Top

Published in:

01-05-2019 | Glioma | Clinical Study

Awake craniotomies for epileptic gliomas: intraoperative and postoperative seizure control and prognostic factors

Authors: Yu-Chi Wang, Cheng-Chi Lee, Hirokazu Takami, Stephanie Shen, Ko-Ting Chen, Kuo-Chen Wei, Min-Hsien Wu, Gregory Worrell, Pin-Yuan Chen

Published in: Journal of Neuro-Oncology | Issue 3/2019

Abstract

Purpose

Awake craniotomy is well-established for tumors resected in eloquent brain areas. Whether awake craniotomy provides improved seizure control in patients with epileptic gliomas has not been well evaluated. This study analyzed the incidence, risk factors and outcome of seizures during and following awake craniotomies for patients presenting with epilepsy and glioma.

Methods

Forty-one patients undergoing awake craniotomies for epileptic gliomas were retrospectively analyzed. Postoperative seizure was defined as either early (postoperative day 7 + before) or late onset (after postoperative day 7). Neurologic function was assessed with modified Rankin Scales (mRS) and seizure outcome was assessed using International League Against Epilepsy (ILAE) classification. Multivariable logistic regression was used for clinical variables associated with postoperative seizures.

Results

Three patients (7.3%) had intraoperative seizures however did not fail the awake craniotomies. Mean mRS before and after the awake craniotomies were 2.4 and 2.1, respectively (P = 0.032). Fourteen (34.1%) patients had early seizures, which caused longer hospitalization than those without early seizures (P = 0.03). Surgical resection to isocitrate dehydrogenase 1 (IDH1) mutation tumors, comparing to IDH1 wild type tumors, caused better postoperative seizure control. 6-month late seizure freedom was achieved in 33 patients (80.5%). Early seizure recurrence (odds ratio = 30.75; P = 0.039) and postoperative mRS ≥ 3 (odds ratio = 7.00; P = 0.047) were independent risk factors for late seizures.

Conclusions

Intraoperative seizures could be well-controlled during awake craniotomies. Early postoperative seizures extended hospitalization and strongly predicted late seizure recurrence. Awake craniotomies benefited long-term seizure control in patients with epileptic gliomas.

Available only for authorised users

Sacko O, Lauwers-Cances V, Brauge D, Sesay M, Brenner A, Roux FE (2011) Awake craniotomy vs surgery under general anesthesia for resection of supratentorial lesions. Neurosurgery 68:1192–1198. https://doi.org/10.1227/NEU.0b013e31820c02a3 (discussion 1198–1199)CrossRefPubMed

Taylor MD, Bernstein M (1999) Awake craniotomy with brain mapping as the routine surgical approach to treating patients with supratentorial intraaxial tumors: a prospective trial of 200 cases. J Neurosurg 90:35–41. https://doi.org/10.3171/jns.1999.90.1.0035 CrossRefPubMed

Duffau H, Capelle L, Denvil D, Sichez N, Gatignol P, Taillandier L, Lopes M, Mitchell MC, Roche S, Muller JC, Bitar A, Sichez JP, van Effenterre R (2003) Usefulness of intraoperative electrical subcortical mapping during surgery for low-grade gliomas located within eloquent brain regions: functional results in a consecutive series of 103 patients. J Neurosurg 98:764–778. https://doi.org/10.3171/jns.2003.98.4.0764 CrossRefPubMed

Kim SS, McCutcheon IE, Suki D, Weinberg JS, Sawaya R, Lang FF, Ferson D, Heimberger AB, DeMonte F, Prabhu SS (2009) Awake craniotomy for brain tumors near eloquent cortex: correlation of intraoperative cortical mapping with neurological outcomes in 309 consecutive patients. Neurosurgery 64:836–845. https://doi.org/10.1227/01.NEU.0000342405.80881.81 (discussion 345–836)CrossRefPubMed

Manninen PH, Tan TK (2002) Postoperative nausea and vomiting after craniotomy for tumor surgery: a comparison between awake craniotomy and general anesthesia. J Clin Anesth 14:279–283CrossRefPubMed

Klimek M, Dammers R (2010) Antiepileptic drug therapy in the perioperative course of neurosurgical patients. Curr Opin Anaesthesiol 23:564–567. https://doi.org/10.1097/ACO.0b013e32833e14f2 CrossRefPubMed

Komotar RJ, Raper DM, Starke RM, Iorgulescu JB, Gutin PH (2011) Prophylactic antiepileptic drug therapy in patients undergoing supratentorial meningioma resection: a systematic analysis of efficacy. J Neurosurg 115:483–490. https://doi.org/10.3171/2011.4.JNS101585 CrossRefPubMed

van Breemen MS, Wilms EB, Vecht CJ (2007) Epilepsy in patients with brain tumours: epidemiology, mechanisms, and management. Lancet Neurol 6:421–430. https://doi.org/10.1016/S1474-4422(07)70103-5 CrossRefPubMed

Kerkhof M, Vecht CJ (2013) Seizure characteristics and prognostic factors of gliomas. Epilepsia 54(Suppl 9):12–17. https://doi.org/10.1111/epi.12437 CrossRefPubMed

10.

Chen H, Judkins J, Thomas C, Wu M, Khoury L, Benjamin CG, Pacione D, Golfinos JG, Kumthekar P, Ghamsari F, Chen L, Lein P, Chetkovich DM, Snuderl M, Horbinski C (2017) Mutant IDH1 and seizures in patients with glioma. Neurology 88:1805–1813. https://doi.org/10.1212/WNL.0000000000003911 CrossRefPubMedPubMedCentral

11.

Fisher RS, Cross JH, French JA, Higurashi N, Hirsch E, Jansen FE, Lagae L, Moshe SL, Peltola J, Roulet Perez E, Scheffer IE, Zuberi SM (2017) Operational classification of seizure types by the International League Against Epilepsy: position paper of the ILAE Commission for Classification and Terminology. Epilepsia 58:522–530. https://doi.org/10.1111/epi.13670 CrossRefPubMed

12.

Chang WH, Pei YC, Wei KC, Chao YP, Chen MH, Yeh HA, Jaw FS, Chen PY (2018) Intraoperative linguistic performance during awake brain surgery predicts postoperative linguistic deficits. J Neuro-oncol. https://doi.org/10.1007/s11060-018-2863-z CrossRef

13.

Quinn TJ, Dawson J, Walters MR, Lees KR (2009) Reliability of the modified Rankin Scale: a systematic review. Stroke 40:3393–3395. https://doi.org/10.1161/STROKEAHA.109.557256 CrossRefPubMed

14.

Wieser HG, Blume WT, Fish D, Goldensohn E, Hufnagel A, King D, Sperling MR, Luders H, Pedley TA (2001) ILAE Commission Report. Proposal for a new classification of outcome with respect to epileptic seizures following epilepsy surgery. Epilepsia 42:282–286CrossRefPubMed

15.

Guerrini R, Rosati A, Giordano F, Genitori L, Barba C (2013) The medical and surgical treatment of tumoral seizures: current and future perspectives. Epilepsia 54(Suppl 9):84–90. https://doi.org/10.1111/epi.12450 CrossRefPubMed

16.

Ruda R, Bello L, Duffau H, Soffietti R (2012) Seizures in low-grade gliomas: natural history, pathogenesis, and outcome after treatments. Neuro oncology 14(Suppl 4):iv55–i64. https://doi.org/10.1093/neuonc/nos199 CrossRefPubMedPubMedCentral

17.

Goellner E, Bianchin MM, Burneo JG, Parrent AG, Steven DA (2013) Timing of early and late seizure recurrence after temporal lobe epilepsy surgery. Epilepsia 54:1933–1941. https://doi.org/10.1111/epi.12389 CrossRefPubMed

18.

Nossek E, Matot I, Shahar T, Barzilai O, Rapoport Y, Gonen T, Sela G, Korn A, Hayat D, Ram Z (2013) Failed awake craniotomy: a retrospective analysis in 424 patients undergoing craniotomy for brain tumor. J Neurosurg 118:243–249. https://doi.org/10.3171/2012.10.JNS12511 CrossRefPubMed

19.

Nossek E, Matot I, Shahar T, Barzilai O, Rapoport Y, Gonen T, Sela G, Grossman R, Korn A, Hayat D, Ram Z (2013) Intraoperative seizures during awake craniotomy: incidence and consequences: analysis of 477 patients. Neurosurgery 73:135–140. https://doi.org/10.1227/01.neu.0000429847.91707.97 (discussion 140)CrossRefPubMed

20.

Szelenyi A, Bello L, Duffau H, Fava E, Feigl GC, Galanda M, Neuloh G, Signorelli F, Sala F (2010) Intraoperative electrical stimulation in awake craniotomy: methodological aspects of current practice. Neurosurg Focus 28:E7. https://doi.org/10.3171/2009.12.FOCUS09237 CrossRefPubMed

21.

Uematsu S, Lesser R, Fisher RS, Gordon B, Hara K, Krauss GL, Vining EP, Webber RW (1992) Motor and sensory cortex in humans: topography studied with chronic subdural stimulation. Neurosurgery 31:59–71 (discussion 71–52)PubMed

22.

Pouratian N, Cannestra AF, Bookheimer SY, Martin NA, Toga AW (2004) Variability of intraoperative electrocortical stimulation mapping parameters across and within individuals. J Neurosurg 101:458–466. https://doi.org/10.3171/jns.2004.101.3.0458 CrossRefPubMed

23.

Szelenyi A, Bello L, Duffau H, Fava E, Feigl GC, Galanda M, Neuloh G, Signorelli F, Sala F, Workgroup for Intraoperative Management in Low-Grade Glioma Surgery within the European Low-Grade Glioma Network (2010) Intraoperative electrical stimulation in awake craniotomy: methodological aspects of current practice. Neurosurg Focus 28:E7. https://doi.org/10.3171/2009.12.FOCUS09237 N )CrossRefPubMed

24.

Sughrue ME, Rutkowski MJ, Chang EF, Shangari G, Kane AJ, McDermott MW, Berger MS, Parsa AT (2011) Postoperative seizures following the resection of convexity meningiomas: are prophylactic anticonvulsants indicated? Clinical article. J Neurosurg 114:705–709. https://doi.org/10.3171/2010.5.JNS091972 CrossRefPubMed

25.

Wang YC, Chuang CC, Tu PH, Wei KC, Wu CT, Lee CC, Liu ZH, Chen PY (2018) Seizures in surgically resected atypical and malignant meningiomas: long-term outcome analysis. Epilepsy Res 140:82–89. https://doi.org/10.1016/j.eplepsyres.2017.12.013 CrossRefPubMed

26.

Englot DJ, Berger MS, Barbaro NM, Chang EF (2011) Predictors of seizure freedom after resection of supratentorial low-grade gliomas. A review. J Neurosurg 115:240–244. https://doi.org/10.3171/2011.3.JNS1153 CrossRefPubMed

27.

Southwell DG, Garcia PA, Berger MS, Barbaro NM, Chang EF (2012) Long-term seizure control outcomes after resection of gangliogliomas. Neurosurgery 70:1406–1413. https://doi.org/10.1227/NEU.0b013e3182500a4c (discussion 1413–1404)CrossRefPubMed

28.

Kerkhof M, Dielemans JC, van Breemen MS, Zwinkels H, Walchenbach R, Taphoorn MJ, Vecht CJ (2013) Effect of valproic acid on seizure control and on survival in patients with glioblastoma multiforme. Neuro oncology 15:961–967. https://doi.org/10.1093/neuonc/not057 CrossRefPubMedPubMedCentral

29.

Stockhammer F, Misch M, Helms HJ, Lengler U, Prall F, von Deimling A, Hartmann C (2012) IDH1/2 mutations in WHO grade II astrocytomas associated with localization and seizure as the initial symptom. Seizure 21:194–197. https://doi.org/10.1016/j.seizure.2011.12.007 CrossRefPubMed

30.

Liubinas SV, D’Abaco GM, Moffat BM, Gonzales M, Feleppa F, Nowell CJ, Gorelik A, Drummond KJ, O’Brien TJ, Kaye AH, Morokoff AP (2014) IDH1 mutation is associated with seizures and protoplasmic subtype in patients with low-grade gliomas. Epilepsia 55:1438–1443. https://doi.org/10.1111/epi.12662 CrossRefPubMed

31.

Feyissa AM, Worrell GA, Tatum WO, Mahato D, Brinkmann BH, Rosenfeld SS, ReFaey K, Bechtle PS, Quinones-Hinojosa A (2018) High-frequency oscillations in awake patients undergoing brain tumor-related epilepsy surgery. Neurology 90:e1119–e1125. https://doi.org/10.1212/WNL.0000000000005216 CrossRefPubMedPubMedCentral

32.

Scheffer IE, Berkovic S, Capovilla G, Connolly MB, French J, Guilhoto L, Hirsch E, Jain S, Mathern GW, Moshe SL, Nordli DR, Perucca E, Tomson T, Wiebe S, Zhang YH, Zuberi SM (2017) ILAE classification of the epilepsies: position paper of the ILAE Commission for Classification and Terminology. Epilepsia 58:512–521. https://doi.org/10.1111/epi.13709 CrossRefPubMedPubMedCentral

33.

Frey LC (2003) Epidemiology of posttraumatic epilepsy: a critical review. Epilepsia 44:11–17CrossRefPubMed

34.

Kilpatrick CJ, Davis SM, Hopper JL, Rossiter SC (1992) Early seizures after acute stroke. Risk of late seizures. Arch Neurol 49:509–511CrossRefPubMed

35.

Zheng Z, Chen P, Fu W, Zhu J, Zhang H, Shi J, Zhang J (2013) Early and late postoperative seizure outcome in 97 patients with supratentorial meningioma and preoperative seizures: a retrospective study. J Neuro-oncol 114:101–109. https://doi.org/10.1007/s11060-013-1156-9 CrossRef

36.

Biffi A, Rattani A, Anderson CD, Ayres AM, Gurol EM, Greenberg SM, Rosand J, Viswanathan A (2016) Delayed seizures after intracerebral haemorrhage. Brain 139:2694–2705. https://doi.org/10.1093/brain/aww199 CrossRefPubMedPubMedCentral

37.

Maschio M, Dinapoli L (2012) Patients with brain tumor-related epilepsy. J Neuro-oncol 109:1–6. https://doi.org/10.1007/s11060-012-0867-7 CrossRef

38.

Glantz MJ, Cole BF, Forsyth PA, Recht LD, Wen PY, Chamberlain MC, Grossman SA, Cairncross JG (2000) Practice parameter: anticonvulsant prophylaxis in patients with newly diagnosed brain tumors. Report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology 54:1886–1893CrossRefPubMed

39.

Lee YJ, Kim T, Bae SH, Kim YH, Han JH, Yun CH, Kim CY (2013) Levetiracetam compared with valproic acid for the prevention of postoperative seizures after supratentorial tumor surgery: a retrospective chart review. CNS Drugs 27:753–759. https://doi.org/10.1007/s40263-013-0094-6 CrossRefPubMed

40.

Szaflarski JP, Sangha KS, Lindsell CJ, Shutter LA (2010) Prospective, randomized, single-blinded comparative trial of intravenous levetiracetam versus phenytoin for seizure prophylaxis. Neurocrit Care 12:165–172. https://doi.org/10.1007/s12028-009-9304-y CrossRefPubMed

41.

Zachenhofer I, Donat M, Oberndorfer S, Roessler K (2011) Perioperative levetiracetam for prevention of seizures in supratentorial brain tumor surgery. J Neuro-oncol 101:101–106. https://doi.org/10.1007/s11060-010-0235-4 CrossRef

42.

Eseonu CI, Eguia F, Garcia O, Kaplan PW, Quinones-Hinojosa A (2018) Comparative analysis of monotherapy versus duotherapy antiseizure drug management for postoperative seizure control in patients undergoing an awake craniotomy. J Neurosurg 128:1661–1667. https://doi.org/10.3171/2017.1.JNS162913 CrossRefPubMed

Title: Awake craniotomies for epileptic gliomas: intraoperative and postoperative seizure control and prognostic factors
Authors: Yu-Chi Wang
Cheng-Chi Lee
Hirokazu Takami
Stephanie Shen
Ko-Ting Chen
Kuo-Chen Wei
Min-Hsien Wu
Gregory Worrell
Pin-Yuan Chen
Publication date: 01-05-2019
Publisher: Springer US
Keywords: Glioma
Craniotomy
Glioma
Epilepsy
Glioma
Published in: Journal of Neuro-Oncology / Issue 3/2019
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI: https://doi.org/10.1007/s11060-019-03131-0

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Awake craniotomies for epileptic gliomas: intraoperative and postoperative seizure control and prognostic factors

Abstract

Purpose

Methods

Results

Conclusions

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 3/2019

Gamma Knife Stereotactic Radiosurgery favorably changes the clinical course of hemangioblastoma growth in von Hippel-Lindau and sporadic patients

Proton therapy for skull-base chondrosarcoma, a single-institution outcomes study

Multicenter, single arm, phase II trial on the efficacy of ortataxel in recurrent glioblastoma

Correction to: Neuro-radiological characteristics of adult diffuse grade II and III insular gliomas classified according to WHO 2016

A multicenter phase II study of temozolomide plus disulfiram and copper for recurrent temozolomide-resistant glioblastoma

Telomere elongation via alternative lengthening of telomeres (ALT) and telomerase activation in primary metastatic medulloblastoma of childhood