Letter to the Editor: Medial temporal epilepsy

Full access

If the inline PDF is not rendering correctly, you can download the PDF file here.

To The Editor: We have read with great interest the paper by Hu et al.11 (Hu WH, Zhang C, Zhang K et al: Selective amygdalohippocampectomy versus anterior temporal lobectomy in the management of mesial temporal lobe epilepsy: a meta-analysis of comparative studies. A systematic review. J Neurosurg 119:1089–1097, November 2013).

The authors' study is an effort to compare seizure and memory outcomes after 2 surgical techniques generally used for the surgical treatment of pharmacoresistant mesial temporal lobe epilepsy (MTLE)—that is, selective amygdalohippocampectomy and anterior temporal lobectomy. First and foremost, the authors should be congratulated for their effort to perform an exhaustive meta-analysis of the pertinent literature concerning this still-debated issue. We obviously agree with the authors about the importance of identifying the surgical approach for achieving the best seizure and neuropsychological outcomes. However, we consider it useful to highlight a limitation of this study represented by the lack of the histological data.

Indeed, an increasing role for underlying pathological disorders has emerged in recent years;2–8,10,12–16 therefore, to better understand seizure and neuropsychological outcomes in temporal lobe epilepsy surgery, more attention should be paid to the histological diagnosis. Seizure prognosis of patients undergoing temporal lobe epilepsy surgery appears strictly related to the type of lesion.2–4,7,8,10,12–16 Even neuropsychological dysfunction may be related to the histological pattern of dentate gyrus granular cell pathology (GCP) and preserved neurogenetic ability.7,13 In our retrospective study about seizure outcome in drug-resistant MTLE10 treated with a tailored anterior temporal lobectomy along with amygdalohippocampectomy, patients with MTLE and an epilepsy-associated low-grade tumor, mesial temporal sclerosis (MTS), or MTS associated with focal cortical dysplasia (FCD) showed the best postsurgical seizure outcome (Engel Class I9 in > 80% of cases), whereas only 63% of patients with isolated FCD achieved the same type of outcome.

Our results support the thesis that the pathological substrate represents a significant predictor of seizure recurrence, with rates of Engel Class I outcomes ranging from 59% for patients with isolated FCD to 82%, 83%, and 84%, respectively, for those with isolated MTS, epilepsy-associated low-grade tumor, and FCD associated with MTS. According to the recent literature,2–6,12–16 our findings suggest that different pathological subtypes are associated with different postsurgery seizure outcomes. The analysis of seizure outcome in histopathological subtypes of FCD showed different prognoses in the different pathological subgroups, with worse outcomes for patients with isolated FCD Type I.10

Analyzing the pathological group of MTS, we have to consider that the histopathological classification system for MTS recognizes 2 main groups—MTS Type 1a and 1b (grouped in hippocampal sclerosis [HS] Type 1 in the latest HS classification5)—and 2 atypical variants—MTS Type 2 and MTS Type 3 with a worse seizure outcome. Furthermore, in 2009 a classification system for GCP was reported,3 distinguishing among 3 different histological patterns: 1) no GCP (normal granule cell layer); 2) GCP Type 1 (substantial granule cell loss); and 3) GCP Type 2 (architectural abnormalities in the granule cell layer, mainly granule cell dispersion).3 Our findings suggested good results after surgery in patients with HS Type 1, with up to 80% of patients having Engel Class I outcomes.

Considering the presence of GCP, we observed that 2 (20%) of 10 patients without GCP were in Engel Class IA, while 12 (66.7%) of 18 patients with GCP achieved complete seizure freedom. These findings indicate better postsurgical results in patients with GCP compared with those without GCP. The decreased potential to generate neurospheres from the subgranular zone appears related to MTS and to alterations of dentate gyrus granule cells, especially in MTS Type 1b and GCP Type 1, suggesting the existence of a relationship between dentate gyrus pathology and postsurgical seizure outcome10,14 and neuropsychological outcome.7

Indeed, these histological findings may have relevant prognostic implications in seizure and neuropsychological outcomes for patients with HS compared to patients with other epileptogenic temporal lobe lesions (such as FCD, glioneuronal tumors, or vascular lesions). In our opinion, with the adoption of the more recent pathological classification systems,2–6,15 some subgroups of histological abnormalities influencing outcomes have emerged and should be considered among factors predictive of seizure outcome such as the type of surgical approach and the extent of resection.

This approach is also in agreement with the recent suggestions of the International League Against Epilepsy (ILAE) Commission on Classifications and Terminology1—that is, to put more emphasis on the underlying pathological substrate in the assessment of postsurgical seizure outcome and in future epilepsy classifications.

Disclosure

The authors report no conflict of interest.

References

  • 1

    Berg ATBerkovic SFBrodie MJBuchhalter JCross JHvan Emde Boas W: Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE Commission on Classification and Terminology, 2005–2009. Epilepsia 51:6766852010

  • 2

    Blümcke ICoras RMiyata HOzkara C: Defining cliniconeuropathological subtypes of mesial temporal lobe epilepsy with hippocampal sclerosis. Brain Pathol 22:4024112012

  • 3

    Blümcke IKistner IClusmann HSchramm JBecker AJElger CE: Towards a clinico-pathological classification of granule cell dispersion in human mesial temporal lobe epilepsies. Acta Neuropathol 117:5355442009

  • 4

    Blümcke IPauli EClusmann HSchramm JBecker AElger C: A new clinico-pathological classification system for mesial temporal sclerosis. Acta Neuropathol 113:2352442007

  • 5

    Blümcke IThom MAronica EArmstrong DDBartolomei FBernasconi A: International consensus classification of hippocampal sclerosis in temporal lobe epilepsy: a Task Force report from the ILAE Commission on Diagnostic Methods. Epilepsia 54:131513292013

  • 6

    Blümcke IThom MAronica EArmstrong DDVinters HVPalmini A: The clinicopathologic spectrum of focal cortical dysplasias: a consensus classification proposed by an ad hoc Task Force of the ILAE Diagnostic Methods Commission. Epilepsia 52:1581742011

  • 7

    Coras RSiebzehnrubl FAPauli EHuttner HBNjunting MKobow K: Low proliferation and differentiation capacities of adult hippocampal stem cells correlate with memory dysfunction in humans. Brain 133:335933722010

  • 8

    da Costa Neves RSJardim APCaboclo LOLancellotti CMarinho TFHamad AP: Granule cell dispersion is not a predictor of surgical outcome in temporal lobe epilepsy with mesial temporal sclerosis. Clin Neuropathol 32:24302013

  • 9

    Engel J JrVan Ness PRasmussen TBOjemann LMOutcome with respect to epileptic seizures. Engel J Jr: Surgical Treatment of the Epilepsies ed 2New YorkRaven Press1993. 609621

  • 10

    Giulioni MMarucci GMartinoni MVolpi LRiguzzi PMarliani AF: Seizure outcome in surgically treated drug-resistant mesial temporal lobe epilepsy based on the recent histopathological classifications. Clinical article. J Neurosurg 119:37472013

  • 11

    Hu WHZhang CZhang KMeng FGChen NZhang JG: Selective amygdalohippocampectomy versus anterior temporal lobectomy in the management of mesial temporal lobe epilepsy: a meta-analysis of comparative studies. A systematic review. J Neurosurg 119:108910972013

  • 12

    Marucci G: Commentary on patterns of hippocampal sclerosis as predictors of postsurgical outcome. Epilepsia 52:6526532011. (Letter)

  • 13

    Marucci GGiulioni MRubboli GParadisi MFernández MDel Vecchio G: Neurogenesis in temporal lobe epilepsy: relationship between histological findings and changes in dentate gyrus proliferative properties. Clin Neurol Neurosurg 115:1871912013

  • 14

    Marucci GRubboli GGiulioni M: Role of dentate gyrus alterations in mesial temporal sclerosis. Clin Neuropathol 29:32352010

  • 15

    Thom MBlümcke IAronica E: Long-term epilepsy-associated tumors. Brain Pathol 22:3503792012

  • 16

    Thom MLiagkouras IElliot KJMartinian LHarkness WMcEvoy A: Reliability of patterns of hippocampal sclerosis as predictors of postsurgical outcome. Epilepsia 51:180118082010

Response

We thank Dr. Giulioni and colleagues for their constructive comments on our study. We also agree with them that pathological substrate is essential to predict seizure outcome after temporal lobe epilepsy (TLE) surgery. However, since pathological results were absent in some studies reported in the literature1,2,8,9 or an FCD diagnosis could not be made in one old study,6 it was difficult to extract adequate pathological data from the studies included in our meta-analysis.

In TLE patients, most isolated FCD lesions are located in the neocortex, and thus they are rarely found in specimens from patients undergoing selective amygdalohippocampectomy (SelAH). This means that isolated FCD is more likely to be diagnosed in an anterior temporal lobectomy (ATL) group than in an SelAH group. The study by Giulioni et al. suggested that isolated FCD was a poor predictor of seizure outcome in TLE patients.5 Our meta-analysis indicated that although it was less frequently performed in patients with isolated FCD, patients undergoing SelAH showed statistically lower odds of being seizure free than those undergoing ATL. Based on the aforementioned findings, the conclusion could be made that the 2 different surgical procedures may produce different seizure outcomes.

In addition to the pathological substrate, other factors such as major depressive disorder,4 extratemporal cortical hypometabolism,3 and epilepsy duration7 were also considered as postoperative seizure outcome predictors in TLE. Randomized grouping is essential to alleviate outcome biases induced by the aforementioned factors. As we recommended in our article, well-designed randomized trials with a sufficient sample size are needed to compare SelAH and ATL in terms of seizure outcome, IQ scores, memory, language ability, visual deficits, and other complications or adverse effects.

References

  • 1

    Assaf BAKarkar KMLaxer KDGarcia PAAustin EJBarbaro NM: Magnetoencephalography source localization and surgical outcome in temporal lobe epilepsy. Clin Neurophysiol 115:206620762004

  • 2

    Bate HEldridge PVarma TWieshmann UC: The seizure outcome after amygdalohippocampectomy and temporal lobectomy. Eur J Neurol 14:90942007. (Erratum in Eur J Neurol 14: 476 2007)

  • 3

    Choi JYKim SJHong SBSeo DWHong SCKim BT: Extratemporal hypometabolism on FDG PET in temporal lobe epilepsy as a predictor of seizure outcome after temporal lobectomy. Eur J Nucl Med Mol Imaging 30:5815872003

  • 4

    de Araujo Filho GMGomes FLMazetto LMarinho MMTavares IMCaboclo LO: Major depressive disorder as a predictor of a worse seizure outcome one year after surgery in patients with temporal lobe epilepsy and mesial temporal sclerosis. Seizure 21:6196232012

  • 5

    Giulioni MMarucci GMartinoni MVolpi LRiguzzi PMarliani AF: Seizure outcome in surgically treated drug-resistant mesial temporal lobe epilepsy based on the recent histopathological classifications. Clinical article. J Neurosurg 119:37472013

  • 6

    Mackenzie RAMatheson JEllis MKlamus J: Selective versus non-selective temporal lobe surgery for epilepsy. J Clin Neurosci 4:1521541997

  • 7

    McIntosh AMKalnins RMMitchell LAFabinyi GCBriellmann RSBerkovic SF: Temporal lobectomy: long-term seizure outcome, late recurrence and risks for seizure recurrence. Brain 127:201820302004

  • 8

    Renowden SAMatkovic ZAdams CBCarpenter KOxbury SMolyneux AJ: Selective amygdalohippocampectomy for hippocampal sclerosis: postoperative MR appearance. AJNR Am J Neuroradiol 16:185518611995

  • 9

    Tanriverdi TOlivier APoulin NAndermann FDubeau F: Long-term seizure outcome after mesial temporal lobe epilepsy surgery: corticalamygdalohippocampectomy versus selective amygdalohippocampectomy. J Neurosurg 108:5175242008

If the inline PDF is not rendering correctly, you can download the PDF file here.

Article Information

Please include this information when citing this paper: published online January 10, 2014; DOI: 10.3171/2013.10.JNS132161.

© AANS, except where prohibited by US copyright law.

Headings

References

  • 1

    Berg ATBerkovic SFBrodie MJBuchhalter JCross JHvan Emde Boas W: Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE Commission on Classification and Terminology, 2005–2009. Epilepsia 51:6766852010

  • 2

    Blümcke ICoras RMiyata HOzkara C: Defining cliniconeuropathological subtypes of mesial temporal lobe epilepsy with hippocampal sclerosis. Brain Pathol 22:4024112012

  • 3

    Blümcke IKistner IClusmann HSchramm JBecker AJElger CE: Towards a clinico-pathological classification of granule cell dispersion in human mesial temporal lobe epilepsies. Acta Neuropathol 117:5355442009

  • 4

    Blümcke IPauli EClusmann HSchramm JBecker AElger C: A new clinico-pathological classification system for mesial temporal sclerosis. Acta Neuropathol 113:2352442007

  • 5

    Blümcke IThom MAronica EArmstrong DDBartolomei FBernasconi A: International consensus classification of hippocampal sclerosis in temporal lobe epilepsy: a Task Force report from the ILAE Commission on Diagnostic Methods. Epilepsia 54:131513292013

  • 6

    Blümcke IThom MAronica EArmstrong DDVinters HVPalmini A: The clinicopathologic spectrum of focal cortical dysplasias: a consensus classification proposed by an ad hoc Task Force of the ILAE Diagnostic Methods Commission. Epilepsia 52:1581742011

  • 7

    Coras RSiebzehnrubl FAPauli EHuttner HBNjunting MKobow K: Low proliferation and differentiation capacities of adult hippocampal stem cells correlate with memory dysfunction in humans. Brain 133:335933722010

  • 8

    da Costa Neves RSJardim APCaboclo LOLancellotti CMarinho TFHamad AP: Granule cell dispersion is not a predictor of surgical outcome in temporal lobe epilepsy with mesial temporal sclerosis. Clin Neuropathol 32:24302013

  • 9

    Engel J JrVan Ness PRasmussen TBOjemann LMOutcome with respect to epileptic seizures. Engel J Jr: Surgical Treatment of the Epilepsies ed 2New YorkRaven Press1993. 609621

  • 10

    Giulioni MMarucci GMartinoni MVolpi LRiguzzi PMarliani AF: Seizure outcome in surgically treated drug-resistant mesial temporal lobe epilepsy based on the recent histopathological classifications. Clinical article. J Neurosurg 119:37472013

  • 11

    Hu WHZhang CZhang KMeng FGChen NZhang JG: Selective amygdalohippocampectomy versus anterior temporal lobectomy in the management of mesial temporal lobe epilepsy: a meta-analysis of comparative studies. A systematic review. J Neurosurg 119:108910972013

  • 12

    Marucci G: Commentary on patterns of hippocampal sclerosis as predictors of postsurgical outcome. Epilepsia 52:6526532011. (Letter)

  • 13

    Marucci GGiulioni MRubboli GParadisi MFernández MDel Vecchio G: Neurogenesis in temporal lobe epilepsy: relationship between histological findings and changes in dentate gyrus proliferative properties. Clin Neurol Neurosurg 115:1871912013

  • 14

    Marucci GRubboli GGiulioni M: Role of dentate gyrus alterations in mesial temporal sclerosis. Clin Neuropathol 29:32352010

  • 15

    Thom MBlümcke IAronica E: Long-term epilepsy-associated tumors. Brain Pathol 22:3503792012

  • 16

    Thom MLiagkouras IElliot KJMartinian LHarkness WMcEvoy A: Reliability of patterns of hippocampal sclerosis as predictors of postsurgical outcome. Epilepsia 51:180118082010

  • 1

    Assaf BAKarkar KMLaxer KDGarcia PAAustin EJBarbaro NM: Magnetoencephalography source localization and surgical outcome in temporal lobe epilepsy. Clin Neurophysiol 115:206620762004

  • 2

    Bate HEldridge PVarma TWieshmann UC: The seizure outcome after amygdalohippocampectomy and temporal lobectomy. Eur J Neurol 14:90942007. (Erratum in Eur J Neurol 14: 476 2007)

  • 3

    Choi JYKim SJHong SBSeo DWHong SCKim BT: Extratemporal hypometabolism on FDG PET in temporal lobe epilepsy as a predictor of seizure outcome after temporal lobectomy. Eur J Nucl Med Mol Imaging 30:5815872003

  • 4

    de Araujo Filho GMGomes FLMazetto LMarinho MMTavares IMCaboclo LO: Major depressive disorder as a predictor of a worse seizure outcome one year after surgery in patients with temporal lobe epilepsy and mesial temporal sclerosis. Seizure 21:6196232012

  • 5

    Giulioni MMarucci GMartinoni MVolpi LRiguzzi PMarliani AF: Seizure outcome in surgically treated drug-resistant mesial temporal lobe epilepsy based on the recent histopathological classifications. Clinical article. J Neurosurg 119:37472013

  • 6

    Mackenzie RAMatheson JEllis MKlamus J: Selective versus non-selective temporal lobe surgery for epilepsy. J Clin Neurosci 4:1521541997

  • 7

    McIntosh AMKalnins RMMitchell LAFabinyi GCBriellmann RSBerkovic SF: Temporal lobectomy: long-term seizure outcome, late recurrence and risks for seizure recurrence. Brain 127:201820302004

  • 8

    Renowden SAMatkovic ZAdams CBCarpenter KOxbury SMolyneux AJ: Selective amygdalohippocampectomy for hippocampal sclerosis: postoperative MR appearance. AJNR Am J Neuroradiol 16:185518611995

  • 9

    Tanriverdi TOlivier APoulin NAndermann FDubeau F: Long-term seizure outcome after mesial temporal lobe epilepsy surgery: corticalamygdalohippocampectomy versus selective amygdalohippocampectomy. J Neurosurg 108:5175242008

TrendMD

Metrics

Metrics

All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 124 124 4
PDF Downloads 57 57 1
EPUB Downloads 0 0 0

PubMed

Google Scholar