Resective temporal lobe surgery in refractory temporal lobe epilepsy: prognostic factors of postoperative seizure outcome

View More View Less
  • 1 Departments of Neurosurgery and
  • 2 Epileptology, and
  • 3 Institute of Neuropathology, University Hospital Bonn, Germany
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00
Print or Print + Online

OBJECTIVE

Temporal lobe epilepsy (TLE) is one of the most common forms of epilepsy. In approximately 30% of patients, seizures are refractory to drug treatment. Despite the achievements of modern presurgical evaluation in recent years, the presurgical prediction of seizure outcome remains difficult. The aim of this study was to evaluate the seizure outcome in patients with drug-refractory TLE who underwent resective temporal lobe surgery (rTLS) and to determine features associated with unfavorable postsurgical seizure outcome.

METHODS

Patients with medically refractory TLE who underwent rTLS between 2012 and 2017 were reviewed from the prospectively collected epilepsy surgery database. A retrospective analysis of clinical, radiological, neuropsychological, histopathological, and perioperative findings of 161 patients was performed. The patients were divided into two groups according to seizure outcome (group I, International League Against Epilepsy [ILAE] class 1; group II, ILAE class ≥ 2). For identification of independent risk factors for unfavorable postoperative seizure outcome (ILAE class ≥ 2), a multivariate logistic regression analysis was performed.

RESULTS

Seizure freedom (ILAE class 1) was achieved in 121 patients (75.2%). The neuropsychological evaluation demonstrated that losses in cognitive performance were more pronounced in verbal memory after resections in the left temporal lobe and in nonverbal memory after right-sided resections, whereas attention improved after surgery. Overall, postoperative visual field deficits (VFDs) were common and occurred in 51% of patients. There was no statistically significant difference in the incidence of VFD in patients with selective surgical procedures compared to the patients with nonselective procedures. The lack of MRI lesions and placement of depth electrodes were preoperatively identified as predictors for unfavorable seizure outcome.

CONCLUSIONS

rTLS is an effective treatment method in patients with refractory TLE. However, patients with a lack of MRI lesions and placement of depth electrodes prior to rTLS are at higher risk for an unfavorable postsurgical seizure outcome.

ABBREVIATIONS AHE = amygdalohippocampectomy; ATL = anterior temporal lobectomy; CA = cornu ammonis; CI = confidence interval; DCS-R = Diagnostikum für Zerebralschäden–Revised; EEG = electroencephalography; FCD = focal cortical dysplasia; HG = hippocampal gliosis; HS = hippocampal sclerosis; ILAE = International League Against Epilepsy; OR = odds ratio; rTLS = resective temporal lobe surgery; sAHE = selective AHE; TLE = temporal lobe epilepsy; VFD = visual field deficit; VLMT = verbal learning and memory test.

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00

Contributor Notes

Correspondence Valeri Borger: University Hospital Bonn, Germany. valeri.borger@ukbonn.de.

INCLUDE WHEN CITING Published online January 8, 2021; DOI: 10.3171/2020.7.JNS20284.

Disclosures Dr. Helmstaedter reports receiving honoraria from UCB, Eisai, Precisis, and GW; receiving royalties from EpiTrack and NeuroCog FX; and being a consultant to Eisai, UCB, Precisis, and GW. Ms. Taube received support of non–study-related clinical or research effort from the University Hospital Bonn Department of Epileptology (European Reference Network EpiCARE Grant).

  • 1

    Engel J Jr. Surgical treatment for epilepsy: too little, too late? JAMA. 2008;300(21):25482550.

  • 2

    Wiebe S, Blume WT, Girvin JP, Eliasziw M. A randomized, controlled trial of surgery for temporal-lobe epilepsy. N Engl J Med. 2001;345(5):311318.

    • Search Google Scholar
    • Export Citation
  • 3

    Engel J Jr, Wiebe S, French J, Practice parameter: temporal lobe and localized neocortical resections for epilepsy: report of the Quality Standards Subcommittee of the American Academy of Neurology, in association with the American Epilepsy Society and the American Association of Neurological Surgeons. Neurology. 2003;60(4):538547.

    • Search Google Scholar
    • Export Citation
  • 4

    Englot DJ, Chang EF. Rates and predictors of seizure freedom in resective epilepsy surgery: an update. Neurosurg Rev. 2014;37(3):389405.

    • Search Google Scholar
    • Export Citation
  • 5

    Bien CG, Raabe AL, Schramm J, Trends in presurgical evaluation and surgical treatment of epilepsy at one centre from 1988–2009. J Neurol Neurosurg Psychiatry. 2013;84(1):5461.

    • Search Google Scholar
    • Export Citation
  • 6

    Kral T, Clusmann H, Urbach J, Preoperative evaluation for epilepsy surgery (Bonn Algorithm). Zentralbl Neurochir. 2002;63(3):106110.

  • 7

    Wellmer J, von der Groeben F, Klarmann U, Risks and benefits of invasive epilepsy surgery workup with implanted subdural and depth electrodes. Epilepsia. 2012;53(8):13221332.

    • Search Google Scholar
    • Export Citation
  • 8

    Blümcke I, Thom M, Aronica E, International consensus classification of hippocampal sclerosis in temporal lobe epilepsy: a Task Force report from the ILAE Commission on Diagnostic Methods. Epilepsia. 2013;54(7):13151329.

    • Search Google Scholar
    • Export Citation
  • 9

    Louis DN, Perry A, Reifenberger G, The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary. Acta Neuropathol. 2016;131(6):803820.

    • Search Google Scholar
    • Export Citation
  • 10

    Blümcke I, Thom M, Aronica E, 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):158174.

    • Search Google Scholar
    • Export Citation
  • 11

    Wieser HG, Blume WT, Fish D, ILAE Commission Report. Proposal for a new classification of outcome with respect to epileptic seizures following epilepsy surgery. Epilepsia. 2001;42(2):282286.

    • Search Google Scholar
    • Export Citation
  • 12

    Grote A, Witt JA, Surges R, 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):379385.

    • Search Google Scholar
    • Export Citation
  • 13

    Sadek AR, Gray WP. Chopping and changing: long-term results of epilepsy surgery. Lancet. 2011;378(9800):13601362.

  • 14

    McIntosh AM, Kalnins RM, Mitchell LA, Temporal lobectomy: long-term seizure outcome, late recurrence and risks for seizure recurrence. Brain. 2004;127(Pt 9):20182030.

    • Search Google Scholar
    • Export Citation
  • 15

    Jeha LE, Najm IM, Bingaman WE, Predictors of outcome after temporal lobectomy for the treatment of intractable epilepsy. Neurology. 2006;66(12):19381940.

    • Search Google Scholar
    • Export Citation
  • 16

    Schmeiser B, Wagner K, Schulze-Bonhage A, Surgical treatment of mesiotemporal lobe epilepsy: which approach is favorable? Neurosurgery. 2017;81(6):9921004.

    • Search Google Scholar
    • Export Citation
  • 17

    Hu WH, Zhang C, Zhang K, Selective amygdalohippocampectomy versus anterior temporal lobectomy in the management of mesial temporal lobe epilepsy: a meta-analysis of comparative studies. J Neurosurg. 2013;119(5):10891097.

    • Search Google Scholar
    • Export Citation
  • 18

    Josephson CB, Dykeman J, Fiest KM, Systematic review and meta-analysis of standard vs selective temporal lobe epilepsy surgery. Neurology. 2013;80(18):16691676.

    • Search Google Scholar
    • Export Citation
  • 19

    Malikova H, Kramska L, Vojtech Z, Different surgical approaches for mesial temporal epilepsy: resection extent, seizure, and neuropsychological outcomes. Stereotact Funct Neurosurg. 2014;92(6):372380.

    • Search Google Scholar
    • Export Citation
  • 20

    Wendling AS, Hirsch E, Wisniewski I, Selective amygdalohippocampectomy versus standard temporal lobectomy in patients with mesial temporal lobe epilepsy and unilateral hippocampal sclerosis. Epilepsy Res. 2013;104(1-2):94104.

    • Search Google Scholar
    • Export Citation
  • 21

    Schramm J. Temporal lobe epilepsy surgery and the quest for optimal extent of resection: a review. Epilepsia. 2008;49(8):12961307.

  • 22

    Yaşargil MG, Krayenbühl N, Roth P, The selective amygdalohippocampectomy for intractable temporal limbic seizures. J Neurosurg. 2010;112(1):168185.

    • Search Google Scholar
    • Export Citation
  • 23

    Parrent AG, Blume WT. Stereotactic amygdalohippocampotomy for the treatment of medial temporal lobe epilepsy. Epilepsia. 1999;40(10):14081416.

    • Search Google Scholar
    • Export Citation
  • 24

    Georgiadis I, Kapsalaki EZ, Fountas KN. Temporal lobe resective surgery for medically intractable epilepsy: a review of complications and side effects. Epilepsy Res Treat. 2013;2013:752195.

    • Search Google Scholar
    • Export Citation
  • 25

    Erba G, Winston KR, Adler JR, Temporal lobectomy for complex partial seizures that began in childhood. Surg Neurol. 1992;38(6):424432.

    • Search Google Scholar
    • Export Citation
  • 26

    Schmeiser B, Daniel M, Kogias E, Visual field defects following different resective procedures for mesiotemporal lobe epilepsy. Epilepsy Behav. 2017;76:3945.

    • Search Google Scholar
    • Export Citation
  • 27

    Helmstaedter C, Richter S, Röske S, Differential effects of temporal pole resection with amygdalohippocampectomy versus selective amygdalohippocampectomy on material-specific memory in patients with mesial temporal lobe epilepsy. Epilepsia. 2008;49(1):8897.

    • Search Google Scholar
    • Export Citation
  • 28

    Helmstaedter C, Elger CE, Witt JA. The effect of quantitative and qualitative antiepileptic drug changes on cognitive recovery after epilepsy surgery. Seizure. 2016;36:6369.

    • Search Google Scholar
    • Export Citation
  • 29

    Tonini C, Beghi E, Berg AT, Predictors of epilepsy surgery outcome: a meta-analysis. Epilepsy Res. 2004;62(1):7587.

  • 30

    Carne RP, O’Brien TJ, Kilpatrick CJ, MRI-negative PET-positive temporal lobe epilepsy: a distinct surgically remediable syndrome. Brain. 2004;127(Pt 10):22762285.

    • Search Google Scholar
    • Export Citation
  • 31

    Téllez-Zenteno JF, Hernández 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(2-3):310318.

    • Search Google Scholar
    • Export Citation
  • 32

    Bien CG, Szinay M, Wagner J, Characteristics and surgical outcomes of patients with refractory magnetic resonance imaging-negative epilepsies. Arch Neurol. 2009;66(12):14911499.

    • Search Google Scholar
    • Export Citation
  • 33

    Ivanovic J, Larsson PG, Østby Y, Seizure outcomes of temporal lobe epilepsy surgery in patients with normal MRI and without specific histopathology. Acta Neurochir (Wien). 2017;159(5):757766.

    • Search Google Scholar
    • Export Citation
  • 34

    Sotero de Menezes MA, Connolly M, Bolanos A, Temporal lobectomy in early childhood: the need for long-term follow-up. J Child Neurol. 2001;16(8):585590.

    • Search Google Scholar
    • Export Citation
  • 35

    Roberts DW, Jobst BC, Siegel AM, Investigation of extra-temporal epilepsy. Stereotact Funct Neurosurg. 2001;77(1-4):216218.

  • 36

    de Lanerolle NC, Kim JH, Williamson A, A retrospective analysis of hippocampal pathology in human temporal lobe epilepsy: evidence for distinctive patient subcategories. Epilepsia. 2003;44(5):677687.

    • Search Google Scholar
    • Export Citation
  • 37

    Blümcke I, Pauli E, Clusmann H, A new clinico-pathological classification system for mesial temporal sclerosis. Acta Neuropathol. 2007;113(3):235244.

    • Search Google Scholar
    • Export Citation
  • 38

    Thom M, Liagkouras I, Elliot KJ, Reliability of patterns of hippocampal sclerosis as predictors of postsurgical outcome. Epilepsia. 2010;51(9):18011808.

    • Search Google Scholar
    • Export Citation
  • 39

    Gales JM, Jehi L, Nowacki A, Prayson RA. The role of histopathologic subtype in the setting of hippocampal sclerosis-associated mesial temporal lobe epilepsy. Hum Pathol. 2017;63:7988.

    • Search Google Scholar
    • Export Citation
  • 40

    Deleo F, Garbelli R, Milesi G, Short- and long-term surgical outcomes of temporal lobe epilepsy associated with hippocampal sclerosis: relationships with neuropathology. Epilepsia. 2016;57(2):306315.

    • Search Google Scholar
    • Export Citation
  • 41

    Savitr Sastri BV, Arivazhagan A, Sinha S, Clinico-pathological factors influencing surgical outcome in drug resistant epilepsy secondary to mesial temporal sclerosis. J Neurol Sci. 2014;340(1-2):183190.

    • Search Google Scholar
    • Export Citation
  • 42

    Hattingen E, Enkirch SJ, Jurcoane A, Hippocampal “gliosis only” on MR imaging represents a distinct entity in epilepsy patients. Neuroradiology. 2018;60(2):161168.

    • Search Google Scholar
    • Export Citation
  • 43

    Bernhardt BC, Fadaie F, Liu M, Temporal lobe epilepsy: hippocampal pathology modulates connectome topology and controllability. Neurology. 2019;92(19):e2209e2220.

    • Search Google Scholar
    • Export Citation
  • 44

    Paolicchi JM, Jayakar P, Dean P, Predictors of outcome in pediatric epilepsy surgery. Neurology. 2000;54(3):642647.

  • 45

    Harroud A, Bouthillier A, Weil AG, Nguyen DK. Temporal lobe epilepsy surgery failures: a review. Epilepsy Res Treat. 2012;2012:201651.

Metrics

All Time Past Year Past 30 Days
Abstract Views 180 180 180
Full Text Views 20 20 20
PDF Downloads 13 13 13
EPUB Downloads 0 0 0