revue neurologique 171 (2015) 315–325

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Hippocampus and epilepsy

Surgical treatment for mesial temporal lobe epilepsy associated with hippocampal sclerosis Traitement chirurgical de l’e´pilepsie temporome´siale associe´e a` une scle´rose hippocampique B. Mathon a,*, L. Be´dos Ulvin b, C. Adam b, M. Baulac b, S. Dupont b, V. Navarro b, P. Cornu a, S. Clemenceau a a

Department of neurosurgery, groupe hospitalier universitaire de la Pitie´-Salpeˆtrie`re, 47–83, boulevard de l’Hoˆpital, 75013 Paris, France b Department of epileptology, groupe hospitalier universitaire de la Pitie´-Salpeˆtrie`re, 47–83, boulevard de l’Hoˆpital, 75013 Paris, France

info article

abstract

Article history:

Introduction. – Hippocampal sclerosis is the most common cause of pharmacoresistant

Received 30 October 2014

epilepsy amenable for surgical treatment and seizure control. The aim of this article is

Received in revised form

to review and evaluate the published literature related to the outcome of the surgical

1 January 2015

treatment of mesial temporal lobe epilepsy (MTLE) associated with hippocampal sclerosis

Accepted 30 January 2015

(HS) and to describe the future prospects in this field.

Available online 3 March 2015

State of art. – Surgery of MTLE associated with HS achieves long-term seizure freedom in

Keywords:

Mortality following temporal resection is very rare (< 1%) and the rate of definitive neuro-

about 70% (62–83%) of cases. Seizure outcome is similar in the pediatric population. Surgery

logical complication is low (1%). Gamma knife stereotactic radiosurgery used as a treatment

Epilepsy

for MTLE would have a slightly worse outcome to that of surgical resection, but would

Hippocampal sclerosis

provide neuropsychological advantage. However, the average latency before reducing or

Mesial temporal lobe

stopping seizures is at least 9 months with radiosurgery. Regarding palliative surgery,

Outcome

amygdalohippocampal stimulation has been demonstrated to improve the control of

Hippocampal stimulation

epilepsy in carefully selected patients with intractable MTLE who are not candidates for

Future prospects

resective surgery. Perspectives. – Recent progress in the field of imaging and image-guidance should allow to

Mots-cle´s :

elaborate tailored surgical strategies for each patient in order to achieve seizure freedom.

Chirurgie E´pilepsie

Concerning therapeutics, closed-loop stimulation strategies allow early seizure detection and responsive stimulation. It may be less toxic and more effective than intermittent and

Scle´rose hippocampique

continuous neurostimulation. Moreover, stereotactic radiofrequency amygdalohippocamp-

Lobe temporal me´sial

ectomy is a recent approach leading to hopeful results. Closed-loop stimulation and

Stimulation hippocampique

stereotactic radiofrequency amygdalohippocampectomy may provide a new treatment

Re´sultats

option for patients with pharmacoresistant MTLE.

Perspectives * Corresponding author. E-mail address: [email protected] (B. Mathon). http://dx.doi.org/10.1016/j.neurol.2015.01.561 0035-3787/# 2015 Elsevier Masson SAS. All rights reserved.

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revue neurologique 171 (2015) 315–325

Conclusions. – Mesial temporal lobe surgery has been widely evaluated and has become the standard treatment for MTLE associated with HS. Alternative surgical procedures like gamma knife stereotactic radiosurgery and amygdalohippocampal stimulation are currently under assessment, with promising results. # 2015 Elsevier Masson SAS. All rights reserved.

r e´ s u m e´ Introduction. – La scle´rose hippocampique est la cause la plus fre´quente d’e´pilepsie pharmacore´sistante pouvant de´boucher sur un traitement chirurgical curatif et, de surcroıˆt, sur la gue´rison du patient. Le but de cet article est de faire un point sur les re´sultats actuels ainsi que sur les axes de recherche et de de´veloppement en chirurgie de l’e´pilepsie du lobe temporal me´sial, notamment dans le contexte d’une scle´rose hippocampique. E´tat des connaissances. – La chirurgie de l’e´pilepsie temporome´siale associe´e a` une scle´rose hippocampique permet d’atteindre la liberte´ de crises a` long terme dans environ 70 % (62– 83 %) des cas. En population pe´diatrique, les re´sultats sont semblables. La mortalite´ suivant une re´section temporale est exceptionnelle (< 1 %) et le taux de complication neurologique de´finitive est tre`s faible (1 %). La radiochirurgie ste´re´otaxique obtiendrait des re´sultats le´ge`rement infe´rieurs a` la chirurgie de re´section, mais offrirait une e´pargne neuropsychologique. Cependant, avec cette technique, un de´lai d’au moins 9 mois est observe´ avant la re´duction ou la disparition des crises. En ce qui concerne la chirurgie palliative, la stimulation amygdalohippocampique a de´montre´ ame´liorer le controˆle de l’e´pilepsie chez des patients soigneusement se´lectionne´s avec une e´pilepsie temporome´siale pharmacore´sistante et qui ne sont pas candidats a` la chirurgie de re´section. Perspectives. – Les progre`s re´cents dans le domaine de l’imagerie et de la chirurgie guide´e par l’image devraient permettre d’e´laborer des strate´gies chirurgicales sur-mesures pour chaque patient afin d’obtenir la liberte´ de crises. Dans le domaine the´rapeutique, les strate´gies de stimulation a` boucle-ferme´e permettent la de´tection pre´coce des crises et une stimulation en re´ponse. Elles peuvent s’ave´rer moins toxiques et plus efficaces que les stimulations intermittentes ou continues. E´galement, l’amygdalohippocampectomie ste´re´otaxique par radiofre´quence est une technique re´cente dont les premiers re´sultats sont encourageants. La stimulation a` boucle-ferme´e et la thermocoagulation amygdalohippocampique par radiofre´quence pourraient s’imposer, dans le futur, comme des nouvelles options the´rapeutiques pour les patients souffrant d’e´pilepsie temporome´siale pharmacore´sistante. Conclusions. – La chirurgie temporome´siale a e´te´ largement e´value´e et est devenue le traitement de re´fe´rence pour l’e´pilepsie temporome´siale associe´e a` une scle´rose hippocampique. Des proce´dures chirurgicales alternatives comme la radiochirurgie ste´re´otaxique et la stimulation amygdalohippocampique sont toujours en cours d’e´valuation, avec des re´sultats prometteurs. # 2015 Elsevier Masson SAS. Tous droits re´serve´s.

1.

Introduction

It is useful to categorize temporal lobe epilepsy into one of two types based on the anatomical site of seizure onset: mesial temporal lobe epilepsy (MTLE) or neocortical. MTLE is the most common syndrome concerning focal epilepsy and it remains particularly drug-resistant [1]. Hippocampal sclerosis (HS) is considered as a distinct syndromic entity of MTLE. Antiepileptic drugs are indicated as a first-line treatment for MTLE associated with hippocampal sclerosis (MTLE/HS) [2]. Should the epilepsy prove to be pharmacoresistant, an early evaluation regarding epilepsy surgery must be performed [3]. This article reviews the different surgical strategies used to treat MTLE/HS: resective surgery, stereotaxic radiosurgery (SRS) and amygdalohippocampal stimulation. Using recent literature,

postoperative seizure outcomes, neuropsychological outcomes and surgical morbidity are described and analyzed in detail. This paper also provides a succinct overview of the future directions explored in MTLE/HS surgery.

2.

State of art

The main outcomes concerning MTLE surgery are summarized in the Table 1.

2.1.

Resective surgery

2.1.1.

Outcomes

Underscoring the paramount role of the mesial temporal limbic structures in MTLE, excellent results reducing the

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Table 1 – Surgical outcome after MTLE or MTLE/HS surgery according to Engel’s class. Curative surgery

Resective surgery

Adult (MTLE/HS)

Childhood (MTLE/HS)

Palliative surgery

Stereotactic radiosurgery

Adult (MTLE and MTLE/HS)

Amygdalohippocampal stimulation

Adult (MTLE and MTLE/HS)

Summary 151 183 108 87 Summary 8 18 Summary 30 MTLE 21 MTLE 10 MTLE/HS

62–76% Engel I (> 5 years) 74% Engel I (7 years) 71% Engel I (10 years) 62% Engel I (18 years) 76% Engel I (5 years) 53–78% Engel I (> 3 years) 78% Engel I (5 years) 67% Engel I (3.6 years) 60–67% Engel I (> 2 years) 67% Engel I (3 years) 65% Engel I (2 years) 60% Engel I (5 years)

[14–17] Wieser et al., 2003 [14] Dupont et al., 2006 [15] Hemb et al., 2013 [16] Savitr Sastri et al., 2014 [17] [19–22] Sinclair et al., 2003 [21] Wyllie et al., 1998 [22] [93–95] Barbaro et al., 2009 [93] Regis et al., 2004 [94] Rheims et al., 2008 [95]

Summary

Mean seizure reduction = 15–75% (> 2 years)  90% seizure reduction = 55% (8.5 years) Mean seizure reduction = 70% (2 years) Mean seizure reduction = 75% (2.5 years) Mean seizure reduction = 15% (2 years)

[126–131]

11 MTLE 2 MTLE/HS 6 MTLE/HS 4 MTLE

Vonck et al., 2013 [126] Boex et al., 2011 [127] Cukiert et al., 2014 [129] Tellez-Zenteno et al., 2006 [131]

MTLE: mesial temporal lobe epilepsy; MTLE/HS: mesial temporal lobe epilepsy associated with hippocampal sclerosis.

seizure frequency have been found using diverse approaches to selective amygdalohippocampectomy (SAH), that is, transsylvian [4], subtemporal [5], and transcortical [6], or to anterior temporal lobectomy (ATL) [7–9]. Functional temporal lobe disconnections have also been described [10,11]. In a controlled randomized trial studying surgical resection versus medical treatment in patients with MTLE, at 1 year, the cumulative proportion of patients who were free of all seizures (Engel class Ia) was 42% in the surgical group and 8% in the medical group [12]. Moreover, 64% of the patients who underwent surgery were free of seizures impairing awareness (Engel class I) at 1 year. Surgical treatment also proved to reduce the occurrence of sudden unexpected death in epilepsy (SUDEP) [12]. A meta-analysis of recent series (retrospective studies) concluded that the seizure-free rate after surgical resection in patients with MTLE was about 70% (33–93%) [13]. In long-term follow-up studies, 62%–83% of the patients were seizure-free (Engel class I) at the 5th year after surgery for MTLE/HS [14–17]. The wide variation of seizure freedom rate could be explained by the different postoperative management of antiepileptic drugs: some teams try to a decay of the drugs, while others retain the preoperative treatment [18]. When looking for predictors of outcome, a higher frequency of preoperative seizures was associated with an unfavorable postoperative outcome [17]. Regarding the pediatric population, the outcomes following the surgical treatment of MTLE/ HS are quite similar [19–22]. Literature suggests that surgical outcome is different for MTLE/HS compared with other forms of temporal lobe epilepsy [23]. In patients with MTLE, normal magnetic resonance imaging (MRI) cases show less seizure control compared with those who have HS. The study of Berkovic et al. [24] showed that, 5 years after surgery, 21% with normal MRI had no postoperative seizures versus 50% with HS and 69% of patients with cortical lesion (cortical dysplasia, dysembrioplasic neuroepithelial tumor [DNET], ganglioglioma). Similarly, a seizure-free state

of at least 2 years was achieved by 36% of those with normal MRI, 62% of those with HS and 80% of patients with cortical lesion. Some studies also suggest that certain cortical lesions, such as DNET and ganglioglioma are associated with a better outcome than HS [14,25–27]. The ATL consists of an anterior temporal cortical resection followed by a removal of the temporal mesial structures. The resection extent of temporal lobe is still debated and may appear controversial. Several authors found that the resection of the lateral part of temporal lobe is not correlated with a better postoperative outcome [28]. Moreover, the resection of the superior temporal gyrus (T1) provides no benefit [29]. These results suggest that the extent of lateral resection while performing an ATL does not improve the outcome, if the suspected epileptogenic zone is not located in the neocortex. The resection of the hippocampus, the amygdala and the parahippocampal gyrus is now considered as essential for the surgical treatment of MTLE/HS. Even if the extent of hippocampal resection is still debated [30], many studies and authors advocate for a complete amygdalohippocampectomy [31–35]. Prospective randomized trials reported contradictory results concerning the optimal extent of hippocampal resection [36–39]. Thus, Schramm et al. conducted a controlled trial comparing 2.5-cm versus 3.5-cm mesial temporal resection and did not show a different seizure freedom rate for the more posteriorly reaching 3.5-cm resection group [37,38]. These findings suggest that not maximal but adequate hippocampal volume resection leads to good seizure freedom [37]. The rationale of the SAH is to spare cerebral tissue not included in the seizure generator. SAH for temporal lobe epilepsy is performed when the data (semiology, neuroimaging, electroencephalography, stereoelectroencephalography) point to the mesial temporal structures. To date, a randomized evaluation comparing SAH to ATL for surgical treatment of MTLE/HS has not been done [40]. Wide retrospective series

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suggest that seizure freedom outcomes are similar in SAH and ATL patients [41–45]. Furthermore, several studies reported cognitive advantages of SAH compared to ATL, with less neuropsychological worsening especially in verbal memory and intellectual quotient [42,43,46,47]. Other studies concluded that SAH might not be better than ATL in improving cognitive function [48,49]. Moreover, transcortical and transsylvian approaches showed no difference in reducing seizure and in preserving memory [50]. It is well known that MTLE is associated with psychiatric disorders [51–53]. These may concern about 50% of patients, especially in the postoperative period [54–56]. Psychiatric status generally either improves or remains the same after MTLE surgery [57–59], but early or delayed post-surgical psychiatric complications can sometimes occur and make worse the psychiatric status [54,56]. The most important predictors of psychiatric outcome after surgery were seizure freedom and presurgical psychiatric history [59,60]. A multicenter trial reported that resective surgery was associated with an improvement in depression at 5 years after surgery. Furthermore, only the patients with good or excellent seizure outcome improved ratings in their mood [61]. When looking for a relation between psychiatric history and seizure outcome, conclusions remain controversial. In retrospective studies, Kanner et al. found that a lifetime psychiatric history predicts a worse seizure outcome following ATL [62], while Adams et al. concluded that a lifetime history of depression or psychosis was not associated with 1-year seizure outcome after ATL for MTLE/HS [63]. Regarding neuropsychological outcomes, global memory deficits occur rarely (1%), however verbal memory deficits after dominant hemisphere resections remain a problem (25– 50%) [3,64–68]. These occur even with good seizure control, but are more severe if seizures persist. Predictors of a postoperative verbal memory decline are a later age of seizure onset as well as the functional status of the mesial temporal lobe. A greater decline will be expected after resection of a structurally intact and well-functioning hippocampus [64,69]. On the other hand, patients who already demonstrate low preoperative verbal memory scores may show postoperative improvement [70]. A higher intellectual quotient has been reported to protect against postoperative memory decline in the patients with MTLE/HS with intact memory functions prior to surgery [71]. After non-dominant hemisphere resections, visuospatial memory deficits may occur (6–32%). Like for verbal memory, predictors of postoperative visual memory decline are a later age of seizure onset and the functional status of the mesial temporal lobe to be resected [69]. To summarize, patients with good preoperative memory function in the context of unilateral MTLE/HS should therefore be counseled regarding the likelihood of a significant postoperative decline in memory function following a mesial temporal lobe surgery [71]. The most frequent language deficit following dominant hemisphere resections is a deficit in naming (25–60%) [72]. Whether this deficit can be attributed to the resection of lateral temporal neocortex [29] or to the resection of the mesial temporal lobe structures [73,74] is debated. Naming difficulties have been reported even after selective amygdalohippocampectomies [75,76]. However, postoperative seizure freedom

may be associated with an improvement of language function [15,77]. Hermann and Wyler found that the patients operated on the temporal lobe in the dominant hemisphere showed significant improvement in receptive language comprehension and associative verbal fluency [77].

2.1.2.

Morbidity

Major complications are rare after mesial temporal surgery and tend to be temporary or limited in their symptomatology, if procedures are performed by experimented surgical teams in carefully selected and evaluated patients. Mortality is very rare (< 1%) [12] and the rate of complication is low: definitive hemiparesis or third cranial nerve paralysis occurs in 1% of the cases [78–82]. Visual field defects occur frequently after surgery for HS and are usually contralateral superior quadrantanopia due to direct trauma to the optic radiations while accessing the mesial temporal structures. Egan et al. reported 17% of visual field defects at 108 from center and 76% of visual field defects at 408 after mesial temporal surgery, but all patients in this study were asymptomatic for visual field defects [83]. No significant difference was found between the frequency of visual field defects produced from SAH and ATL. A recent study has shown the interest of preoperative tractographic study of the Meyer loop especially for left-sided temporal lobe epilepsy surgery, in order to decrease the risk of optic radiations injury [84].

2.1.3.

Conclusions

Literature observed excellent seizure free outcome in a carefully selected cohort of patients with MTLE/HS with refractory epilepsy. Worldwide, mesial temporal lobe surgery has been widely evaluated and has become the standard treatment for MTLE [2,3,85–87]. Patients with MTLE/HS should be referred early for presurgical evaluation.

2.2.

Gamma knife stereotactic radiosurgery

2.2.1.

Outcomes

Gamma knife SRS is indicated in the treatment of epilepsy, in particular on epileptogenic zones located in eloquent area. Although the first case of radiosurgical treatment of MTLE was reported in 1995 [88], the success with hypothalamic hamartomas has prompted interest in the use of SRS for MTLE associated with HS [89–92]. Two multicenter trials studied patients’ outcomes after SRS for MTLE. In the European trial, a 24-Gy marginal dose was used in 21 patients, while in the North American trial 20- and 24-Gy marginal doses were compared in 30 patients. In both studies, a significant reduction in seizure frequency was observed by 1 year and 65% of patients were seizure free at 2 years [93,94]. In another study, 60% of patients were seizure free at 5 years [95]. The average latency before reducing or stopping seizures was 9 to 18 months [96–98]. During this period, patients experience a dramatic increase in auras coinciding with the reduction, or cessation, of seizures [93,94]. However, wide differences between the results are observed in other retrospective series, highlighting the importance of patient selection and radiosurgical expertise [99,100]. A definitive randomized, controlled trial, the radiosurgery or open surgery for epilepsy (ROSE) trial, using 24 Gy for the margin, is currently underway in the

revue neurologique 171 (2015) 315–325

United States. SRS has also shown efficacy in the treatment of recurrent seizures after incomplete temporal lobectomy [101]. In addition, delayed MRI changes were constantly observed, specifically in the amygdalohippocampal target, indicating focused destruction [96,102]. Concerning cognition and memory, 15% of patients who underwent dominant temporal lobe SRS experienced a significant decline in either measure of verbal memory, and the prevalence of significant verbal memory improvements was 12% [93]. Thus, SRS may provide benefit with respect to verbal memory preservation compared to open surgery [94]. Moreover, Quigg et al. reported that the changes in cognitive outcomes, mood, and quality of life are unremarkable following SRS for MTLE [103].

2.2.2.

Morbidity

Literature has shown that SRS is safe for the treatment of MTLE. The most frequent adverse event following SRS is headache (70%), often requiring steroid treatment [93]. Furthermore, 50%–62.5% of patients experienced a contralateral superior quadrantanopia caused by lesion of optic radiations [93,94,104,105]. This is quite similar to the rate described after open surgery [83]. Several other adverse events have been reported: brain edema, intracranial hypertension and transient increase of seizure frequency [93,94]. Long-term complications can also rarely occur. SRS may result in tumor genesis and progressive cognitive disorders [106–108].

2.2.3.

Conclusions

Open surgery may confer a benefit as regards the possibility of immediate seizure cessation, therefore reduced SUDEP risk, as compared with the more delayed cognitive benefits of radiosurgical treatment [109,110]. As open surgery is proving to be satisfactory due to the rarity of complications and a high rate of seizure freedom, candidates for radiosurgical treatment must be carefully selected. Thus, the best candidates are young patients with middle severity epilepsy, a high risk of memory deficit with surgical resection [103,111].

2.3.

Amygdalohippocampal stimulation

2.3.1.

Outcomes

There is a considerable amount of patients suffering from pharmacoresistant MTLE who are not candidates for resective surgery. Some of these patients may benefit from deep brain stimulation or cortical stimulation. Therefore, electrical stimulation of the brain has been proposed as an additional option to resective surgery [112]. Since 1973, several studies have suggested some effect on seizure frequency by stimulation of several targets among deep brain structures including the anterior thalamus [113,114], the centromedian thalamic nucleus [115], the subthalamic nucleus [116,117], the caudate nucleus [118] and, more recently, the amygdalohippocampal (AH) complex [119–121]. Currently, deep brain stimulation is considered as a credible option for palliative treatment of MTLE [122–124]. The outcomes following AH (or hippocampal) stimulation are very variable. Successful reduction in seizure frequency by hippocampal stimulation was first reported in two patients by

319

Sramka et al. [125]. Vonck et al. evaluated the efficacy of stimulation in 11 patients with an extended long-term followup [126]. In more than half of the patients, a seizure frequency reduction of at least 90% was reached and 3 patients were seizure-free for more than 3 years [126]. In addition, Vonck et al. suggest that bilateral mesial temporal lobe stimulation may herald superior efficacy in unilateral MTLE [121,126]. However, in another studies, AH stimulation produced a reduction in seizures of 15%–75% [127–132]. The high variability of these results could be explained by the small number of patients of each study and the heterogeneity of included patients (seizure type and frequency). For comparison with other palliative neuromodulation techniques, vagus nerve stimulation allows a 50% reduction of seizures in half of patients (30–63%) [133–136]. As regards cognitive outcomes, intellectual and neuropsychological evaluation performed after AH stimulation revealed no overall pattern of change in cognitive measures [137].

2.3.2.

Morbidity

Current AH stimulation safety studies are mainly small sample size with short follow-up time. The long-term safety of implanted electrodes for treating MTLE is unknown. Experience has been gained from deep brain electrodes implanted to treat pain and movement disorders. The risk of hemorrhage is about 5% [138]. This includes potential intraparenchymal hemorrhage along the course of the wire, as well as possible postoperative subdural or epidural hematoma. There is also at least a 5% chance of infection, which may require removal of the hardware [139,140]. Less serious risks include headache, local pain or discomfort at the equipment sites, fullness or ringing in the ears, tingling or uncomfortable sensations on the face or body when stimulation comes on, or changes in mood, memory, thinking, and energy level. Animal research has also shown immunological consequences from hippocampal stimulation [141].

2.3.3.

Conclusions

AH stimulation has been demonstrated to improve the control of epilepsy in carefully selected patients with intractable MTLE who are not candidates for resective surgery [142]. The best candidates are patients with MTLE and unilateral independent epileptogenic zone, a postictal severe memory dysfunction ipsilateral to the epileptogenic zone with potentially severe professional and psychosocial impact of memory dysfunction, and no associated psychiatric illness [143]. However, only a few controlled clinical trials have been completed to definitely validate this as a standard therapy [144]. Additional studies with larger numbers of patients and long-term follow-up are needed to identify outcomes and complications that are not obvious in the studies with limited sample sizes.

3.

Perspectives

Future prospects in MTLE surgery are numerous and variable and especially concern stereotactic procedures, neurostimulation and new devices allowing an improvement of safety and accuracy of surgery [145,146].

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3.1.

revue neurologique 171 (2015) 315–325

Image-guided surgery

Neuronavigation can be used in all resective epilepsy surgeries. As previously described, resective surgery can be performed using various techniques (SAH, ATL, functional temporal lobe disconnection) or can be tailored. Imageguidance can be useful for some of these procedures. Image-guidance is already known to guide the surgeon during surgery and help to confirm the extent of mesial temporal resection. Moreover, MRI-rendered model can be achieved before surgery to measure the temporal lobe and the extent of resection can be planned related to anatomical structures (arteries, veins). More interestingly, although these findings remain controversial [147], several studies suggest that frameless imageguidance electrode placement would be as accurate as frame placement [148,149]. Thus, image-guidance represents a new option to place depth mesial temporal electrodes in context of stereoelectroencephalography. To the same model, intraoperative depth electrodes can be placed with image-guidance into mesial temporal lobe at the time of surgery to supplement electrocorticography [149]. Similarly, many of the principles of computer-guided imaging can be extrapolated to neurostimulation procedures, intraoperative imaging [150,151] or radiosurgery [152]. Long-term postoperative MRI can also be analyzed with this device and compared with preoperative studies. The analysis of radiological data allows a global reflection by looking at seizure and neuropsychological outcomes. Lessons learned in this way can be applied to plan image-guided surgery of future patients. In the future, image-guidance should allow to elaborate tailored surgical strategies (including open surgery, radiosurgery, neurostimulation, gene therapy) for each patient in order to achieve seizure freedom, by increasing the accuracy of targeting. Finally, recent progress in the field of imaging and image-guidance may change our knowledge about epilepsy and epileptogenesis [153].

3.2. Stereotactic radiofrequency amygdalohippocampectomy Stereotactic radiofrequency amygdalohippocampectomy (SRAH) has been proposed as an alternative, minimally invasive method for the treatment of MTLE [154]. The target was reached through an occipital approach using MRI stereotactic localization. Small series, published by a unique team (Prague, Czech Republic), evaluated the safety and the effectiveness of this technique with short follow-up ( 5 years). They showed that the clinical outcome of SRAH is comparable with that of resective surgery [155–159]. Vojtech et al. also suggest that SRAH could be superior to open surgery in terms of its neurocognitive outcomes [160]. Concerning the safety of this procedure, a higher rate of hemorrhagic complications is reported compared to open surgery [161]. A larger multicenter randomized trial of these approaches is required to evaluate this technique properly. However, in the future, SRAH could be an alternative therapy for MTLE. To the same model, laser [162] or ultrasonic [163] therapies could be used to lead to the thermocoagulation of the AH structures.

3.3. Neurostimulation and closed-loop (responsive) stimulation Several neurostimulation protocols are being investigated for MTLE [164,165]. These include continuous or intermittent stimulation of the hippocampus. However, the most immediate need is for a properly controlled, randomized clinical trial to document efficacy and safety of AH stimulation for intractable epilepsy. Studies of predictive factors for success also should be a high priority. There are also some protocols that use a closed-loop strategy in which a recording electrode in the hippocampus records a seizure onset that activates a stimulator to activate an electrode in an attempt to abort the seizure [166–168]. Safety of closed-loop stimulation was assessed in a clinical study. Results of this study revealed no serious adverse events [168]. A study evaluating this closed-loop device has already described about a 45% decrease in seizure frequency in the majority of patients at 9-months follow-up [169]. More recently, a randomized, double-blinded, multicenter, controlled trial demonstrated efficacy of the closed-loop stimulation in reducing the frequency of disabling seizures in 38% of patients with pharmacoresistant partial onset seizures [170,171]. Osorio et al. also concluded that closedloop devices are more efficient and should be better tolerated than an open-loop modality because of lower daily doses of stimulation [172]. Finally, ‘‘intelligent’’ detection of seizures using a closed-loop strategy may be less toxic and more effective than intermittent and continuous neurostimulation. Closed-loop strategy may provide a new treatment option for a subgroup of patients with pharmacoresistant MTLE, but further work is necessary to identify which target is most effective, the optimal stimulation parameters, and the ideal mode of stimulation [173,174].

4.

Conclusions

Surgery for MTLE/HS is a safe and effective strategy. It is necessary to differentiate curative procedures (resective surgery and radiosurgery) allowing seizure freedom for a high rate of patients, and palliative techniques (AH stimulation). Resective surgery has been widely evaluated and has become the standard treatment for MTLE/HS. The field of MTLE surgery is a new and promising one for SRS and AH stimulation. To definitively validate the routine use of SRS for MTLE/HS treatment, a comparison using a prospective randomized comparative trial, to the reference technic, which is resection, would be required. However, the use of AH stimulation for MTLE/HS treatment is still considered investigational. To date, this surgical strategy can only be used in patients who are not candidates for resective surgery. Although still requiring validation, important advances in image-guidance technique, neurophysiology and neurostimulation allow for increasing precision in mapping brain function, planning surgical resections or treating epileptogenic zone, and may also expand our understanding of the underlying mechanisms of MTLE.

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Disclosure of interest The authors declare that they have no conflicts of interest concerning this article.

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