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The Effect of Neocortical Pathology on Lateralization and Seizure Outcome in Lobectomy Materials in Surgically Treated Hippocampal Sclerosis Patients

Year 2019, Volume: 33 Issue: 1, 69 - 81, 26.04.2019
https://doi.org/10.5505/deutfd.2019.08379

Abstract

INTRODUCTION: The aim of this study was to investigate the effect of histopathological neocortical pathology on lateralization and surgical seizure in patients with temporal epilepsy, resistant temporal epilepsy and hippocampal sclerosis.
METHODS: In our clinic, from 2008 to 2016, 18 patients with resistant temporal lobe epilepsy and hippocampal sclerosis were included in the study.
RESULTS: Thirteen patients (72.2%) right side, 5 patients (27.8%) left side amygdalohipocampectomy + anterior temporal lobectomy procedure was performed. Neocortical pathology was found histopathologically in 11 patients (61.1%) and normal in 7 patients (38.9%). Six (33.3%) of the neocortical pathology were microdisgenesia and 5 (27.8%) were cortical dysplasia. The effect of preoperative examination on lateralization was investigated according to neocortical pathology and normalization of seizure semiology (78.4%) was statistically significant (p = 0.019). The best investigations for lateralization waere cranial MRI (94.5%) and ictal EEG (94.5%). PET (83.3%) investigation was found to contribute to lateralization. Early onset seizures were remarkable in patients with neocortical pathology. In the first 5 years after surgery,according to Engel classification, 83.3% grade 1, 11.1% grade 2, 5.6% grade 3 seizure rates were obtained. There were no statistically significant differences between the patients with neocortical pathology and those with normal surgical results.
DISCUSSION AND CONCLUSION: In our study we found that the rate of pathology in neocortical tissue is high in patients with hippocampal sclerosis. This result, supports the standard temporal lobectomy surgical procedure. More studies are needed to determine the effect of the presence of pathology on lateralization value, epileptogenesis and surgical outcomes.

References

  • Bell GS, Neligan A, Sander JW. An unknown quantity--the worldwide prevalence of epilepsy. Epilepsia. 2014;55:958-962.
  • Engel J, Jr. Introduction to temporal lobe epilepsy. Epilepsy Res. 1996;26:141-150.
  • Wiebe S, Blume WT, Girvin JP, Eliasziw M, Effectiveness, Efficiency of Surgery for Temporal Lobe Epilepsy Study G. A randomized, controlled trial of surgery for temporal-lobe epilepsy. N Engl J Med. 2001;345:311-318.
  • Alvim MK, Coan AC, Campos BM et al. Progression of gray matter atrophy in seizure-free patients with temporal lobe epilepsy. Epilepsia. 2016;57:621-629.
  • Vaughan DN, Rayner G, Tailby C, Jackson GD. MRI-negative temporal lobe epilepsy: A network disorder of neocortical connectivity. Neurology. 2016;87:1934-1942.
  • Choi D, Na DG, Byun HS et al. White-matter change in mesial temporal sclerosis: correlation of MRI with PET, pathology, and clinical features. Epilepsia. 1999;40:1634-1641.
  • Eriksson SH, Free SL, Thom M, Harkness W, Sisodiya SM, Duncan JS. Reliable registration of preoperative MRI with histopathology after temporal lobe resections. Epilepsia. 2005;46:1646-1653.
  • Meiners LC, Witkamp TD, de Kort GA et al. Relevance of temporal lobe white matter changes in hippocampal sclerosis. Magnetic resonance imaging and histology. Invest Radiol. 1999;34:38-45.
  • Cormack F, Gadian DG, Vargha-Khadem F, Cross JH, Connelly A, Baldeweg T. Extra-hippocampal grey matter density abnormalities in paediatric mesial temporal sclerosis. Neuroimage. 2005;27:635-643.
  • Keller SS, Roberts N. Voxel-based morphometry of temporal lobe epilepsy: an introduction and review of the literature. Epilepsia. 2008;49:741-757.
  • Labate A, Cerasa A, Aguglia U, Mumoli L, Quattrone A, Gambardella A. Voxel-based morphometry of sporadic epileptic patients with mesiotemporal sclerosis. Epilepsia. 2010;51:506-510.
  • Nishio S, Morioka T, Hisada K, Fukui M. Temporal lobe epilepsy: a clinicopathological study with special reference to temporal neocortical changes. Neurosurg Rev. 2000;23:84-89.
  • Schramm J, Clusmann H. The surgery of epilepsy. Neurosurgery. 2008;62:463-481
  • Falconer MA, Serafetinides EA. A follow-up study of surgery in temporal lobe epilepsy. J Neurol Neurosurg Psychiatry. 1963;26:154-165.
  • Wieser HG, Yasargil MG. Selective amygdalohippocampectomy as a surgical treatment of mesiobasal limbic epilepsy. Surg Neurol. 1982;17:445-457.
  • Bernhardt BC, Bernasconi N, Concha L, Bernasconi A. Cortical thickness analysis in temporal lobe epilepsy: reproducibility and relation to outcome. Neurology. 2010;74:1776-1784.
  • Engel J, Jr. Surgery for seizures. N Engl J Med. 1996;334:647-652.
  • Cavanagh JB, Meyer A. Aetiological aspects of Ammon's horn sclerosis associated with temporal lobe epilepsy. Br Med J. 1956;2:1403-1407.
  • Meyer A, Beck E. The hippocampal formation in temporal lobe epilepsy. Proc R Soc Med. 1955;48:457-462.
  • Thom M, Eriksson S, Martinian L et al. Temporal lobe sclerosis associated with hippocampal sclerosis in temporal lobe epilepsy: neuropathological features. J Neuropathol Exp Neurol. 2009;68:928-938.
  • Blanc F, Martinian L, Liagkouras I, Catarino C, Sisodiya SM, Thom M. Investigation of widespread neocortical pathology associated with hippocampal sclerosis in epilepsy: a postmortem study. Epilepsia. 2011;52:10-21.
  • Jensen I. Temporal lobe epilepsy. Late mortality in patients treated with unilateral temporal lobe resections. Acta Neurol Scand. 1975;52:374-380.
  • Hardiman O, Burke T, Phillips J et al. Microdysgenesis in resected temporal neocortex: incidence and clinical significance in focal epilepsy. Neurology. 1988;38:1041-1047.
  • Taylor DC, Falconer MA, Bruton CJ, Corsellis JA. Focal dysplasia of the cerebral cortex in epilepsy. J Neurol Neurosurg Psychiatry. 1971;34:369-387.
  • Ho SS, Kuzniecky RI, Gilliam F, Faught E, Morawetz R. Temporal lobe developmental malformations and epilepsy: dual pathology and bilateral hippocampal abnormalities. Neurology. 1998;50:748-754.
  • Kuzniecky R, Garcia JH, Faught E, Morawetz RB. Cortical dysplasia in temporal lobe epilepsy: magnetic resonance imaging correlations. Ann Neurol. 1991;29:293-298.
  • Martinoni M, Marucci G, Rubboli G et al. Focal cortical dysplasias in temporal lobe epilepsy surgery: Challenge in defining unusual variants according to the last ILAE classification. Epilepsy Behav. 2015;45:212-216.
  • Wolf HK, Campos MG, Zentner J et al. Surgical pathology of temporal lobe epilepsy. Experience with 216 cases. J Neuropathol Exp Neurol. 1993;52:499-506.
  • Whelan CD, Altmann A, Botia JA et al. Structural brain abnormalities in the common epilepsies assessed in a worldwide ENIGMA study. Brain. 2018;141:391-408.
  • Paglioli E, Palmini A, Portuguez M et al. Seizure and memory outcome following temporal lobe surgery: selective compared with nonselective approaches for hippocampal sclerosis. J Neurosurg. 2006;104:70-78.
  • Mackenzie RA, Matheson J, Ellis M, Klamus J. Selective versus non-selective temporal lobe surgery for epilepsy. J Clin Neurosci. 1997;4:152-154.
  • Alonso-Vanegas MA, Freire Carlier ID, San-Juan D, Martinez AR, Trenado C. Parahippocampectomy as a New Surgical Approach to Mesial Temporal Lobe Epilepsy Caused By Hippocampal Sclerosis: A Pilot Randomized Comparative Clinical Trial. World Neurosurg. 2018;110:1063-1071.
  • Schramm J, Lehmann TN, Zentner J et al. Randomized controlled trial of 2.5-cm versus 3.5-cm mesial temporal resection in temporal lobe epilepsy--Part 1: intent-to-treat analysis. Acta Neurochir (Wien). 2011;153:209-219.
  • McIntosh AM, Wilson SJ, Berkovic SF. Seizure outcome after temporal lobectomy: current research practice and findings. Epilepsia. 2001;42:1288-1307.
  • Erdem A, Sarılar C, Bilir E, Serdaroğlu A, Çapraz İY. Dirençli Temporal Lob Epilepsisinde Cerrahi Tedavi. Turkiye Klinikleri J Surg Med Sci. 2007;3:50-56.
  • Blumcke I, Pauli E, Clusmann H et al. A new clinico-pathological classification system for mesial temporal sclerosis. Acta Neuropathol. 2007;113:235-244.
  • Duncan JS. Selecting patients for epilepsy surgery: synthesis of data. Epilepsy Behav. 2011;20:230-232.
  • Uysal Aİ, Erdoğan E, Gökçil Z. Epilepsi Cerrahisi Uygulanmış Hastalarda Klinik Spektrum, Nöbet Sonuçları, Nöroradyoloji ve Nöropatoloji Korelasyonunun İncelenmesi. Epilepsi. 2013;19:63-70.
  • Dworetzky BA, Reinsberger C. The role of the interictal EEG in selecting candidates for resective epilepsy surgery. Epilepsy Behav. 2011;20:167-171.
  • Tellez-Zenteno JF, Hernandez Ronquillo L, Moien-Afshari F, Wiebe S. Surgical outcomes in lesional and non-lesional epilepsy: a systematic review and meta-analysis. Epilepsy Res. 2010;89:310-318.
  • So EL. Role of neuroimaging in the management of seizure disorders. Mayo Clin Proc. 2002;77:1251-1264.
  • Struck AF, Hall LT, Floberg JM, Perlman SB, Dulli DA. Surgical decision making in temporal lobe epilepsy: a comparison of [(18)F] FDG-PET, MRI, and EEG. Epilepsy Behav. 2011;22:293-297.

Cerrahi Olarak Tedavi Edilmiş Hipokampal Sklerozlu Hastalarda Lobektomi Materyallerindeki Neokortikal Patoloji Varlığının Lateralizasyona ve Nöbete Etkisi

Year 2019, Volume: 33 Issue: 1, 69 - 81, 26.04.2019
https://doi.org/10.5505/deutfd.2019.08379

Abstract


GİRİŞ ve AMAÇ: Hipokampal sklerozlu dirençli temporal epilepsili, standart temporal lobektomi uygulanmış olguların histopatolojik neokortikal patoloji varlığının lateralizasyon ve cerrahi nöbetsizliğe etkisini retrospektif olarak araştırmaktır.
YÖNTEM ve GEREÇLER: Kliniğimizde 2008-2016 yılları arasında epilepsi cerrahisi uygulanmış olgular arasından dirençli temporal lob epilepsili, radyolojik ve histopatolojik olarak hipokampal sklerozlu 18 olgu çalışmaya dahil edilmiştir.
BULGULAR: Onüç olguya (%72.2) sağ, 5 olguya (% 27.8) sol taraf amigdalohipokampektomi + anterior temporal lobektomi prosedürü uygulandı. Onbir olguda (%61.1) neokortikal patoloji histopatolojik olarak tespit edilmiş, 7 olgu (%38.9) ise normal bulunmuştur. Neokortikal patolojinin 6’sı (%33.3) mikrodisgenezi, 5’i (%27.8) kortikal displazi idi. Neokortikal patoloji varlığının normal olan olgulara göre preoperatif incelemelerin lateralizasyona etkisi araştırılmış ve nöbet semiyolojisinin lateralize edilmesinde (%78.4) istatistiksel anlamlı farklılık (p=0,019) bulunmuştur. En iyi lateralize eden incelemelerin ise kranial MRG (%94.5) ve iktal EEG (%94.5) olduğu, PET’in yüksek oranda (%83.3) lateralizasyona katkısı olduğu görülmüştür. Neokortikal patolojisi olan olgularda erken yaşta nöbet başlangıcı ise dikkat çekiciydi. Cerrahi sonrası ilk 5 yılda Engel sınflamasına göre, ilk 5 yılda %83,3 derece 1, %11,1 derece 2, %5,6 derece 3 nöbetsizlik oranları elde edildi. Cerrahi sonuç açısından neokortikal patoloji olan ve normal olan olgular arasında istatistiksel anlamlı fark bulunmadı.
TARTIŞMA ve SONUÇ: Hipokampal sklerozlu olgularda neokortikal dokuda patoloji varlığının oranının yüksek olduğu görülmektedir. Bu sonuç standart temporal lobektomi cerrahi prosedürünü desteklemektedir. Patoloji varlığının ön incelemelerin lateralizasyon değerine, epileptogenezise ve cerrahi sonuçlara etkisini tespit edebilmek için daha fazla sayıda olguda çalışmaya ihtiyaç vardır. 

References

  • Bell GS, Neligan A, Sander JW. An unknown quantity--the worldwide prevalence of epilepsy. Epilepsia. 2014;55:958-962.
  • Engel J, Jr. Introduction to temporal lobe epilepsy. Epilepsy Res. 1996;26:141-150.
  • Wiebe S, Blume WT, Girvin JP, Eliasziw M, Effectiveness, Efficiency of Surgery for Temporal Lobe Epilepsy Study G. A randomized, controlled trial of surgery for temporal-lobe epilepsy. N Engl J Med. 2001;345:311-318.
  • Alvim MK, Coan AC, Campos BM et al. Progression of gray matter atrophy in seizure-free patients with temporal lobe epilepsy. Epilepsia. 2016;57:621-629.
  • Vaughan DN, Rayner G, Tailby C, Jackson GD. MRI-negative temporal lobe epilepsy: A network disorder of neocortical connectivity. Neurology. 2016;87:1934-1942.
  • Choi D, Na DG, Byun HS et al. White-matter change in mesial temporal sclerosis: correlation of MRI with PET, pathology, and clinical features. Epilepsia. 1999;40:1634-1641.
  • Eriksson SH, Free SL, Thom M, Harkness W, Sisodiya SM, Duncan JS. Reliable registration of preoperative MRI with histopathology after temporal lobe resections. Epilepsia. 2005;46:1646-1653.
  • Meiners LC, Witkamp TD, de Kort GA et al. Relevance of temporal lobe white matter changes in hippocampal sclerosis. Magnetic resonance imaging and histology. Invest Radiol. 1999;34:38-45.
  • Cormack F, Gadian DG, Vargha-Khadem F, Cross JH, Connelly A, Baldeweg T. Extra-hippocampal grey matter density abnormalities in paediatric mesial temporal sclerosis. Neuroimage. 2005;27:635-643.
  • Keller SS, Roberts N. Voxel-based morphometry of temporal lobe epilepsy: an introduction and review of the literature. Epilepsia. 2008;49:741-757.
  • Labate A, Cerasa A, Aguglia U, Mumoli L, Quattrone A, Gambardella A. Voxel-based morphometry of sporadic epileptic patients with mesiotemporal sclerosis. Epilepsia. 2010;51:506-510.
  • Nishio S, Morioka T, Hisada K, Fukui M. Temporal lobe epilepsy: a clinicopathological study with special reference to temporal neocortical changes. Neurosurg Rev. 2000;23:84-89.
  • Schramm J, Clusmann H. The surgery of epilepsy. Neurosurgery. 2008;62:463-481
  • Falconer MA, Serafetinides EA. A follow-up study of surgery in temporal lobe epilepsy. J Neurol Neurosurg Psychiatry. 1963;26:154-165.
  • Wieser HG, Yasargil MG. Selective amygdalohippocampectomy as a surgical treatment of mesiobasal limbic epilepsy. Surg Neurol. 1982;17:445-457.
  • Bernhardt BC, Bernasconi N, Concha L, Bernasconi A. Cortical thickness analysis in temporal lobe epilepsy: reproducibility and relation to outcome. Neurology. 2010;74:1776-1784.
  • Engel J, Jr. Surgery for seizures. N Engl J Med. 1996;334:647-652.
  • Cavanagh JB, Meyer A. Aetiological aspects of Ammon's horn sclerosis associated with temporal lobe epilepsy. Br Med J. 1956;2:1403-1407.
  • Meyer A, Beck E. The hippocampal formation in temporal lobe epilepsy. Proc R Soc Med. 1955;48:457-462.
  • Thom M, Eriksson S, Martinian L et al. Temporal lobe sclerosis associated with hippocampal sclerosis in temporal lobe epilepsy: neuropathological features. J Neuropathol Exp Neurol. 2009;68:928-938.
  • Blanc F, Martinian L, Liagkouras I, Catarino C, Sisodiya SM, Thom M. Investigation of widespread neocortical pathology associated with hippocampal sclerosis in epilepsy: a postmortem study. Epilepsia. 2011;52:10-21.
  • Jensen I. Temporal lobe epilepsy. Late mortality in patients treated with unilateral temporal lobe resections. Acta Neurol Scand. 1975;52:374-380.
  • Hardiman O, Burke T, Phillips J et al. Microdysgenesis in resected temporal neocortex: incidence and clinical significance in focal epilepsy. Neurology. 1988;38:1041-1047.
  • Taylor DC, Falconer MA, Bruton CJ, Corsellis JA. Focal dysplasia of the cerebral cortex in epilepsy. J Neurol Neurosurg Psychiatry. 1971;34:369-387.
  • Ho SS, Kuzniecky RI, Gilliam F, Faught E, Morawetz R. Temporal lobe developmental malformations and epilepsy: dual pathology and bilateral hippocampal abnormalities. Neurology. 1998;50:748-754.
  • Kuzniecky R, Garcia JH, Faught E, Morawetz RB. Cortical dysplasia in temporal lobe epilepsy: magnetic resonance imaging correlations. Ann Neurol. 1991;29:293-298.
  • Martinoni M, Marucci G, Rubboli G et al. Focal cortical dysplasias in temporal lobe epilepsy surgery: Challenge in defining unusual variants according to the last ILAE classification. Epilepsy Behav. 2015;45:212-216.
  • Wolf HK, Campos MG, Zentner J et al. Surgical pathology of temporal lobe epilepsy. Experience with 216 cases. J Neuropathol Exp Neurol. 1993;52:499-506.
  • Whelan CD, Altmann A, Botia JA et al. Structural brain abnormalities in the common epilepsies assessed in a worldwide ENIGMA study. Brain. 2018;141:391-408.
  • Paglioli E, Palmini A, Portuguez M et al. Seizure and memory outcome following temporal lobe surgery: selective compared with nonselective approaches for hippocampal sclerosis. J Neurosurg. 2006;104:70-78.
  • Mackenzie RA, Matheson J, Ellis M, Klamus J. Selective versus non-selective temporal lobe surgery for epilepsy. J Clin Neurosci. 1997;4:152-154.
  • Alonso-Vanegas MA, Freire Carlier ID, San-Juan D, Martinez AR, Trenado C. Parahippocampectomy as a New Surgical Approach to Mesial Temporal Lobe Epilepsy Caused By Hippocampal Sclerosis: A Pilot Randomized Comparative Clinical Trial. World Neurosurg. 2018;110:1063-1071.
  • Schramm J, Lehmann TN, Zentner J et al. Randomized controlled trial of 2.5-cm versus 3.5-cm mesial temporal resection in temporal lobe epilepsy--Part 1: intent-to-treat analysis. Acta Neurochir (Wien). 2011;153:209-219.
  • McIntosh AM, Wilson SJ, Berkovic SF. Seizure outcome after temporal lobectomy: current research practice and findings. Epilepsia. 2001;42:1288-1307.
  • Erdem A, Sarılar C, Bilir E, Serdaroğlu A, Çapraz İY. Dirençli Temporal Lob Epilepsisinde Cerrahi Tedavi. Turkiye Klinikleri J Surg Med Sci. 2007;3:50-56.
  • Blumcke I, Pauli E, Clusmann H et al. A new clinico-pathological classification system for mesial temporal sclerosis. Acta Neuropathol. 2007;113:235-244.
  • Duncan JS. Selecting patients for epilepsy surgery: synthesis of data. Epilepsy Behav. 2011;20:230-232.
  • Uysal Aİ, Erdoğan E, Gökçil Z. Epilepsi Cerrahisi Uygulanmış Hastalarda Klinik Spektrum, Nöbet Sonuçları, Nöroradyoloji ve Nöropatoloji Korelasyonunun İncelenmesi. Epilepsi. 2013;19:63-70.
  • Dworetzky BA, Reinsberger C. The role of the interictal EEG in selecting candidates for resective epilepsy surgery. Epilepsy Behav. 2011;20:167-171.
  • Tellez-Zenteno JF, Hernandez Ronquillo L, Moien-Afshari F, Wiebe S. Surgical outcomes in lesional and non-lesional epilepsy: a systematic review and meta-analysis. Epilepsy Res. 2010;89:310-318.
  • So EL. Role of neuroimaging in the management of seizure disorders. Mayo Clin Proc. 2002;77:1251-1264.
  • Struck AF, Hall LT, Floberg JM, Perlman SB, Dulli DA. Surgical decision making in temporal lobe epilepsy: a comparison of [(18)F] FDG-PET, MRI, and EEG. Epilepsy Behav. 2011;22:293-297.
There are 42 citations in total.

Details

Primary Language Turkish
Subjects Clinical Sciences
Journal Section Research Articles
Authors

Gönül Güvenç 0000-0002-9382-8610

Ceren Kızmazoğlu 0000-0001-6146-0842

Publication Date April 26, 2019
Submission Date December 4, 2018
Published in Issue Year 2019 Volume: 33 Issue: 1

Cite

Vancouver Güvenç G, Kızmazoğlu C. Cerrahi Olarak Tedavi Edilmiş Hipokampal Sklerozlu Hastalarda Lobektomi Materyallerindeki Neokortikal Patoloji Varlığının Lateralizasyona ve Nöbete Etkisi. DEU Tıp Derg. 2019;33(1):69-81.