KISEP REVIEW ARTICLE J of The Kor Soc of Ster and Func Neurosur 2005;1:127-131

Temporal Lobectomy

Dae-Hee Seo, MD1, Seung-Chyul Hong, MD, PhD2 1Department of , Myongji Hospital, Kwandong University, Goyang, Korea 2Department of Neurosurgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea

The temporal lobe is an area of great importance for the surgical treatment of . (TLE) is not a single clinicopathologic entity but a number of disease variants with different anatomic, electrophysiologic, and behavioral cha- racteristics. TLE surgery has recently demonstrated a highly significant superiority over optimal medical therapy in recent studies. Technical advances such as high-resolution MRI, microneurosurgical methods, neuronavigation techniques and intraoperative MRI have improved the effectiveness of these procedures. The neurosurgeon perform the task of temporal lobe resection for epilepsy often encounters no apparent anatomic abnormalities and is expected to proceed with resection of seemingly normal tis- sue. Therefore, successful surgery within the temporal lobe requires an understanding of both structural and functional relation- ships and demands the three-dimensional grasp of anatomy. Diverse surgical approaches have been proposed to achieve better seizure outcome with fewer complications. Recently there has been a trend to remove less lateral temporal neocortex and excise more mesial structure. But, there are controversies in the matter of seizure, neuropsychological and psychosocial outcomes. Va- rious selective amygdalohippocampectomies have been increasingly used but advantages or disadvantages with respect to pos- toperative cognitive outcome are still a matter of debate. The authors review and compare the diverse surgical approaches of the temporal lobectomy briefly.

KEY WORDS: Temporal lobectomy·Surgical approach·Nonlesional temporal lobe epilepsy.

INTRODUCTION because often there is neuronal loss in the neighboring entorhinal cortex (Broadman’s area 28 in the anterior part Brain damage resulting to epileptogenesis can be indu- of the parahippocampal gyrus) and . There is ced by a variety of brain insults. Consequent reorganization vigorous debate about whether hippocampal sclerosis is of neuronal circuitries during epileptogenesis includes neu- a cause or an effect of seizures.2)3) This article focus on ronal loss, axonal and dendritic plasticity of surviving diverse surgical approaches of the temporal lobectomy neurons, neurogenesis, gliosis, and molecular reorgani- for nonlesional TLE. zation in cellular membranes and extracellular matrix (Fig. 1).1) HISTORICAL ASPECTS The growing knowledge about the neurobiology of epi- leptogenesis and progression of epilepsy may affect the In 1928, Penfield systematized temporal lobe resection timing of operation, choice of the tissue to be resected to treat uncontrolled seizure. During the following decade, and consequently improve the seizure outcome after ope- Penfield and Jasper’s conception of temporal lobe resec- ration. tion expanded to include the removal of the amygdala and The most common lesion in surgically resected tissue . In 1951, Falconer modernized Penfield’s from patients with mesial TLE is hippocampal sclerosis, operation by designing the en bloc resection of the ante- a well-described entity whose cause remains elusive. The rior temporal lobe.4) dense gliosis that accompanies the loss of neurons causes Recently there has been a trend to remove less lateral shrinkage and hardening of tissue. The term “mesial tem- temporal neocortex and excise more mesial structure. This poral sclerosis (MTS)” has also been used for this lesion, topic will be discussed in other paragraph of this review. Controversies with regard to the removal of mesial struc- Address for correspondence: Seung-Chyul Hong, MD, PhD, Department of Neurosurgery, Samsung Medical Center, Sungkyun- tures persist. According to several studies, the resection kwan University School of Medicine, 50 Ilwon-dong, Kangnam-gu, of the mesial structure is associated with a better seizure Seoul 135-710, Korea outcome. Especially, the extent of hippocampal resection Tel: +82-2-3410-3493, Fax: +82-2-3410-0048 5) E-mail: [email protected] may be associated with better outcome. Wyler et al., re-

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be blend into the pes hippocampus without a sharply de- Epileptic process marcated borders. So, the amount removed is difficult to Neuronal damage judge during surgery. Removing the amygdala by this approach is not generally a bloody procedure, but it should Latency period (epileptogenesis) be remembered that on approaching the ventricular wall, especially medially, there are veins returning from the Epilepsy amygdala within the subependymal layer and its injury may result in the torrential bleeding. The vital step in the hippocampal removal is the iden- TLE with good Drug-refractory TLE Secondary epileptogenesis (?) seizure control (mirror focus) tification of the hippocampal sulcus and Ammon’s horn arteries from the anterior and posterior choroidal arteries. Fig. 1. Symptomatic TLE typically develops in three phases：brain The sclerotic hippocampus is carefully separated from the damage → latency phase or epileptogenesis → appearance of intact pial surface. It is crucial to keep the pial boundary spontaneous seizures or epilepsy which can be easy to control or turn out to be drug-refractory over the time. †：TLE：tempo- intact. But, Hippocampal sclerosis make the hippocampus ral lobe epilepsy. hard and rubbery, necessitating a considerable degree of manipulation and the ultrasound aspirator frequently is ported that postoperative seizure control was best with unable to manage this degree of fibrosis and it may injure removal of hippocampus to the level of the superior col- the thin arachnoid layer. Pial bleeding should be carefully liculus (total hippocampectomy group had a 69%, partial controlled by bipolar cautery at a low setting. During the hippocampectomy group had a 38% of seizure-free out- hippocampal resection, care is taken to coagulate and cut come). But, the association between the extent of amy- the numerous small vessels arising from the posterior gdala resection and outcome remains to be proven. Similar communicating and posterior cerebral arteries without outcomes for a variety of anterior temporal lobectomies damaging vessels supplying the peduncle and . in which the amount of hippocampus varies from entire Usually 4 to 7 perforating arteries supplying the hippo- resection to no removal were also reported.6) Other stu- campus are encountered. The vessel injury may cause the dies have pointed out that sparing of mesial structure may traction hemiplegia or homonymous hemianopsia. It is produce a good outcome when preoperative or intraope- recommended that posterior hippocampus is usually left rative electrographic studies do not implicate mesial struc- beyond the beginning of the P3 segment of the posterior ture in the seizure focus.6)7) cerebral artery to minimize injury to the lateral geniculate body and the geniculocalcarine radiations of Meyer. Va- ANATOMICAL AND INTRAOPERATIVE riations in PHG resection usually correspond to variations CONSIDERATIONS in extent of hippocampal resection.

The boundaries of temporal lobe include the sylvian SURGICAL APPROACHES fissure superiorly and the middle fossa inferiorly and an- teriorly. The medial boundaries are formed by the insula, The goal of surgical treatment is the removal of a focal the crural and ambient cisterns. The posterior limit is de- source for intractable seizures. Several variations of tem- fined by the lateral, basal parieto-temporal lines and tem- poral lobectomy are used. These are en bloc anterior poro-occipital line. The mesial temporal structures lie temporal lobectomy, anteromedial temporal lobectomy, medial to the collateral sulcus and inferior to the temporal cortico-amygdalohippocampectomy (AH), cortico-amy- horn of the lateral ventricle and include the parahippo- gdalectomy, selective hippocampectomy, and selective AH. campal gyrus (PHG), the hippocampal formation, the un- Unfortunately, the terminology used is often misleading cus, and the amygdala. and does not describe all the resected structures. The main The amygdala is a large nuclear complex composed of variant in the different anatomic resections for TLE is the several subunits which lies anterosuperior to the pes hip- medial temporal resection and lateral temporal resection. pocampi. The identification of this nucleus, and especially Also, the surgical approach varies depending on how the its borders is not easy because the amygdala appears to hippocampal complex is approached.

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Table 1. Recent studies of seizure control outcome of selective amygdalohippocampectomy Authors & year No. of cases Approach† Outcome Follow up duration Renowden et al., 1995 017 sel-AH 47% (best*) 2 yrs (TS：10, TC：7) 88% (best & good*) Mackenzie et al., 1997 028 sel-AH 21% (Engel I) 1yr ILAE report, 199722) 341 60.1% (seizure-free) NA sel-AH 81.5% (>90% reduction) Vajkoczy et al., 1998 016 sel-AH 81% (Engel I) 1-6.8yrs (TS-transcisternal) 97% (Engel I & II) (24.6mos) Wieser et al., 2003 182 sel-AH (TS) 76.4% curative 1-24 (7.2)yrs Lutz et al., 2004 080 sel-AH Seizure-free rate Up to 7mos TS：41 73.2% TC：39 76.9% *：outcome according to the Oxford grading of seizure, best (Engel classification IA), good (Engel IB, ID, IIB, IID and IIIA), †： sel-AH： selective amygdalohippocampectomy, NA：not available, TS：transsylvian, TC：transcortical

Recently, selective procedures that resect the amygdala hippocampal gyrus are transected 3-3.5cm behind the tip and hippocampus, sparing as much lateral temporal cortex of the pes hippocampi. as possible, have been used, with good outcome (Table 1). In a standard anterior temporal lobectomy, the lateral as- Anteromedial temporal lobectomy pect of the anterior temporal lobe is resected, entering the This procedure practiced at the Yale epilepsy center temporal horn along the lateral aspect. The hippocampus minimize resection of inferior and middle temporal gyrus and amygdala are then evident as soon as the ventricle is and avoids the superior temporal gyrus. But it includes entered. Once the horn is entered, a cottonoid serves to resection of uncus, part of amygdale, and most of the protect the choroid plexus and to prevent intraventricular hippocampus and the PHG. Language mapping and elec- hematoma. The hippocampus is then resected posteriorly trocorticogram (EcoG) are not employed. This allows the at least 1.5-3.5cm from the anterior portion of the hip- procedure to be performed under general anesthesia in all pocampus. The lateral amygdala is additionally removed. cases. This procedure commenced with a cortical incision Selective AH is performed through a small lateral corti- in middle and inferior temporal gyri 3.5cm from the tem- cal window or through a subtemporal cortical resection poral tip in the nondominant hemisphere and 3cm from that enters the ventricle through the inferior temporal or the tip on the dominant temporal lobe because the likeli- fusiform gyri, or through a sylvian fissure. The term “se- hood of language cortex extending to the anterior 3cm lective” may be misleading because the amygdala is not of the middle or inferior temporal gyrus is quite low.8) Hip- removed completely. At least 10% is reported to remain pocampus is resected en bloc to the portion of the tail at medially where it abuts the striatum, anterior commissure, the posterior margin of the midbrain. The typical speci- and tail of the caudate. men is 4cm in length. The advantages of this procedure are the low morbidity associated with the limited neo- En bloc anterior temporal lobectomy cortical resection and the ability to resect completely the This technique was developed by Falconer and collea- mesial structures. gues. The hallmark of this procedure is a one stage re- moval of lateral and mesial temporal lobe structure in one The tailored temporal lobectomy piece. In en bloc anterior temporal lobectomy, an incision Approaches to resective surgery for epilepsy divide into is made in the middle temporal gyrus about 4.5cm behind two major groups. One is using anatomically uniform ope- the temporal tip in dominant hemisphere and 6cm in the ration and another is tailoring each resection to each indi- nondominant hemisphere. The sylvian fissure is opened vidual’s pathophysiology. Tailored surgery divide into two above the anterosuperior aspect of the superior temporal methods, planning the surgery using the extraoperatively gyrus exposing the limen insula. The posterior incision derived data (preoperative tailoring) and the detailed ex- is deepened and extended through the fusiform gyrus. The tent of the patient’s epileptic pathophysiology is based on temporal horn is opened and the hippocampus and para- presence of interictal epileptiform activity in the EcoG

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and the individual location of eloquent areas with intra- cular approach and 12-15mm incision (20% of total operative electrical stimulation mapping.9) There are no length of the temporal stem) at the level of the limen hard scientific data to support the belief that EcoG-gui- insula. This procedure allows more generous resection ded surgery produce superior results to standard resection, and en bloc hippocampal removal comparing to the tran- especially when dealing with MTS.5)10) Tailored, nonu- scortical approach which allows a limited exposure and niform resection is more confounding than a standard theoretically advantageous because more frontal fiber con- resection from the standpoint of the outcome evaluation. nections are divided. This procedure is technically deman- ding. Four specific problems encountered during procedure Selective AH are as follows：a) in case of large frontoorbital vein and This procedure refers to those surgical procedures whose too many major branches, the sylvian dissection must goal is to further minimize temporal neocortical resection proceed lateral to the sylvian vein, b) the variation in the (Fig. 2). It is reported that patients have better neuropsycho- form and distribution of the lateral M1 segment and dif- logical and psychosocial outcomes after AH than en bloc ficulty in finding the sufficient space to make incision, anterior temporal lobectomy but this is controversial.10)11) c) the possible variation of the vascularization, size and There are two main routes to achieving this goal. The form of medial structures, d) torrential bleeding from the first one is the transsylvian approach developed by Ya- veins returning from the amygdala. It is important to make sargil12) in the late 1970s and the other is transcortical- correct incision not too near the temporal pole. If so, the transventricular approach refined by various authors such operation becomes more difficult to perform. Wieser et as Niemeyer in 1958 (via the middle temporal gyrus； al.,16) reported that 76.4% of operations using the trans- MTG), Rougier (via superior temporal gyrus；STG),13) sylvian approach were curative after long-term follow up Olivier (via the superior temporal sulcus), Shimuzu (via in the nonlesional mesial TLE group. For a better anato- the inferior temporal gyrus after removal of the zygoma- mical orientation and sufficient intraoperative control over tic arch),14) and Park (via PHG).15) the mesial temporal lobe, transsylvian-transcisternal ap- Yasargil’s selective amygdalahippo-parahippocampec- proach was suggested by Vajkoczy.17) tomy was performed through a transsylvian-transventri- Advantages or disadvantages with respect to postope-

Transsylvian AH

Via STG

Via superior temporal sulcus

Via MTG

Fig. 2. Diverse surgical approaches for amygdalohippocampectomy. †：AH： amygdalohippocampectomy, STG：su- Via PHG Combined subtemporal & Via fusiform gyrus perior temporal gyrus, MTG：middle transventricular/transcho- roidal fissure approach temporal gyrus, PHG：parahippocam- pal gyrus.

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rative cognitive outcome are still a matter of debate. A 1266, 2003 4. Sperling MR, Schnur JK: Temporal lobectomy. Arch Neurol 59: report showed that the remaining temporal lobe was more 482-484, 2002 extensively damaged on MRI after transsylvian and trans- 5. Wyler AR, Hermann BP, Somes GW: Extent of medial temporal 18) resection on outcome from anterior temporal lobectomy: a ran- cortical AH than previously thought. 1n 2004, Lutz et domized prospective study. Neurosurgery 37:982-991, 1995 19) al., studied eighty randomized patients and showed that 6. Goldring S, Edwards I, Harding GW, Bernardo KL: Temporal cognitive outcome after both approaches were same except lobectomy that spares the amygdala for temporal lobe epilepsy. Neurosurg Clin N Am 4:263-272, 1993 the recovery of phonemic fluency. The recovery of pho- 7. Kanner AM, Kaydanova Y, de Toledo-Morrell L, Morrell F, Smith nemic fluency might be hindered in transsylvian approach MC, Bergen D, et al: Tailored anterior temporal lobectomy: Re- lation between extent of resection of mesial structure and post- due to frontal lobe manipulation. A combined subtemporal surgical seizure outcome. Arch Neurol 52:173-178, 1995 and transventricular/transchoroidal fissure approach was 8. Ojemann G, Ojemann J, Lettich E, Berger M: Cortical lan- also described as a variation.20) However, modifications guage localization in left, dominant hemisphere. J Neurosurg 71: 316-326, 1989 of the subtemporal approaches requires extensive retraction 9. Quarato PP, Di Gennaro G, Mascia A, Grammaldo LG, Meldo- of the basal temporal lobe and may have a risk to injure lesi GN, Picardi A, et al: Temporal epilepsy surgery: different surgical strategies after a non-invasive diagnostic protocol. J the vein of Labbe and the laterobasal cortex. Neurol Neurosurg Psychiatry 76:815-824, 2005 10. Fiol ME, Gates JR, Torres F, Maxwell RE: The prognostic value Temporal of residual spikes in the postexcision electrocorticogram after temporal lobectomy. Neurology 41:512-516, 1991 Bailey and Gibbs reported the poor outcome of anterior 11. Mackenzie RA, Matheson J, Ellis M, Klamus J: Selective versus temporal lobotomy in 1951. Recently, Smith et al.,21) sug- non-selective temporal lobe surgery for epilepsy. J Clin Neuro- sci 4:52-154, 1997 gested temporal lobotomy may be effective disconnective 12. Yasargil MG, Wieser HG, Valavanis A, von Ammon K, Roth procedure in the treatment of TLE. But, the determina- P: Surgery and results of selective amygdala-hippocampectomy in one hundred patients with nonlesional limbic epilepsy. Neu- tion of the indications, efficacy, and safety of this proce- rosurg Clin N Am 4:243-261, 1993 dure requires further study. 13. Rougier A, Saint-Hilaire JM, Louiseau P, Bouvier G: Evaluation and surgical treatment of the . Neurochirurgie 38:3-112, 1992 CONCLUSION 14. Shimuzu H, Suzuki I, Ishijima B: Zygomatic approach for resec- tion of mesial temporal epileptic focus. Neurosurgery 25:798-801, 1989 Temporal lobectomy has played an important role in 15. Park TS, Bourgeois BFD, Silbergeld DL, Dodson WE: Subtem- the treatment of epilepsy. poral transparahippocampal amygdalohippocampectomy for sur- AH is increasingly performed but it is still unclear whe- gical treatment of mesial temporal lobe epilepsy. J Neurosurg 85:1172-1176, 1996 ther more limited surgical approaches produce equal 16. Wieser HG, Ortega M, Friedman A, Yonekawa Y: Long-term success rates with respect to seizure control or better seizure outcomes following amygdalohippocampectomy. J Neu- rosurg 98:751-763, 2003 neuropsychological performance. 17. 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