Predictors of Class I epilepsy surgery outcome in tumour-related chronic temporal lobe epilepsy in adults
Abstract
Objective. Temporal lobe tumours, especially low-grade gliomas and glioneuronal tumours, are common causes of seizures in patients referred for epilepsy surgery. We here present our experience of surgical treatment of patients with intractable chronic epilepsy associated with temporal lobe tumours, focusing on the long-term surgical outcomes and the features associated with better seizure control.
Methods. In this study, we retrospectively analysed 44 consecutive patients from a total of 182 with refractory temporal lobe epilepsy presenting with long-term intractable epilepsy due to a temporal lobe tumour who were surgically treated at our institution between 2005 and 2015 with post-surgical follow-up of at least two years. All patients underwent a standard pre-surgical evaluation that included: history and physical examination with a description of the seizure semiology, serial scalp EEG recording, brain MR imaging, and a detailed neuropsychological evaluation. Our surgical strategy comprised tumour resection, and combined mesial temporal and neocortical resection in most cases.
Results. No patient died during surgery or the postoperative course. Seven patients had postoperative complications, of whom two had permanent hemiparesis due to ischaemic stroke. At the final follow-up, a favourable seizure outcome (Engel Class I) was found in 37 patients (84%), including 31 (70.5%) in Engel Class IA (excellent result). Two (4.5%) patients presented with an Engel Class II outcome (unfavourable outcome). Five patients (11.5%) were in Engel Classes III or IV (surgical failure). We found that complete
resection of the hippocampus along with tumour and temporal pole removal was strongly associated with seizure freedom (p = 0.015). Pathological diagnosis was also a significant prognostic indicator of tumour-related seizure freedom. Patients with a diagnosis of a glioneuronal tumour benefited from more seizure freedom after resection compared to those who had a low-grade glioma (p = 0.024).
Conclusion. The most appropriate management of tumour-related chronic temporal lobe epilepsy in adults appears to be tai-lored temporal lobe resection including tumour and hippocampal complex removal. Surgical treatment of tumoural temporal lobe epilepsy demonstrates excellent results in terms of seizure improvement, especially in patients with glioneuronal tumours.
Keywords: seizureintractable epilepsytemporal lobetumorsurgical treatment
References
- Klein M, Engelberts NHJ, van der Ploeg HM, et al. Epilepsy in low-grade gliomas: the impact on cognitive function and quality of life. Ann Neurol. 2003; 54(4): 514–520.
- Taphoorn MJB, Klein M. Cognitive deficits in adult patients with brain tumours. Lancet Neurol. 2004; 3(3): 159–168.
- Zaatreh MM, Firlik KS, Spencer DD, et al. Temporal lobe tumoral epilepsy: characteristics and predictors of surgical outcome. Neurology. 2003; 61(5): 636–641.
- Iannelli A, Guzzetta F, Battaglia D, et al. Surgical treatment of temporal tumors associated with epilepsy in children. Pediatr Neurosurg. 2000; 32(5): 248–254.
- Bourgeois M, Di Rocco F, Sainte-Rose C. Lesionectomy in the pediatric age. Childs Nerv Syst. 2006; 22(8): 931–935.
- Giulioni M, Galassi E, Zucchelli M, et al. Seizure outcome of lesionectomy in glioneuronal tumors associated with epilepsy in children. J Neurosurg. 2005; 102(3 Suppl): 288–293.
- Aronica E, Leenstra S, van Veelen CW, et al. Glioneuronal tumors and medically intractable epilepsy: a clinical study with long-term follow-up of seizure outcome after surgery. Epilepsy Res. 2001; 43(3): 179–191.
- Chan CH, Bittar RG, Davis GA, et al. Long-term seizure outcome following surgery for dysembryoplastic neuroepithelial tumor. J Neurosurg. 2006; 104(1): 62–69.
- Cossu M, Lo Russo G, Francione S, et al. Epilepsy surgery in children: results and predictors of outcome on seizures. Epilepsia. 2008; 49(1): 65–72.
- Jooma R, Yeh HS, Privitera MD, et al. Lesionectomy versus electrophysiologically guided resection for temporal lobe tumors manifesting with complex partial seizures. J Neurosurg. 1995; 83(2): 231–236.
- Luyken C, Blümcke I, Fimmers R, et al. The spectrum of long-term epilepsy-associated tumors: long-term seizure and tumor outcome and neurosurgical aspects. Epilepsia. 2003; 44(6): 822–830.
- Luyken C, Blümcke I, Fimmers R, et al. Supratentorial gangliogliomas: histopathologic grading and tumor recurrence in 184 patients with a median follow-up of 8 years. Cancer. 2004; 101(1): 146–155.
- Louis DN, Ohgaki H, Wiestler OD, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007; 114(2): 97–109.
- Blümcke I, Thom M, Aronica E, et al. The clinicopathologic spectrum of focal cortical dysplasias: a consensus classification proposed by an ad hoc Task Force of the ILAE Diagnostic Methods Commission. Epilepsia. 2011; 52(1): 158–174.
- Palmini A, Najm I, Avanzini G, et al. Terminology and classification of the cortical dysplasias. Neurology. 2004; 62(6 Suppl 3): S2–S8.
- Fischer-Williams M. Surgical treatment of the epilepsies, 2nd edition. Electroencephalography and Clinical Neurophysiology. 1994; 90(3): 249–250.
- Britton JW, Cascino GD, Sharbrough FW, et al. Low-grade glial neoplasms and intractable partial epilepsy: efficacy of surgical treatment. Epilepsia. 1994; 35(6): 1130–1135.
- Bernasconi A, Bernasconi N, Bernhardt BC, et al. Advances in MRI for 'cryptogenic' epilepsies. Nat Rev Neurol. 2011; 7(2): 99–108.
- Vogt VL, Witt JA, Delev D, et al. Cognitive features and surgical outcome of patients with long-term epilepsy-associated tumors (LEATs) within the temporal lobe. Epilepsy Behav. 2018; 88: 25–32.
- Berger MS, Ghatan S, Haglund MM, et al. Low-grade gliomas associated with intractable epilepsy: seizure outcome utilizing electrocorticography during tumor resection. J Neurosurg. 1993; 79(1): 62–69.
- Cataltepe O, Turanli G, Yalnizoglu D, et al. Surgical management of temporal lobe tumor-related epilepsy in children. J Neurosurg. 2005; 102(3 Suppl): 280–287.
- Ruban D, Byrne RW, Kanner A, et al. Chronic epilepsy associated with temporal tumors: long-term surgical outcome. Neurosurg Focus. 2009; 27(2): E6.
- Aronica E, Redeker S, Boer K, et al. Inhibitory networks in epilepsy-associated gangliogliomas and in the perilesional epileptic cortex. Epilepsy Res. 2007; 74(1): 33–44.
- Blümcke I, Wiestler OD. Gangliogliomas: an intriguing tumor entity associated with focal epilepsies. J Neuropathol Exp Neurol. 2002; 61(7): 575–584.
- Chassoux F, Daumas-Duport C. Dysembryoplastic neuroepithelial tumors: where are we now? Epilepsia. 2013; 54 Suppl 9: 129–134.
- Giulioni M, Rubboli G, Marucci G, et al. Seizure outcome of epilepsy surgery in focal epilepsies associated with temporomesial glioneuronal tumors: lesionectomy compared with tailored resection. J Neurosurg. 2009; 111(6): 1275–1282.
- Becker AJ, Blümcke I, Urbach H, et al. Molecular neuropathology of epilepsy-associated glioneuronal malformations. J Neuropathol Exp Neurol. 2006; 65(2): 99–108.
- Sasaki A, Hirato J, Nakazato Y, et al. Recurrent anaplastic ganglioglioma: pathological characterization of tumor cells. Case report. J Neurosurg. 1996; 84(6): 1055–1059.
- Wiebe S, Blume WT, Girvin JP, et al. Effectiveness and Efficiency of Surgery for Temporal Lobe Epilepsy Study Group. A randomized, controlled trial of surgery for temporal-lobe epilepsy. N Engl J Med. 2001; 345(5): 311–318.
- Chong S, Phi JiH, Lee JiY, et al. Surgical Treatment of Lesional Mesial Temporal Lobe Epilepsy. J Epilepsy Res. 2018; 8(1): 6–11.
- Yaşargil MG, Krayenbühl N, Roth P, et al. The selective amygdalohippocampectomy for intractable temporal limbic seizures. J Neurosurg. 2010; 112(1): 168–185.
- Ko A, Kim SeH, Kim SeH, et al. Epilepsy Surgery for Children With Low-Grade Epilepsy-Associated Tumors: Factors Associated With Seizure Recurrence and Cognitive Function. Pediatr Neurol. 2019; 91: 50–56.
- Babini M, Giulioni M, Galassi E, et al. Seizure outcome of surgical treatment of focal epilepsy associated with low-grade tumors in children. J Neurosurg Pediatr. 2013; 11(2): 214–223.
- Englot DJ, Berger MS, Barbaro NM, et al. Factors associated with seizure freedom in the surgical resection of glioneuronal tumors. Epilepsia. 2012; 53(1): 51–57.
- Abel TJ, Woodroffe RW, Nourski KV, et al. Role of the temporal pole in temporal lobe epilepsy seizure networks: an intracranial electrode investigation. J Neurosurg. 2018; 129(1): 165–173.
- Josephson CB, Dykeman J, Fiest KM, et al. Systematic review and meta-analysis of standard vs selective temporal lobe epilepsy surgery. Neurology. 2013; 80(18): 1669–1676.
- Englot DJ, Berger MS, Barbaro NM, et al. Predictors of seizure freedom after resection of supratentorial low-grade gliomas. A review. J Neurosurg. 2011; 115(2): 240–244.
- Grote A, Witt JA, Surges R, et al. A second chance--reoperation in patients with failed surgery for intractable epilepsy: long-term outcome, neuropsychology and complications. J Neurol Neurosurg Psychiatry. 2016; 87(4): 379–385.
- Giulioni M, Marucci G, Pelliccia V, et al. Commission for Epilepsy Surgery of the Italian League Against Epilepsy. Epilepsy surgery of "low grade epilepsy associated neuroepithelial tumors": A retrospective nationwide Italian study. Epilepsia. 2017; 58(11): 1832–1841.
- Pallud J, Varlet P, Devaux B, et al. Diffuse low-grade oligodendrogliomas extend beyond MRI-defined abnormalities. Neurology. 2010; 74(21): 1724–1731.
- Daszkiewicz P, Kowalczyk P, Roszkowski M. Surgical treatment of neuronal-glial tumors of mesial-basal part of temporal lobe: Long term outcome and control of epilepsy in pediatric patients. Neurol Neurochir Pol. 2018; 52(1): 2–8.
- Yang I, Chang EF, Han SJ, et al. Early surgical intervention in adult patients with ganglioglioma is associated with improved clinical seizure outcomes. J Clin Neurosci. 2011; 18(1): 29–33.
- Lowe NM, Eldridge P, Varma T, et al. The duration of temporal lobe epilepsy and seizure outcome after epilepsy surgery. Seizure. 2010; 19(5): 261–263.
- Hader WJ, Tellez-Zenteno J, Metcalfe A, et al. Complications of epilepsy surgery: a systematic review of focal surgical resections and invasive EEG monitoring. Epilepsia. 2013; 54(5): 840–847.
- Schramm J, Aliashkevich AF, Schramm J, et al. Surgery for temporal mediobasal tumors: experience based on a series of 235 patients. Neurosurgery. 2007; 60(2): 285–94; discussion 294.
- Helmstaedter C, Elger CE, Vogt VL. Cognitive outcomes more than 5 years after temporal lobe epilepsy surgery: Remarkable functional recovery when seizures are controlled. Seizure. 2018; 62: 116–123.
