Letter to the Editor: Anterior temporal lobectomy

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To The Editor: We have read with great interest the paper by Elliott et al.8 (Elliott RE, Bollo RJ, Berliner JL, et al: Anterior temporal lobectomy with amygdalohippocampectomy for mesial temporal sclerosis: predictors of long-term seizure control. Clinical article. J Neurosurg 119:261–272, August 2013). The authors' study is an effort to identify the predictors of long-term seizure control after anterior temporal lobectomy with amygdalohippocampectomy in patients affected by pharmacoresistant temporal lobe epilepsy associated with mesial temporal sclerosis (MTS). First of all, the authors should be congratulated on their excellent epilepsy outcomes (89% modified Engel Class I at 6.7 years of median follow-up) in a homogeneous study of pharmacoresistant temporal lobe epilepsy associated with MTS. We agree with the authors about the importance of identifying factors that predict seizure outcome in epilepsy surgery. However, we think that more attention should be paid to the histological pattern facing the following issues.

Besides the clinical, neurophysiological, and imaging factors, the underlying histological type and subtype of MTS affecting the hippocampus and dentate gyrus have emerged as having an increasing role in seizure outcome in the last years.2–5,7,10–13 Seizure prognosis in patients undergoing epilepsy surgery for MTS has been hypothesized to depend on either the subtype of hippocampal sclerosis4,5,13 or the status of the dentate gyrus, namely the absence or presence of granule cell pathology (GCP).3,12 Indeed, the histopathological classification system for MTS recognizes 2 main groups, MTS Type 1a and 1b (grouped into MTS Type 1 in the latest hippocampal sclerosis classification),5 and 2 atypical variants, MTS Type 2 and Type 3, with a worse seizure outcome. Furthermore, in 2009 a classification system for GCP was elaborated,3 distinguishing 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

In our retrospective study10 about seizure outcomes in drug-resistant mesial temporal lobe epilepsy,8 in which we analyzed an MTS group as a whole, seizure outcome was optimal, with Engel Class I9 outcomes in 82% of cases (although Engel Class IA outcomes occurred in only 50%), whereas Engel Class II outcomes occurred in the remaining 18%. The various outcome classes were scattered among the different MTS subtypes. Regarding the 14 patients with the best outcome, Engel Class IA was attained in 11 (61%) of 18 patients with MTS Type 1a (with or without GCP), in 2 (40%) of 5 patients with MTS Type 1b, and in 1 (20%) of 5 patients with MTS Type 2. Our findings suggested good results after surgery in patients with MTS Types 1a and 1b (MTS Type 1 in the latest hippocampal sclerosis classification), 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 attained complete seizure freedom. These findings indicated better postsurgical results in patients with GCP than in those without GCP. The demonstration that a decreased potential to generate neurospheres from the subgranular zone is related to MTS and to alterations of dentate gyrus granule cells, especially in MTS Type 1b and GCP Type 1, suggests the existence of a relationship between dentate gyrus pathology and postsurgical seizure outcome11,12 and neuropsychological outcome.6 Indeed, these histological findings may have relevant prognostic implications in seizure and neuropsychological outcomes in patients affected by hippocampal sclerosis as compared with patients with other epileptogenic lesions (such as focal cortical dysplasia [FCD], glioneuronal tumors, or vascular lesions).

In our opinion, with the adoption of the more recent neuropathological classification systems,2–5 some subgroups of pathological abnormalities conditioning outcomes have emerged and have to be considered among the factors predictive of seizure outcome. We suggest that the recognition of the different subgroups of pathological conditions associated with different seizure outcomes should stimulate the investigation of the specific epileptogenic mechanisms, relating outcome mainly to the pathological substrate. This approach is also in agreement with the recent suggestions of the International League Against Epilepsy (ILAE) Commission on Classifications and Terminology1 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 clinico-neuropathological 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

    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

  • 7

    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

  • 8

    Elliott REBollo RJBerliner JLSilverberg ACarlson CGeller EB: Anterior temporal lobectomy with amygdalohippocampectomy for mesial temporal sclerosis: predictors of long-term seizure control. Clinical article. J Neurosurg 119:2612722013

  • 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

    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

  • 12

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

  • 13

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

Response

We thank the authors for their insightful comments. Their work and remarks certainly coincide with the direction in which the field is heading. In truth, we did a preliminary analysis of pathological findings in our series, but sufficient detail was not available for subclassification in the clinical reports. We plan to conduct a blinded review of the pathology findings using the current classification systems to correlate such findings with seizure control.

There are 2 major shortcomings of postoperative pathological analyses, however. First, there is currently no way to know the pathology classification before surgery. Therefore, this information cannot be used to guide therapy or prognosticate. To fully realize the benefits of correlative studies between subclassification of MTS pathology and outcomes, viable presurgical biomarkers are necessary. Such biomarkers would allow for a priori prognostication on outcomes, thus providing better presurgical counseling to patients and families.

The second limitation of postoperative pathological analysis is that we do not know what is left behind after resection. As Daniel Kahneman notes in Thinking, Fast and Slow, “what you see is all there is.” What may be more critical to failures in epilepsy surgery is not what is seen, but what is left unseen or left behind. Thus, the pathological correlate for a poor surgical outcome may relate to the pathology available for analysis, the unresected margins, or even distant regions.

The purpose of our study was to analyze our own methods of patient selection for single- or multistage epilepsy surgery for MTS to determine if our criteria were sound. We believe such results may help surgeons determine who is best suited for single-stage surgery. We congratulate the advancement made in pathological analysis to help us further understand this disease and welcome new advancements to make the treatment of MTS more successful and safe.

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Article Information

Please include this information when citing this paper: published online January 3, 2014; DOI: 10.3171/2013.8.JNS131785.

© 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 clinico-neuropathological 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

    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

  • 7

    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

  • 8

    Elliott REBollo RJBerliner JLSilverberg ACarlson CGeller EB: Anterior temporal lobectomy with amygdalohippocampectomy for mesial temporal sclerosis: predictors of long-term seizure control. Clinical article. J Neurosurg 119:2612722013

  • 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

    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

  • 12

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

  • 13

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

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