Egyptian Journal of Volume 29 / No. 4 / October - December 2014 31-38

Original Article Non-image Guided Selective Amygdalohippocampectomy for Refractory Mesial Temporal Lobe

Mohamed H. El-Sissy* Neurosurgery Department, Cairo University Egypt

ARTICLE INFO ABSTRACT Background: is the most frequent type of treatment-resistant epilepsy. Mesial temporal sclerosis (MTS) is the most common recognized cause of Received: temporal lobe epilepsy (TLE). Only half of patients responds to medical treatment. 18 December 2014 Surgery is the only effective treatment for mesial temporal sclerosis epilepsy in case of

failure of medical treatment with a success rate of 60% - 90%. Objective: is to assess the Accepted: 21 February 2015 feasibility of performing selective amygdalohippocampectomy without image guidance for refractory mesial temporal lobe epilepsy cases caused by hippocamppal sclerosis. Patients and Methods: Twenty six patients (fifteen females and eleven males) with age Key words: range 11-64 years, with intractable temporal lobe epilepsy, after proper evaluation; Temporal lobe epilepsy, clinical, magnetic resonance imaging (MRI) and video , all Mesial temporal sclerosis, selected cases had minimally invasive non-image guided selective Amygdalohippocampectomy amygdalohippocampectomy. Results: Precipitating factors were evident in 46,15% of cases; subdivided as follows: 26,92 % had febrile seizure (the most common), 11,53% had head trauma, 3,84% had encephalitis and 3,84% had perinatal asphyxia. The preoperative median weekly seizure frequency was two. 53,84% of cases had CPS with secondary generalization and 46,15% of cases had complex partial seizures (CPS) without secondary generalization. Patients used a median of 2 antiepileptic medications (AEDs) preoperatively. Seizure control outcomes at the last follow up revealed by modified Engel outcome (table III): 65,38% of cases were Engel Class I, 11,53% of cases were Engel Class II, 15,38% of cases were Engel Class III and 7,69% of cases were Engel Class IV. Single case developed wound infection. 38,46% of cases had complete AED cessation, 53,84% had reduction in AED doses and 7,69% had no change in AED regimen. Conclusion: Selective amygdalohippocampectomy is a safe, precise, easy and effective surgical procedure, without the necessity of image guidance or larger resection, in properly selected cases with refractory mesial temporal lobe epilepsy due hippocampal sclerosis © 2014 Egyptian Journal of Neurosurgery. Published by MEDC. All rights reserved

INTRODUCTION follow-up, and use different statistical methods. Such discrepancies likely explain the wide variation in Temporal lobe epilepsy is the most frequent type of seizure freedom after surgery for MTS and the factors 25,26 treatment-resistant epilepsy.19,22,23 Mesial temporal that predict the outcome . sclerosis (MTS) is the most common recognized cause of temporal lobe epilepsy (TLE), only 50% of cases PATIENTS AND METHODS respond to medical treatment 18 A randomized, controlled trial demonstrated the superior efficacy of This study included twenty six patients (fifteen surgery over prolonged medical therapy for TLE 20,57 females and eleven males), age range 11 to 64 years, and rates of seizure freedom after surgery range from with intractable temporal lobe epilepsy, defined as 60% to 90% in most studies. 5,12,16,50,57 failure of at least two trials of antiepileptic monotherapy Various centers use different definitions of seizure and one combination therapy at therapeutic levels over freedom, assess seizure freedom at different times of two years at least, all cases were managed in Kasr Al Aini Hospital, Cairo university, Egypt, between June 2003 and January 2009 after having detailed informed *Corresponding Author: consent. Mohamed Hamdy El-Sissy All patients underwent a standard presurgical Neurosurgery Department, Cairo University Egypt Email: [email protected], Tel.: +966508324521 evaluation that included 1) demographic information 2) history and physical examination including epilepsy

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El-Sissy / Non-image Guided Selective Amygdalohippocampectomy, Volume 29 / No. 4 / October - December 2014 31-38 characteristics, mean weekly seizure frequency, Follow up: treatment history and current antiepileptic medications All patients underwent follow-up after surgery for with full description of the seizure semiology; 3) video- four years, data on seizure frequency and AED electroencephalography (EEG) ictal and interictal were regimens were recorded at each visit. Neurological and a prerequisite prehand and before admission to Kasr Al non-neurological complications were recorded. Epilepsy Ainy Hospital; 4) magnetic resonance imaging (MRI) outcomes were assessed at each visit using a modified with T1- and T2-weighted and Flair sequences to assess Engel scale17 Engel I: seizure free with or without aura, for hippocampal atrophy and increased T2 signal. Engel II: greater than 90% reduction in seizure Selection criteria included patients with classic frequency, Engel III: 50%–90% reduction in seizure findings consistent with MTS such as complex partial frequency; and Engel IV: less than 50% reduction in seizures (CPS), epileptiform activity arising in the seizure frequency. Routine interictal EEG was mesial temporal structures, and unilateral hippocampal performed, and antiepileptic medications were managed atrophy with or without a T2 hyperintense signal at the discretion of the treating epileptologist. (Figure 1,2,3.4). Surgical technique: RESULTS The patient is positioned supine with the head held in position in 3-pin fixation, rotated 90 degrees to the The studied cases were analyzed demographically opposite side and parallel to the floor, 4 cm linear scalp and clinically (Table 1): fifteen cases were females and incision above the root of the zygoma, 2,5 cm in front of eleven cases were males with age range of 11 – 64 the auricle. The temporalis fascia and muscle is incised years, the mean age at seizures onset was 13,3 years and retracted. is performed and dura opened with age range 1 – 42 years. Hippocampal sclerosis was and flapped inferiorly. Transverse cortical incision in left sided in sixteen cases (61,53%) and right sided in the middle temporal gyrus that is 3.0 cm behind the tip ten cases (38,46%). Precipitating factors were of the temporal lobe and in an area free of cortical encountered in twelve cases (46,15%); subdivided as vessels. The corticectomy is generally 2.5 cm in length, follow: seven cases (26,92 %) had febrile seizure as the followed by temporal lobe dissection toward the most common, three cases (11,53%) had head trauma, temporal horn until it is entered. With gentle single case (3,84%) had encephalitis and another case retraction an optimal view of the intraventricular (3,84%) had perinatal asphyxia. The preoperative anatomy is evident, and key anatomical structures are median weekly seizure frequency was two. Fourteen identified. The parahippocampal gyrus is resected patients (53,84%) had CPS with secondary beginning with subpial resection of the uncus and then generalization and twelve patients (46,15%) had CPS advancing medially and posteriorly. With resection of without secondary generalization. Patients used a the anterior uncus, the incisura is visualized, and median of two AEDs preoperatively. Regarding superiorly the internal carotid artery and third nerve can significance of risk factors only SGS and postoperative be seen through the pia. The choroidal fissure is early seizures were statistically significant; P value in identified. Care must be taken to ensure that the case of SGS; at the end of the first year was p=0,033 dissection is not carried superior to the choroidal and at the last follow up p=0.056, for postoperative fissure. The is then mobilized laterally and early seizures p=0,003 at the end of the first year, while resected beginning anteriorly, with care to preserve the at the last follow up p=0,002. Seizure control outcomes anterior choroidal artery, and carried posteriorly to the at the last follow up by modified Engel outcome (table level of the tectal plate. Once the hippocampal resection 2) revealed: seventeen cases (65,38%) were Engel Class is completed, the cerebral peduncle and anterior I, three cases (11,53%) were Engel Class II, four cases choroidal artery are visualized through the pia. Careful (15,38%) were Engel Class III and two cases (7,69%) hemostasis is obtained. In stepwise fashion the dura is was Engel Class IV. There were no operative deaths and closed, bone flap fixed, temporalis muscle no neurological deficits occurred after surgery, only reapproximated, and scalp closed in layers to the skin. single case developed wound infection managed by Pathological examination: repeated dressings and antibiotics according to culture Mesial temporal sclerosis was diagnosed via and sensitivity. Regarding AED cessation, ten cases pathological findings: cell loss in the CA3 and CA1 (38,46%) had complete AED cessation, fourteen cases pyramidal cells and dentate hilar neurons with relative (53,84%) had reduction in AED doses and only two sparing of the dentate granular cells and CA2 pyramidal cases (7,69%) had no change in AED regimen. cells. The pathologists reported their findings without clinical or imaging data.

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Table (1): Demographic and clinical data of patients Sex (female/male) 15 (57.69%) / 11 (42.3%) Mean age at seizures onset in years 13,3 y ( 1 – 42 y) Mean age at surgery 38,3 y (11 – 64 y) Lateralization ( left / right ) 16 (61.53%) / 10 (38.46%) Precipitating factors: 12 (46.15%) Febrile seizures 7 (26.92%) Head trauma 3 (11.53%) CNS infection 1 (3.84%) Perinatal insult 1 (3.84%) Median seizure frequency per week 2 Median number of antiepileptic drugs 2 Secondary seizure generalization 14 (53.84%)

Table 2: Modified Engel classification of cases End of first year End of 2nd year End of 3rd year End of 4th year Engel I 80,69% 73,07% 69,23% 65,38% Engel II 7,69% 11,53% 15,38% 11,53% Engel III 7,69% 11,53% 7,69% 15,38% Engel IV 3,84% 3,84% 7,69% 7,69%

a b Fig. 1 a&b: a: Coronal MRI T2-weighted image with right sided hippocampal atrophy, b: Postoperative axial MRI T2- weighted image after transcortical non-image guided selective amygdalohippocampectomy

a b Fig. 2 a&b: a: Coronal MRI T2-weighted image with right sided hippocampal atrophy, b: Postoperative coronal MRI T1-weighted image after transcortical non-image guided selective amygdalohippocampectomy.

Egyptian Journal of Neurosurgery 33 El-Sissy / Non-image Guided Selective Amygdalohippocampectomy, Volume 29 / No. 4 / October - December 2014 31-38

Fig. 3: Lateralized temporal spike and slow wave complex at the T5 electrode and a field that includes the T3 electrode are seen in left temporal lobe region.

Fig. 4: EEG trace showed focal interical epileptiform discharge. Lateralized temporal spike and slow wave complex with phase reversal at the T6 electrode and a field that includes the T4 electrode are seen in right temporal lobe region.

DISCUSSION MTLE associated with hippocampal sclerosis (HS), 20 14 either anterior temporal lobectomy (ATL) or selective 60 Temporal lobe epilepsy is the most common type of amygdalohippocampectomy (SEAH) is the treatment intractable partial epilepsy. The typical substrate of choice. The surgical results in HS are gratifying; associated with medial temporal lobe epilepsy (MTLE) seizure freedom is achieved in 60% to 90% of patients, is hippocampal sclerosis (HS) accounting for 60% to with low morbidity and the findings of HS, both 70% of cases. 1,61 The etiology of HS remains unclear. preoperatively by MRI and postoperatively by histology Histologically, severe neuronal loss and gliosis are and electrophysiology, predict higher seizure-free 12,37,41,45,55,57,59 observed, especially in the CA1, CA3, and CA4 outcomes. In this study we report the subfields of the hippocampus.6 Recurrent sprouting of surgical outcome of patients with MTLE due to HS, mossy fibers is also seen. In most patients, the who underwent standard pre and postoperative epileptogenic focus involves the mediobasal structures evaluations and a uniform surgical procedure, which is of the temporal lobe. These structures include the transcortical selective amygdalohippocampectomy hippocampus, , uncus and parahippocampal without navigation guidance. This approach is gyrus. Antiepileptic drugs usually suppress secondary employed in cases of medically refractory temporal lobe generalized seizures successfully, but 50% of patients or epilepsy of mesial temporal origin. There is no more will continue to have partial seizures.18 When universally agreed upon definition of medically seizures persist, surgery is an effective treatment for refractory or treatment-resistant epilepsy. Many

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El-Sissy / Non-image Guided Selective Amygdalohippocampectomy, Volume 29 / No. 4 / October - December 2014 31-38 authorities use a working definition of failure of at least scores between the ipsilateral and contralateral two trials of antiepileptic drug monotherapy and one hemispheres, and the Wada results were concordant combination therapy when used at therapeutic levels with the side of operation in about 80% of patients, over 1-2 years, this was the protocol we followed in our 24,34,35,36,49,54,62 and may result from hippocampal study; however, a variety of definitions have been dysfunction by chronic epilepsy impairing functioning employed. 4,30 In practice, many patients have failed while the other temporal lobe is anesthetized by amytal. much more extensive medication trials over much more Other centers have reported similar rates of correlation extended time periods. Most commonly, suitable between Wada testing and noninvasive studies (80%– candidates are selected based on convergent lines of 90%) and hippocampal volume. 11,34,35,36,53 Greater evidence implicating unilateral mesial temporal disparity on Wada testing and hippocampal volumetric structures as the epileptogenic region.15 Consolidated analyses were inversely correlated with memory decline with compatible ictal semiology and neurological after surgery 11 (greater dysfunction in the involved history. Video-EEG monitoring should confirm ictal hemisphere) and predicted seizure control. 34,35,36 Based semiology and stereotyped ictal onset on scalp EEG on previous studies, IAT offers important localization consistent with mesial temporal origin. Interictal EEG information and prognostication in terms of may show concordant unilateral or bilateral (usually postoperative deficits (memory and language) and ipsilateral predominant) epileptiform discharges. MRI seizure freedom. Some contend that IAT is obsolete and often demonstrates an abnormality in the mesial can be replaced by preoperative language and memory temporal structures: most commonly hippocampal testing by functional MRI. 3,10,52 Others stated that atrophy with or without mesial temporal signal change noninvasive functional studies such as functional MRI on T2-weighted or FLAIR sequences. Patients with cannot predict the amnestic risk after temporal exclusively mesial temporal foreign tissue lesions (e.g., lobectomy as accurately as IAT. Functional MRI low grade tumor) or neurodevelopmental abnormalities memory protocols are lagging behind language may also be good candidates for this procedure but not assessments, and results of memory testing with this included in our study. Additional studies may be used noninvasive modality are limited to small including positron emission tomography (PET), series.7,29,34,46,48 In our study we did not depend on IAT (MEG) and ictal single to investigate patients preoperatively. As brief photon emission computed tomography (SPECT). historical background; Paulo Niemeyer reported Particularly in non-lesional cases, if standard evaluation, selective resection of mesial temporal structures for supplemented by specialized imaging studies, defines a intractable epilepsy in 1958. 42 In a letter to his unilateral temporal lobe onset, intracranial EEG colleague Henri Gastaut, he related “because the focus monitoring may be required for distinguishing mesial of this epilepsy is usually in the nucleus amygdalae, in from temporal neocortical onset so as to determine Ammon’s horn, or in the hippocampus of gyrus, I whether SEAH is indicated or ATL is mandatory. None resected these 3 structures via a transventricular of our cases was non-lesional in MRI. The intracarotid approach, almost without touching the temporal cortex”. amobarbital test (IAT) or was first described 8 The fascinating history of his pioneering work in in 1960 by Wada and Rasmussen 56 and was originally neurosurgery in Brazil is related in a recent historical conceived to obtain functional information concerning article by Cavalcanti et al. 8 Subsequently Wieser and language prior to surgery and was later adapted to Yasargil popularized a transsylvian approach to SEAH assess memory. Worse functioning of one temporal lobe and reported outcomes of large numbers of patients who (as measured by memory performance) suggests greater underwent this procedure. 60,63 Other approaches underlying damage from chronic epilepsy. A Wada including subtemporal47 and variants of the transcortical memory asymmetry between involved and uninvolved approach have been described. 33,43 Use of SEAH hemispheres of as little as 25% can differentiate medial became more widespread in the 1990s in tandem with versus lateral neocortical TLE. 24 Compared with non- increased utilization of intraoperative neuronavigation MTS patients with TLE, Wada memory testing may be systems. There are data comparing SEAH and anterior more specific for MTS patients, possibly due to direct temporal lobectomy (ATL) in terms of seizure control. involvement of the mesial temporal structures, regions Selective amygdalohippocampectomy was suggested known to be involved in proper memory functioning. 28 with advantages of reduced risk of cognitive side effects Others have reported that significant asymmetry and injury to the optic radiation.60 A poorer between the hemispheres on Wada memory testing can psychosocial outcome for ATL was reported compared predict seizure control after surgery in children and to more selective techniques. 10 Two recent studies have adults. 31,32,34,35,36,49,54 Greater memory asymmetries on also compared seizure outcomes for ATL and SEAH.2,44 Wada testing between ipsilateral and contralateral A better outcome (Engel I and II) was reported more hemispheres (that is, correctly lateralized) were frequently in ATL than SEAH, giving 66% associated with a greater likelihood of seizure freedom improvement versus 44%. 2 Ozkara et al. 44 reported an after surgery. 34,35,49 Several reports mentioned that overall seizure outcome of 72.1% in Engel I and 56.4% about 60% difference in the Wada memory testing in ILAE I (International League Against Epilepsy) at the

Egyptian Journal of Neurosurgery 35 El-Sissy / Non-image Guided Selective Amygdalohippocampectomy, Volume 29 / No. 4 / October - December 2014 31-38 last available follow-up in a patient group operated on REFERENCES either by SEAH or ATL and the prognosis was found to be better with ATL surgery according to Engel, but not 1. Babb T, Brown WJ: Pathological findings in epilepsy according to ILAE classification. A more recent study In: Engel J ed. Surgical treatment of . New reviewed 53 studies addressing the extent of resection in York: Raven Press. pp: 511-540, 1987 surgery for TLE and concluded that SEAH appears to 2. Bate H, Eldridge P, Varma T, Wieshmann UC: The have similar seizure outcome but a better cognitive seizure outcome after amygdalohippocampectomy and outcome than temporal lobectomy. 51 In our study, at the temporal lobectomy. European Journal of last follow up 65,38% were classified in Engel I , Neurology 14:90-94, 2007 11,53%% as Engel II and 15,38% as Engel III and 3. 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