Current Literature In Clinical Science

The Risk–Benefit Ratio for Temporal Lobe Resection in Patients with Bilateral Mesial Temporal Lobe Epilepsy

Neuropsychological Outcome After Epilepsy Surgery in Patients with Bilateral Ammon’s Horn Sclerosis. Vogt VL, Witt JA, Malter MP, Schoene-Bake JC, von Lehe M, Elger CE, Helmstaedter C. J Neurosurg 2014;121:1247–1256.

OBJECT: The purpose of this study was to retrospectively assess the objective and subjective neuropsychological outcome after epilepsy surgery in patients with bilateral Ammon’s horn sclerosis (AHS). METHODS: Memory and executive functions were evaluated at baseline and at follow-up in 11 surgically treated patients and compared with 8 pharmacologically treated patients with temporal lobe epilepsy and bilateral AHS. The median follow-up duration was 16 months in the surgically treated patients and 80.5 months in the pharmacologically treated group. Subjective outcome was evaluated by questionnaires and included mood, quality of life, subjective memory, and activities of daily living. RESULTS: At the follow-up assessment, 82% of the surgically treated patients as opposed to 0% of the nonsurgery patients were seizure free. In the surgical group, nonverbal memory performance did not change significantly in any patient after surgery, but there was a floor effect in 55% of the surgical patients. Regarding verbal memory, 9% of the surgical patients improved while 73% declined, despite severe impairments already evident at baseline. In the nonsurgery control group, 13% of the patients declined in nonverbal memory (floor effect in 63%) and 25% declined in verbal memory (floor effect in 25%) at follow-up. None of the controls improved at follow-up. Executive functions remained unchanged on an impaired level in both groups. At follow-up, the patient groups did not differ significantly with respect to mood, quality of life, subjective memory, or activities of daily living. However, in most aspects, surgically treated patients reported a slightly better subjective outcome than pharmacologically treated patients and a significantly improved quality of life. CONCLUSIONS: These results suggest that beyond benefits concerning seizure control, surgically treated patients with bilateral AHS, despite already poor baseline performance, are still at risk for severe postoperative decline in memory. In the light of predominantly minor benefits on a subjective level, the findings put the overall outcome of epilepsy surgery in bilateral AHS patients into perspective.

Commentary Drug-resistant focal epilepsy in the context of bilateral hippocampal sclerosis (HS) is a predicament with many obstacles and very few solutions. Like other patients with drug-resistant epilepsy, those who struggle with this condition carry the burden of uncontrolled seizures, poor quality of life, medication side effects, and increased mortality risk. In particular, though, they are vulnerable to the cognitive and neuropsychiatric consequences of bilateral hippocampal dysfunction, including memory loss and psychiatric comorbidities (1–3). Resective epilepsy surgery, representing the typical “magical” solution for drug-resistant epilepsy, is actually a very challenging option for this patient population. The article by Vogt et al., chosen for this commentary, is the most recent addition to a very small body of literature highlighting this conundrum. In this article, Vogt et al. describe in detail 11 patients with imaging evidence of bilateral HS who underwent temporal Epilepsy Currents, Vol. 15, No. 2 (March/April) 2015 pp. 78–79 © American Epilepsy Society

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lobe epilepsy surgery in their center between 2003 and 2006, and compare them to 8 epilepsy patients with similar bilateral HS who continued with medical therapy alone. The crux of surgical decision-making in this special context usually centers around two main questions: 1) how likely is a resection to render patients with bilateral HS seizure free or even significantly help with seizure control? and 2) will surgery in this context “hurt” the patients cognitively? While limited by a small sample size, the report at hand presents significant detail with a comprehensive assessment of these patients, extending beyond seizure control to impact on quality of life, mood, memory, and cognitive functions. Seizure Control In Vogt et al., 82% of the surgically treated group (9/11) were seizure free after a median follow-up of 16 months as opposed to none of the nonsurgery patients. Such favorable success rates with regard to seizure control are comparable with some earlier studies with similarly short postoperative follow-up durations or small sample sizes: Martin et al. reported a “higher than 70%” seizure-freedom rate about a year after temporal lobe resection in 21 patients with bilateral hippocampal atro-

Surgery for Bilateral Temporal Lobe Epilepsy

phy (4). In another report, four of five patients with bilateral hippocampal atrophy evaluated with intracranial recordings were seizure free more than 2 years after temporal lobe resection (5). Unilateral seizures recorded on intracranial depth recordings may, in fact, guide surgical resection and correlate with a better prognosis (6). However, when compared to patients with unilateral hippocampal atrophy in larger surgical series with longer follow-up durations, the seizure outcomes in patients with bilateral HS were not very optimistic: in a series of 371 patients with TLE surgery, 58% of 31 patients with bilateral hippocampal atrophy were seizure free at 2 postoperative years as opposed to 78% of patients with unilateral hippocampal atrophy or even a normal brain MRI (7). Similarly, bilateral hippocampal atrophy correlated with worse seizure outcomes in several other studies (8, 9). Recent data from chronic responsive neurostimulation suggest that patients with bilateral TLE cluster not only in space (one temporal lobe “sicker” than the other) but also in time (one temporal lobe seizing for several weeks or months before contralateral seizures are recorded): this helps explain why intracranial recordings typically performed for several days do not necessarily provide a comprehensive picture of the epilepsy disease burden and have not consistently been found to modify seizure outcomes for patients with this inherently bilateral epilepsy substrate (10). Overall, a fair statement is that long-term seizure outcomes after unilateral temporal lobe surgery for patients with bilateral hippocampal atrophy are less than optimal but remain better than medical therapy alone. These benefits have to be weighed against the risks of surgery before an informed decision can be made. Neuropsychological Risks The data presented by Vogt et al. suggest that the cognitive risk of surgery is noteworthy. In their series, 73% of surgical patients showed a significant decline in their verbal memory by last follow-up as opposed to 25% of the medically treated group. This is despite the fact that both medical and surgical groups had significant verbal memory deficits at baseline. Nonverbal memory, executive function, quality of life, and mood were the same in both the medical and surgical groups at last follow-up. These results are in line with older literature showing significant memory worsening after temporal lobe resection in patients with bilateral TLE, particularly when the left hippocampus is the one being removed (1, 11). These results are also in line with recent functional MRI data, suggesting that it is the capacity of the posterior remnant of the ipsilateral hippocampus rather than the functional reserve of the contralateral hippocampus that is important for maintaining verbal memory function after left anterior temporal lobe resection (12)—potentially explaining why patients would still be at risk for memory decline even after removal of a seemingly sclerosed dominant hippocampus. The extent to which these memory impairments affects patients’ daily function needs to be better defined. The fact that the end result in Vogt et al. was a similar quality of life in both the medical and the surgical group suggests that improvements gained by seizure control were shadowed by the negative functional impacts; however, conclusions in this regard are limited by small sample

size and methodological issues with variable administration of the scales at baseline and follow-up. Acquiring detailed knowledge about this balance between benefit and harm in this patient group is critical and is going to be even more important to drive decision-making in the future as nonresective options become more available for patients with focal epilepsy in the setting of bilateral HS through the introduction of responsive neurostimulation. An accurate understanding of the risk–benefit ratio is needed, and larger scale well-designed studies of this problem are going to be crucial. by Lara E. Jehi, MD References 1. Trenerry MR, Jack CR, Jr, Cascino GD, Sharbrough FW, So EL. Bilateral magnetic resonance imaging-determined hippocampal atrophy and verbal memory before and after temporal lobectomy. Epilepsia 1996;37:526–533. 2. Shaw P, Mellers J, Henderson M, Polkey C, David AS, Toone BK. Schizophrenia-like psychosis arising de novo following a temporal lobectomy: Timing and risk factors. J Neurol Neurosurg Psychiatry 2004;75:1003–1008. 3. DeLong GR, Heinz ER. The clinical syndrome of early-life bilateral hippocampal sclerosis. Ann Neurol 1997;42:11–17. 4. Martin RC, Sawrie SM, Knowlton RC, Bilir E, Gilliam FG, Faught E, Morawetz RB, Kuzniecky R. Bilateral hippocampal atrophy: Consequences to verbal memory following temporal lobectomy. Neurology 2001;57:597–604. 5. King D, Spencer SS, McCarthy G, Luby M, Spencer DD. Bilateral hippocampal atrophy in medial temporal lobe epilepsy. Epilepsia 1995;36:905–910. 6. Hirsch LJ, Spencer SS, Spencer DD, Williamson PD, Mattson RH. Temporal lobectomy in patients with bitemporal epilepsy defined by depth electroencephalography. Ann Neurol 1991;30:347–356. 7. Jeha LE, Najm IM, Bingaman WE, Khandwala F, Widdess-Walsh P, Morris HH, Dinner DS, Nair D, Foldvary-Schaeffer N, Prayson RA, Comair Y, O’Brien R, Bulacio J, Gupta A, Lüders HO. Predictors of outcome after temporal lobectomy for the treatment of intractable epilepsy. Neurology 2006;66:1938–1940. 8. Garcia PA, Laxer KD, Barbaro NM, Dillon WP. Prognostic value of qualitative magnetic resonance imaging hippocampal abnormalities in patients undergoing temporal lobectomy for medically refractory seizures. Epilepsia 1994;35:520–524. 9. Kuzniecky R, Ho SS, Martin R, Faught E, Morawetz R, Palmer C, Gilliam F. Temporal lobe developmental malformations and hippocampal sclerosis: Epilepsy surgical outcome. Neurology 1999;52:479–484. 10. Spencer D, Gwinn R, Salinsky M, O’Malley JP. Laterality and temporal distribution of seizures in patients with bitemporal independent seizures during a trial of responsive neurostimulation. Epilepsy Res 2011;93:221–225. 11. Martin RC, Kretzmer T, Palmer C, Sawrie S, Knowlton R, Faught E, Morawetz R, Kuzniecky R. Risk to verbal memory following anterior temporal lobectomy in patients with severe left-sided hippocampal sclerosis. Arch Neurol 2002;59:1895–1901. 12. Bonelli SB, Thompson PJ, Yogarajah M, Powell RH, Samson RS, McEvoy AW, Symms MR, Koepp MJ, Duncan JS. Memory reorganization following anterior temporal lobe resection: A longitudinal functional MRI study. Brain 2013;136(pt 6):1889–1900.

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The Risk-Benefit Ratio for Temporal Lobe Resection in Patients with Bilateral Mesial Temporal Lobe Epilepsy.

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