce = collateral eminence; cer = cerebellum; cp = cerebral peduncle; fi = fimbria; hi-b = body of the hippocampus; hi-h = head of the hippocampus; hi-t = tail of the hippocampus; ica = internal carotid artery; ico = inferior colliculus; M1 = sphenoidal (first) segment of the middle cerebral artery; mf = middle fossa; ot = optic tract; P2 = second (ambient) segment of the posterior cerebral artery; pc = piriform cortex; pr = petrous ridge; ps = pituitary stalk; sca = superior cerebellar artery; sco = superior colliculus; sr = sphenoidal ridge; sts = straight sinus; su = subiculum; te = tentorium; tee = tentorial edge; tp = temporal pole; u = uncus; vg = vein of Galen; II = optic nerve; III = oculomotor nerve; IV = trochlear nerve; V = trigeminal nerve; VI = abducent nerve; VII = facial nerve; VIII = vestibulocochlear nerve. tory of the PST approach, its presence should be always retaining retractor is never used in any part of the surgery. kept in mind during the rest of the surgery. Next, the posterior leaflet is pulled up in a similar fashion. Tack-up sutures are then placed to help elevate the upper Tentorial Opening. After the trochlear nerve is clearly leaflet of the tentorium to displace the transverse sinus. identified, the tentorium is coagulated and incised. An in- This maneuver opens more space for visualization and cision is made about 2–3 cm posterolateral from the pos- manipulation. In some patients, we modify this tentorial terior portion of the tentorial incisura, right in the center incision because of venous variations. We leave a cuff of of the exposure. A cottonoid is placed above this open- dura around the tentorial draining vein; hence, we are ing to protect the supratentorial structures. The incision able to preserve the vein in most patients (Fig. 8E). is then gently carried toward the tentorial hiatus to the After this maneuver, various anatomical structures lateral and posterior aspects of the quadrigeminal cistern. can be identified as landmarks to help with orientation The incision is then extended from the starting point an- during the rest of the surgery. The quadrigeminal and teriorly to the midpoint of the petrous ridge. After the posterior portions of the ambient cisterns should be well tentorium has been cut in this fashion, the anterior leaflet opened to create a large working space. The inferior col- of the tentorium is retracted downward with 3 sutures, liculus, the trochlear nerve, the main stem and branches with Dandy forceps hanging from the tails of the sutures. of the posterior cerebral and superior cerebellar arteries, To prevent the sutures from biting into the cerebellum, the galenic venous system with the basal vein of Rosen- the tentorial surface of the cerebellum is padded with cot- thal, and the superior petrosal vein should be explored. ton patties. The cerebellum hangs by gravity, and the self- Large portions of the MTR and fusiform gyrus become

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Fig. 6. Left: The posteroinferior view of a cadaver brain after the cerebellum is removed. The left-sided tentorium has been removed (the tentorial edge is preserved) to disclose the inferior view of the MTR as well as the fusiform gyrus (fg). The dotted line indicates the border between the middle and posterior portions of the MTR at the level of the inferior colliculus. The anterior portion of the MTR is hidden in the middle fossa. Right: Inferior view of the same hemisphere. The gray area shows the maximum exposure after total tentorial resection. The portions of the MTR are separated by dotted lines. Abbreviations with white letters denote the sulci and fissures. A = anterior portion of the mediotemporal region; atbv = anterior temporal basal vein; cas-a = anterior calcarine sulcus; cc-s = splenium of the corpus callosum; cos = collateral sulcus; cp = cerebral peduncle; csi = confluence of sinuses; fg = fusiform gyrus; ico = inferior colliculus; ist = isthmus cinguli; lg = lingual gyrus; M = middle portion of the mediotemporal region; mcp = middle cerebellar peduncle; ots = occipitotemporal sulcus; P = posterior portion of the mediotemporal region; P2 = second (ambient) segment of the posterior cerebral artery; P3 = third segment of the posterior cerebral artery; P4 = fourth segment of the posterior cerebral artery; pb = pineal body; pc = piriform cortex; pr = petrous ridge; ptbv = temporal basal vein; rs = rhinal sulcus; scp = superior cerebellar peduncle; sts = straight sinus; te = tentorium; tee = tentorial edge; tg = transverse insular gyrus; tp = temporal pole; trs = transverse sinus; T3 = inferior temporal gyrus; u = uncus; vg = vein of Galen; 1 = inferior anterior temporal artery; 2 = inferior middle temporal artery; 3 = inferior posterior temporal artery; 4 = inferior temporooccipital artery; I = olfactory nerve; IV = trochlear nerve. visible. The collateral sulcus, which separates the para- of the surgery. The collateral sulcus, which marks the lat- hippocampal gyrus and the fusiform (lateral temporo- eral limit of resection, is identified next. The choroidal occipital) gyrus, should be identified. In patients with fissure and midbrain form the medial limit of resection. hippocampal sclerosis, because of atrophic mediobasal A perpendicular posterior parahippocampal incision structures, the uncus and third cranial nerve may be dis- is made with bipolar forceps at the level of the inferior closed at this step. In patients with tumors, however, it colliculus, which is limited by the collateral sulcus later- may be dangerous to try to expose these structures be- ally. Subpial dissection is done, taking care to preserve cause of the voluminous tumor tissue in this step. These the major inferior temporal arteries originating from the various landmarks guide the surgeon during the rest of P3 and P2 segments of the posterior cerebral artery. Next, surgery; this is the great advantage of the PST approach. subpial resection of the posterior aspect of the subiculum is done and is carried forward to the uncus medially. Removal of the Parahippocampal Gyrus, Hippocam- The hippocampal arteries originating from the P3 and P2 pus, and Amygdala. To remove these structures, intraoper- segments of the posterior cerebral artery are identified, ative surface EEG is done first and then a depth electrode coagulated, and cut. The uncal arteries are then identi- is passed into the hippocampus and the parahippocampal fied, coagulated, and cut. Subpial dissection is continued gyrus. Recordings are made in all cases. In our experi- laterally to identify the collateral sulcus and, with gentle ence, contrary to that of patients with hippocampal scle- dissection of the inferior aspect of the parahippocampal rosis, we did not find epileptic EEG activity within the gyrus just medial to the collateral sulcus, the dentate gy- tumor. rus is identified by its distinct grayish color. The alveus The inferior colliculus is the main landmark for the is then dissected and the posterior aspect of the temporal starting point of the parahippocampal gyrus resection. In horn, near the atrium, is entered. patients with MTE, the inferior colliculus is also the pos- Unique to this exposure is that the roof of the tem- terior limit of resection because of the need to preserve poral horn is in the line of sight. The choroidal fissure the anterior extension of the visual cortex. In patients with is identified in the temporal horn of the lateral ventricle tumors, however, if the lesion extends behind this point, and dissection is carried forward to the tip of the tempo- then the tumor is dissected anterior to this point initially. ral horn. Dissection is done between the fimbria and the We then reach and resect the posterior portion at the end choroid plexus. At this point, the body and most of the

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Fig. 7. Inferior view of the MTR of a cadaveric specimen. The brainstem has been dissected away at the level between the superior (sco) and inferior colliculi. The brain is upside down so as to simulate the surgical perspective. A: The right-sided cortex of the parahippocampal gyrus is removed to expose the cingulum (cin). On the left side, the portions of the MTR (inferior view) are designated by dotted lines. B: Further dissection of the same cadaver revealed the amygdala (ab), the roof of the temporal horn (rth), and the deep portions of the Ammon Horn (ah). Abbreviations with white letters denote sulci and fissures. A = anterior portion of the mediotemporal region; ahi = alveus of the hippocampus; aps = anterior periinsular sulcus; cas-a = anterior calcarine sulcus; cc-s = splenium of the corpus callosum; cos = collateral sulcus; cp = cerebral peduncle; f-cr = crus of the fornix; fag = fasciolar gyrus; fg = fusiform gyrus; fma = forceps major (radiation of the corpus callosum); ist = isthmus cinguli; lg = lingual gyrus; lg-a = anterior lingual gyrus; M = middle portion of the mediotemporal region; mb = mammillary body; mgb = medial geniculate body; ot = optic tract; P = posterior portion of the mediotemporal region; pc = piriform cortex; pt = pulvinar of the thalamus; rs = rhinal sulcus; sco = superior colliculus; tg = transverse insular gyrus; tp = temporal pole; u = uncus; I = olfactory nerve; II = optic nerve. head of the hippocampus are ready to be delivered with- cistern subpially and the point where the anterior cho- out damage, allowing for detailed pathological examina- roidal artery departs the internal carotid artery. At this tion of the hippocampus in patients with MTE (Fig. 8F). point, the high-definition neuroendoscope (Aesculap) is In patients with tumors, the hippocampus and parahip- introduced to visualize the inferior and anterior aspects pocampal gyrus are removed in piecemeal fashion with of the parahippocampal gyrus. This area is not well seen bipolar forceps, suction tubes, and ultrasonic surgical as- through the microscope, as it is hidden from view by the piration. petrous ridge. This phenomenon is truer in patients with The remainder of the head of the hippocampus, the tumors than in those with MTE, in whom we try selective uncus, and the amygdala are then resected, taking care to amygdalohippocampectomy. stop at the point where the lateral wall meets the roof of The technique of placing a cotton ball below the the temporal horn near the collateral eminence. Resec- parahippocampal gyrus brings it into view; therefore, tion of the amygdala is begun at the junction of the amyg- resecting the most anterior and inferior aspects of the dala and the tail of the caudate nucleus; the amygdala is parahippocampal gyrus becomes possible. With the identified clearly by its nutmeg color under the ependy- high-definition neuroendoscope and a suction tube with mal layer. This technique prevents injury to the visual a curved tip, we continue to resect the remaining tissue in fibers within the Meyer loop. Care must be taken during this region, attaining hemostasis. The internal carotid ar- subpial resection of the medial aspect of the amygdala tery with its perforators, the anterior choroidal artery, the as both the optic tract and the anterior choroidal artery posterior communicating artery, the third and fourth cra- are at risk. We prefer to use only gentle suction at this nial nerves, the roof of the temporal horn with the choroid stage of the procedure, when we can identify the crural plexus and the tail of the caudate nucleus, the P2 and P3

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Fig. 8. A: Lateral view of the patient in the semisitting position. The seat section (ss) of the operating table is parallel to the ground and the back section (bs) is tilted up approximately 25°. The head is flexed in the neutral position without any rotation or tilt. The back section’s accessory rail is used for the Mayfield crossbar adaptor (cba). With this modification, the position of the back section can be changed easily without having to go under the drapes to disconnect the Mayfield system from the operating table adapter during surgery. B: A vertical linear incision, approximately 12 cm long, is made through the midpoint between the mastoid process and the external occipital protuberance (eop). One-third of the incision is above the transverse sinus while two- thirds is below. During the operation, any possible air embolism is monitored using the TEE monitor (tee-m). C: The anatomical landmarks necessary to localize the craniotomy and the operative field after the dural opening are shown. The vertical dashed line indicates the skin incision. Note the small dural opening just above the inferior border of the craniotomy, which is made to reach the cisterna magna to release CSF. The ideal spots for the 3 bur holes are demarcated. The first bur hole is placed 2 cm above the superior nuchal line, the second bur hole is placed just lateral to the external occipital protuberance right over the transverse sinus, and the third bur hole is placed on the asterion just medial to the junction of the transverse and sigmoid sinuses. Care must be taken not to open the mastoid air cells to prevent a CSF leak. The asterisk indicates the tentorial incision. D: Illustration showing the inferior view of the middle portion of the left MTR (M) and the midbrain after the tentorial opening. The exposure is wide enough without retraction of the cerebellum. The anterior leaflet of the tentorium is retracted downward with 3 holding sutures and Dandy forceps, and the posterior leaflet is retracted upward. E: The illustration of the surgical field after the selective removal of the left amygdala, hippocampus, and parahippocampal gyrus is shown. F: The head (hi-h) and body (hi-b) of the hippocampal formation can be removed in 1 piece through the PST approach. These portions correspond to the anterior and middle portions of the MTR. G: The endoscopic view of the surgical field after the selective removal of the left amygdala, hippocampus, and parahippocampal gyrus is shown. The asterisk indicates the bed of the amygdala. (See Video 1.) H: The surgeon’s position during excision of the amygdala; the foremost point of the surgical field, is demonstrated. With the small head of the surgical microscope (without autofocus and zoom functions) and correct instrumentation, (continued)→

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Fig. 8. (continued) the surgeon does not need to stretch his or her arms even when reaching the foremost point of this approach, which is the amygdala. A mouth switch and armrest are also useful. Abbreviations with white letters denote sulci and fissures. A1 = precommunicating (first) segment of the anterior cerebral artery; bu = base unit; bvr = basal vein of Rosenthal; cer = cerebellum; chp = choroid plexus; cos = collateral gyrus; cp = cerebral peduncle; eoc = external occipital crest; fg = fusiform gyrus; ICA = internal carotid artery; lgb = lateral geniculate body; M1 = sphenoidal (first) segment of the middle cerebral artery; M = middle portion of the mediotemporal region; P2 = second segment of the posterior cerebral artery; P3 = third segment of posterior cerebral artery; pt = pulvinar of the thalamus; rth = roof of the temporal horn; scl = skull clamp; swa = Swivel adaptor; te = tentorium; tee-p = probe of the TEE; trs = transverse sinus; zpr = zygomatic process; 3 = inferior posterior temporal artery; 4 = inferior temporooccipital artery; II = optic nerve; III = oculomotor nerve; IV = trochlear nerve. segments of the posterior cerebral artery with their main Minimal air inflow in a short period of time was detected branches, the superior cerebellar artery, and the basal by TEE in 6 patients (40%). No airflow was detected in vein of Rosenthal should be seen (Fig. 8G, Video 1). the remaining 9 patients (60%). None of the patients had Video 1. High-definition endoscopic recording demon- any clinical sign of air embolism, such as a sudden de- strating the surgical field after the selective removal of the left crease in end-tidal CO2, desaturation, a decrease in arteri- amygdala, hippocampus and parahippocampal gyrus using a al blood pressure, ventricular dysrhythmia, or an increase left-sided PST approach. The asterisk indicates the bed of the in central venous pressure. amygdala (same case as in Fig. 8G). cer = cerebellum; cp = Postoperatively, imaging studies revealed that the le- cerebral peduncle; ICA = internal carotid artery; lgb = lateral sions had been totally resected macroscopically (Figs. 9 geniculate body; M1 = first segment of middle cerebral artery; P2 = second segment of the posterior cerebral artery; P3 = third and 10). The postoperative follow-up period ranged from segment of posterior cerebral artery; rth = roof of the temporal 10 to 39 months (mean 21.4 months) (Table 1). Patients horn; te = tentorium; III = oculomotor nerve. Click here to with high-grade tumors (Cases 1, 2, 6, and 11) received view with Windows Media Player. Click here to view with adjuvant radiotherapy and/or chemotherapy in the post- Quicktime. operative period. Three of these patients (Cases 1, 2, and A critical factor in the success of the PST approach is 6), however, underwent repeated surgery 13, 28, and 9 to have a small optical head for the surgical microscope. months after the first surgery, respectively, because of re- For the surgeon to work in the depth of a small space with current tumors. One of these patients (Case 1) died due both hands continuously, without stretching his or her to recurrence 30 months after the first surgery. In Case 3, arms, the use of a surgical microscope without autofocus the tumor extended to the posterior and middle portions and zoom functions that can be controlled with a mouth of the cingulate gyrus; therefore, we combined the PST switch is crucial. The hydraulic armrest is also important approach with the posterior interhemispheric approach equipment for the surgeon’s comfort (Fig. 8H). in the same session with a modified craniotomy. In all patients with hippocampal sclerosis, antiepileptic drugs Closure. After hemostasis is achieved, the tentorial could be gradually decreased to 1 drug, and there had sutures are released and reapproximated to reconstruct been no seizure activity at the time of this writing. The the anatomical position of the tentorium. The small in- postoperative visual field remains intact in all patients ferior and large superior incisions of the dura of the pos- with MTE. terior fossa are closed watertight and the bone flap is Detailed information regarding the characteristics of replaced with skull-fixation devices. The occipital belly patients and their surgical results and outcomes are sum- of the occipitofrontal muscle is reapproximated and the marized in Table 1. suboccipital muscles are brought together with 0 Vicryl. The wound is then closed. Illustrative Cases Patients are extubated in the operating room at the Case 2 end of the procedure, and they are then transferred to the ICU until the next morning. In the ICU, the patient is kept This 63-year-old woman experienced epileptic sei- with the head elevated 30°. Postoperative MR imaging is zures 1 year prior to her presentation at another institu- done the morning after surgery. A detailed MR imaging tion. An MR imaging study disclosed a right-sided MTR study with fiber tractography is repeated routinely 2–3 tumor, and the patient was subsequently observed. Be- months after surgery. cause of the growth pattern of the tumor during the obser- vation period, the patient was referred to our institution. Surgical Results and Outcome The MR images disclosed a tumor at the MTR extending The PST approach provided excellent exposure and from the piriform cortex to the isthmus cinguli, which safe resection of various lesions in the MTR and/or fu- enhanced minimally after contrast injection (Fig. 9A). A siform gyrus in 9 patients. This approach also ensured preoperative study of the visual field showed peripheral selective removal of the anterior two-thirds of the para- narrowing with left-sided homonym hemianopia. Surgery hippocampal gyrus and hippocampus, and the amygdala was recommended, and gross-total resection of the tumor in 6 patients with MTE due to hippocampal sclerosis. The was achieved in 1 session by using a right-sided PST ap- mean operation time was 4 hours 55 minutes (range 3 proach (Fig. 9B). The patient’s postoperative course was hours 20 minutes to 7 hours 10 minutes), and the mean uneventful, and the histopathological diagnosis yielded time spent under the microscope was 2 hours 8 minutes a glioblastoma (WHO Grade IV). The patient received (range 1 hour 33 minutes to 3 hours 10 minutes). There adjuvant radiotherapy and chemotherapy in the postop- were no intraoperative or postoperative complications. erative period. At the 3-month follow-up, MR imaging

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Fig. 9. Case 2. A: Preoperative axial FLAIR and T1-weighted postcontrast MR imaging sections in coronal and sagittal planes at different levels showing the MTR lesion extending from the piriform cortex to the isthmus cinguli. The early diagnosis was a neuroepithelial tumor. B: Endoscopic view of the surgical field after resection of the large, right-sided MTR tumor. The internal carotid artery (ICA), anterior choroidal artery (ach), choroid plexus (chp), posterior communicating artery (pco), third cranial nerve (III), and cerebral peduncle (cp) are shown. C: Three months after surgery, MR imaging studies show no residual or recurrent tumor and the neighboring structures have been preserved. L = left; rth = roof of the temporal horn. disclosed no residual or recurrent tumor (Fig. 9C). The intact. The lesion was totally removed through a left PST patient underwent a second surgery 18 months afterward approach (Fig. 10B). Intraoperative electrocorticography for recurrent tumor. was done with a strip electrode placed onto the parahippocampal gyrus, and a depth electrode was placed into Case 4 the hippocampal formation in the sagittal plane. Epilepti- This 11-year-old boy was admitted to our clinic with form activity was detected in the hippocampal formation. seizures that started 20 days before admission. During Therefore, we carried out a selective amygdalohippocam- the seizures, he asked meaningless questions but never pectomy. The patient’s postoperative period was unevent- remembered this event. He had a history of afebrile con- ful, and the histopathological diagnosis was pleomorphic vulsions at the age of 5 years. Magnetic resonance imag- xanthoastrocytoma (WHO Grade II). Histopathologi- ing disclosed a left-sided posterior fusiform gyrus lesion cal tests of the hippocampal specimen revealed disper- (Fig. 10A). During video-EEG monitoring, the ictal and sion and neuronal loss at the CA1 to CA3 regions of the interictal findings showed that the clinical and electro- Ammon horn. The 2-month postoperative MR imaging physiological seizures originated in the left anterior tem- studies demonstrated radical resection of the tumor with poral lobe. He had bitemporal inferior quadrantanopia selective removal of the amygdala, the hippocampus, and (pie-on-the-floor), but he was otherwise neurologically the parahippocampal gyrus. No adjuvant therapy was

Fig. 10. Case 4. A: Axial FLAIR and T1-weighted postcontrast MR imaging studies obtained in coronal and sagittal planes at different levels showing a left-sided (L) lesion located in the posterior portion of the fusiform gyrus (lateral temporooccipital gyrus) and the MTR, which minimally enhances after contrast injection. B: Three months after surgery, MR imaging studies show the resection of the fusiform gyrus and selective amygdalohippocampectomy for seizure control through the PST approach.

J Neurosurg / Volume 116 / April 2012 785 Unauthenticated | Downloaded 10/09/21 06:20 AM UTC U. Türe et al. recommended. The patient has not had a seizure since and hippocampus was followed by some modifications the surgery. through the temporal gyri and sulci.15,32 However, all of these approaches have limitations in exposing the entire Case 5 length of the MTR and necessitate more or less temporal This 24-year-old woman was admitted with a 17-year lobe retraction or incisions, which endanger the optic ra- history of intractable MTE. She had automotor seizures diation. without consciousness 2–3 times a week while she was The posterior interhemispheric approach is very × useful for lesions located in the posterior portion of the taking levetiracetam (2 1500 mg per day, lamotrigine 62 (2 × 200 mg per day), and topiramate (2 × 100 mg per MTR. Other alternatives for such lesions are the supratentorial infraoccipital approach46 and the lateral occipi- day). Ictal and interictal EEG findings revealed that the 57 seizures originated in the left frontotemporal region. tal subtemporal approach. These latter two approaches The MR imaging findings disclosed left-sided hippo- were also used to reach the middle portion of the MTR; campal sclerosis, especially in the posterior part, with however, extensive retraction of the occipital lobe is nec- hyperintensity on T2-weighted images and volume loss essary and endangers the occipital basal and posterior on T1-weighted images (Fig. 11A). On PET-CT scan- temporal veins. ning, hypometabolism was located especially around the The supracerebellar transtentorial approach was de- left hippocampus, whereas the neocortical regions were veloped by Yaşargil to remove posterior hippocampal cavernous malformations without injuring the optic ra- spared. With successful experience from previous cases 56 and especially because the patient had posteriorly located diation. Later, he used this approach in 2 patients with posterior parahippocampal dysplasia and 1 patient with hippocampal sclerosis, we decided to use the PST ap- 62 proach for selective amygdalohippocampectomy. An in- an oligodendroglioma. The supracerebellar transtentorial approach was revitalized by Yonekawa and col- traoperative strip electrode was placed on the left MTR, 66 and a depth electrode in the left hippocampus verified leagues to approach the posterior portion of the MTR. abnormal electrical activity. Selective removal of the left De Oliveira (E. de Oliveira, personal communication, 2008) and Moftakhar et al.28 also used this approach for parahippocampal gyrus, the hippocampus, and the amyg- 64 dala was done, and the postoperative course of the patient the posterior portion of the MTR. Yaşargil developed was uneventful. The postoperative MR images obtained the idea of a PST approach for selective amygdalohip- at 2 months showed selective removal of the amygdala, pocampectomy. His main concern was the possible diffi- hippocampus, and parahippocampal gyrus on the left side culty of removing the amygdala and piriform cortex using (Fig. 11B). Postoperative fiber tractography also showed the PST approach. preservation of the major fiber tracts of the left temporal Since the first such posterior procedure was performed in lobe (Fig. 11C), and a visual field study showed that the 1968, I am continually reflecting on the issue and suggesting visual field remained intact (Fig. 11D). The patient has not to colleagues that this approach could be applied routinely for selective [amygdalohippocampectomy]. It would be quite dif- suffered a seizure or aura during the postoperative period ficult to access the amygdala and temporal pole areas along (29 months) with lamotrigine (2 × 100 mg per day). the semicircular trajectory around the cerebral peduncle. Nevertheless, if experts in the field of epileptology could determine with certainty that only the hippocampus and parahip- Discussion pocampal gyrus should be removed, I would not hesitate to use The MTR is deeply located and extended, and there the supracerebellar approach.64 remain some controversies regarding surgical approaches Following extensive cadaveric studies, we found that to it. The main reason for this controversy is that the MTR it is possible to remove the amygdala and piriform cortex is such a long structure anteroposteriorly and is curved using the PST approach. However, we did not submit this around the midbrain, which further complicates the abil- study for publication until we had the experience of sur- ity to reach the entirety of its length in a single surgical gical application, and we had to wait 10 years to perform session. The various approaches for resecting lesions of the first surgery. This delay was due to the need to un- the MTR can be classified as anterior, lateral (subtempo- derstand in greater detail the anatomy of the fiber system ral or transcortical), and posterior.52 Some authors prefer and the microsurgical anatomy of the MTR region and to carry out an anterior temporal lobectomy or antero- to gain enough experience with tumor and epilepsy cases medial temporal lobectomy to approach lesions located involving the MTR region. We first used this approach in the MTR.9,47,48 Yaşargil introduced the pterional-trans- to remove a tumor in the entire length of the MTR and sylvian approach and demonstrated that it is suitable for then applied it in patients with MTE due to hippocampal removing the anterior two-thirds of the MTR in patients sclerosis. with MTE due to hippocampal sclerosis.60,63 Its usage also The PST approach offers several advantages for se- was shown to be appropriate for many patients with large lectively removing lesions involving various portions of tumors involving the entire length of the MTR.62 the MTR. In lesions involving the entire length of the Lateral approaches are other alternatives to reaching MTR, the senior author (U.T.) had previously performed the MTR and may be divided into subtemporal and trans- a second procedure using the posterior interhemispher- cortical approaches. The subtemporal approaches include ic approach if there was residual tumor in the posterior the subtemporal,12,37 zygomatic,45 petrosal,52 and transoc- portion of the MTR after the pterional-transsylvian ap- cipitotemporal sulcus.5 The lateral-transcortical approach proach. However, the PST approach allows surgery to described by Niemeyer30 for resecting the amygdala be completed in a single session rather than 2, and it is

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Fig. 11. Case 5. A: Axial T2-weighted and FLAIR images obtained through the hippocampal formation and coronal inver- sion recovery sequences showing left-sided (L) hippocampal sclerosis, especially in the posterior portion. B: Postoperative axial T2-weighted (upper left) and T1-weighted (upper right), coronal T2-weighted (center row), and sagittal T1-weighted (lower row) images showing left-sided selective amygdalohippocampectomy through the PST approach. C: Postoperative fiber tractography demonstrates that the major fiber systems (in various colors) of the temporal lobe have been preserved. green = uncinate fasciculus; red = anterior commissure; blue = frontooccipital fasciculus; yellow = posterior thalamic peduncle, which includes the optic radiation. D: A postoperative visual field study demonstrated a normal visual field. the least invasive technique for removing these lesions. the middle and anterior portions of the MTR as well as Consequently, we now prefer this approach. For extended the amygdala. Table 2 summarizes the various locations tumoral lesions of the MTR, the PST approach provides of the MTR lesions and appropriate approaches to these an excellent panoramic view of the entire MTR without lesions. disturbing the neighboring structures. The PST discloses excellent landmarks during the For lesions restricted to the posterior portion of the entire surgery, which may be surprising, as the PST is not MTR, the PST is a good alternative to the posterior in- a difficult approach compared with others. Of course, it terhemispheric approach. However, exposing the superior does require a different perspective of the MTR region, part of the posterior portion may be difficult because of but this perspective can be learned through cadaver dis- obstruction by the galenic venous system. If the lesion sections and it provides excellent orientation with precise is located in the posterior and middle portions, or re- landmarks. The brainstem and major vascular structures stricted to the middle portion, the PST approach is most near the MTR are located medially and the vascular suitable. Although the PST is a posterior approach, it is course with its branches is visualized intracisternally, more useful for removing not only the posterior but also which prevents major injury to these structures during

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TABLE 2: Options for the surgical approach to various locations in the MTR

Approach Tumor Location* Pterional-Transsylvian PST Posterior Interhemispheric only in the anterior portion (A) X anterior & middle portions (A+M) X X anterior, middle, & posterior portions (A+M+P) X† X only in the middle portion (M) X middle & posterior portions (M+P) X only in the posterior portion (P) X X posterior portion & isthmus cinguli X

* The abbreviations in this column refer to locations in Fig. 1. † In some cases, the pterional-transsylvian approach may be limited for these lesions. In this situation, a second session should be done with a posterior interhemispheric approach. resection of the MTR. Neither the visual cortex nor the be due to iatrogenic damage to the temporal neocortex, optic radiation is related to the surgical trajectory, and sylvian region, or temporal pole. However, none of these therefore, the risk of injury to these structures is minimal. areas is damaged during the PST approach. This differ- Nonetheless, the surgeon should be aware of the location ence also needs further evaluation and studies in large of the lateral geniculate body when opening the choroidal series. fissure. Like many other approaches, the PST approach has For patients with MTE, the advantages may be even potential problems and difficulties. For example, the greater. This technique makes possible real selective re- semisitting position needs special attention from the neu- moval of MTR structures with a more posterior resection. rosurgeon, anesthesiologist, nurses, technicians, and the This avenue may be an advantage for more successful sei- entire operating team.14,21,62 However, modern neuroan- zure control and better neuropsychological and psycho- esthesiology with TEE and modern monitoring methods social outcome in patients with posteriorly located hip- have made this position safe. It is important to mention pocampal sclerosis. However, this difference should be that the absence of any septal defect must be confirmed verified through further studies. with TEE through the bubble test, as transthoracic echo- The long history, discussions and controversies over cardiography may miss small defects. In one of our pa- iatrogenic visual field defect after epilepsy surgery4,8,11,20, tients with MTE, a small atrial septal defect was detected 25,38–40 will come to an end with the use of the PST ap- using TEE before the patient was positioned. Therefore, proach. With precise knowledge of surgical anatomy and we used the pterional-transsylvian approach for selective microsurgical technique, surgeons have achieved excel- amygdalohippocampectomy. The semisitting position lent results with the pterional-transsylvian approach with- makes the PST approach possible. We do not recommend out visual field defects.60,63,64 The senior author (U.T.) has performing it in any other position. had the same experience when using that approach for The patient should be positioned in a stepwise fash- selective amygdalohippocampectomy.51 After using the ion, checking the hemodynamics and other parameters PST approach more frequently for tumor cases, how- and also adjusting the depth of anesthesia appropriately. ever, we are more comfortable using it for MTE cases Padded cushions should be kept under areas vulnerable as well, especially if hippocampal sclerosis is evident in to nerve compression. An experienced anesthetist and the posterior portion. The PST approach may be prefer- his or her assistant must be present throughout the en- able as it allows more posterior resection compared with tire surgical procedure. Instead of discarding this method the pterional-transsylvian approach. We must mention, because of the risk of air embolism, we can concentrate however, that removing a sclerotic hippocampus in MTE on discovering the reasons for them through the surgical cases is much easier than removing MTR tumors because area, as well as ways to prevent or minimize them while a tiny and atrophied hippocampus and an evident tempo- developing advanced techniques to determine the admis- ral horn make the surgery less complicated, and even re- sion of air. Using TEE helps detect airflow to the blood moving the hippocampus in one piece becomes possible circulation in the early stage of surgery, making it pos- for the sake of research studies. We recommend the PST sible to make necessary changes before any problems oc- approach as an alternative for those who have difficulty cur. One maneuver is to decrease the degree of elevation with selective amygdalohippocampectomy through the of the back section, which is possible only when the back pterional-transsylvian approach. section’s accessory rail is used for the Mayfield crossbar One possible criticism of the PST approach for MTE adaptor (Fig. 8A). Approximately 25° of head elevation patients is the difficulty of temporal pole resection, if it provides adequate exposure when the surgical table is is necessary. As we gained more experience using this raised as necessary. Modifying the semisitting position approach in tumor cases, however, we noticed that it is with flexion of the patient’s head and elevating the legs possible to remove the temporal pole. Recurrent seizures make the semisitting position safe. In our series, we did after anterior selective amygdalohippocampectomy may not encounter any complications related to air embolism.

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Another possible problem with having the patient in MTR tumors extending from the piriform cortex to the the semisitting position is that modern microscopes with isthmus of the cingulate gyrus in a single session with- autofocus and zoom systems are not suitable because of out disturbing neural and vascular structures. This ap- the large optical head of the surgical microscope, which proach appears to be superior to previously described ap- necessitates extreme stretching of the surgeon’s arms. proaches as well as to 2-session surgery, which combines This problem is solved by using a surgical microscope the pterional transsylvian and posterior interhemispheric with a small optical head controlled by a mouth switch approaches. More significantly, selective removal of the and using an armrest.62 The mouth switch frees up the amygdala and hippocampus could be done for patients surgeon’s hands, especially for the semisitting position, with MTE due to hippocampal sclerosis. This approach in which long instruments are used. This device allows is a good alternative to other amygdalohippocampectomy the surgeon to move the microscope in various directions techniques because there is no danger of injuring the ma- while working with 2 hands at great depth without inter- jor white matter structures, such as the uncinate fascicu- fering with the surgery. lus; anterior commissure, inferior and posterior thalamic The tentorial bridging veins between the superior peduncles (including the optic radiation); and the fron- surface of the cerebellum and the tentorium are a topic topontine, temporopontine, and occipitopontine fasciculi. worthy of discussion. Releasing CSF from the cisterns and Furthermore, there is no danger of damage to the super- dissecting the superior or tentorial surface of the cerebel- ficial and deep sylvian veins, the middle cerebral artery lum from the tentorium provides enough space to remove and its branches, and especially the temporal pole and the entire length of the MTR. The major components of temporal neocortex. The posterior portions of the hip- the tentorial bridging veins are located in the midline, and pocampus and parahippocampal gyrus can be removed the surgeon must certainly preserve these vermian bridg- through this approach, possibly allowing better seizure ing veins to prevent cerebellar edema, venous infarction, control, especially in patients with posterior hippocampal or hemorrhage in certain instances.22,41,49,55 Rather than sclerosis. Nonetheless, larger series and long-term follow- a midline trajectory, using the paramedian approach al- up are needed to confirm the advantages of the PST ap- lows the surgeon to preserve these major supracerebellar proach for patients with MTE. This approach also seems veins. A few and generally minor bridging veins also ex- to be the best option for removing lesions in the fusiform ist in the paramedian part of the supracerebellar tentorial gyrus, especially in the posterior portion. region. In 4 of our early patients (26.7%), we sacrificed these veins to gain enough exposure. Even though we did Appendix not see any clinical or neuroradiological signs, we tried to preserve these veins in later cases. By mobilizing the Major White Matter Fiber System of the Temporal Lobe veins and modifying the tentorial incision, depending on 1. Short association (U) fibers the variations of these veins, preservation became pos- 2. Superior longitudinal fasciculus (inferior arm) sible, and we have succeeded in preserving these veins in 3. Uncinate fasciculus the later cases (73.3%). 4. Occipitofrontal fasciculus The PST approach makes it difficult to visualize and 5. Anterior commissure reach the inferior surface of the anterior parahippocam- 6. Sublenticular part of the internal capsule pal gyrus with the microscope because of the obstruc- I. Temporopontine fibers tion created by the petrous ridge. The main reason for II. Occipitopontine fibers this difficulty is variations in the shape of the skull, which III. Inferior thalamic peduncle change the angle relationship between the transverse si- IV. Posterior thalamic peduncle (includes optic & audi- tory radiations) nus and petrous ridge. To overcome this difficulty, we 7. Tapetum placed cotton sponges in the middle fossa underneath 8. Inferior longitudinal fasciculus the parahippocampal gyrus to bring the hidden part 9. Alveus-fimbria-fornix into view, making removal of these areas possible. The 10. Cingulum (inferior arm) high-definition neuroendoscope and a suction tube with a curved tip are of great help in visualizing and resecting Disclosure residual tissue in this blind spot at the anteromedial part of the middle fossa. The authors report no conflict of interest concerning the mate- In our experience, the PST approach is very appro- rials or methods used in this study or the findings specified in this paper. priate for removing various MTR lesions with patients in Author contributions to the study and manuscript preparation the semisitting position. Releasing CSF from the cisterna include the following. Analysis and interpretation of data: U Türe, magna and the quadrigeminal and ambient cisterns pulls Harput, Kaya, H Türe. Drafting the article: U Türe, Harput, Kaya, the cerebellum downward, so no cerebellar or supratento- Baimedi, H Türe. Critically revising the article: U Türe, Harput, rial retraction is needed. The PST approach also allows Kaya, Baimedi, H Türe, Bingöl. Reviewed submitted version precise anatomical orientation, and resection of even the of manuscript: U Türe, Harput, Kaya, Baimedi, H Türe, Bingöl. anterior portion of the MTR is possible and comfortable Administrative/technical/material support: U Türe, Firat, H Türe, for the surgeon. Bingöl.

Acknowledgments Conclusions The authors thank Julie Yamamoto for editing the text and The PST approach allows for safe removal of large Peter Roth for artistic illustrations.

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