Seizure outcome in temporal glioblastoma surgery: lobectomy as a supratotal resection regime outclasses conventional gross-total resection.


Journal

Journal of neuro-oncology
ISSN: 1573-7373
Titre abrégé: J Neurooncol
Pays: United States
ID NLM: 8309335

Informations de publication

Date de publication:
Apr 2021
Historique:
received: 09 10 2020
accepted: 19 01 2021
pubmed: 9 2 2021
medline: 17 11 2021
entrez: 8 2 2021
Statut: ppublish

Résumé

The postoperative seizure freedom represents an important secondary outcome measure in glioblastoma surgery. Recently, supra-total glioblastoma resection in terms of anterior temporal lobectomy (ATL) has gained growing attention with regard to superior long-term disease control for temporal-located glioblastoma compared to conventional gross-total resections (GTR). However, the impact of ATL on seizure outcome in these patients is unknown. We therefore analyzed ATL and GTR as differing extents of resection in regard of postoperative seizure control in patients with temporal glioblastoma and preoperative symptomatic seizures. Between 2012 and 2018, 33 patients with preoperative seizures underwent GTR or ATL for temporal glioblastoma at the authors' institution. Seizure outcome was assessed postoperatively and 6 months after tumor resection according to the International League Against Epilepsy (ILAE) classification and stratified into favorable (ILAE class 1) versus unfavorable (ILAE class 2-6). Overall, 23 out of 33 patients (70%) with preoperative seizures achieved favorable seizure outcome following resection of temporal located glioblastoma. For the ATL group, postoperative seizure freedom was present in 13 out of 13 patients (100%). In comparison, respective rates for the GTR group were 10 out of 20 patients (50%) (p = 0.002; OR 27; 95% CI 1.4-515.9). ATL in terms of a supra-total resection strategy was associated with superior favorable seizure outcome following temporal glioblastoma resection compared to GTR. Regarding above mentioned survival benefit following ATL compared to GTR, ATL as an aggressive supra-total resection regime might constitute the surgical modality of choice for temporal-located glioblastoma.

Identifiants

pubmed: 33554293
doi: 10.1007/s11060-021-03705-x
pii: 10.1007/s11060-021-03705-x
pmc: PMC7997820
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

339-346

Références

Potthoff AL, Heiland DH, Evert BO, Almeida FR, Behringer SP, Dolf A, Güresir A, Güresir E, Joseph K, Pietsch T, Schuss P, Herrlinger U, Westhoff MA, Vatter H, Waha A, Schneider M (2019) Inhibition of gap junctions sensitizes primary glioblastoma cells for temozolomide. Cancers (Basel). https://doi.org/10.3390/cancers11060858
doi: 10.3390/cancers11060858
Cai X, Sughrue ME (2018) Glioblastoma: new therapeutic strategies to address cellular and genomic complexity. Oncotarget 9(10):9540–9554. https://doi.org/10.18632/oncotarget.23476
doi: 10.18632/oncotarget.23476 pubmed: 29507709
Preusser M, de Ribaupierre S, Wohrer A, Erridge SC, Hegi M, Weller M, Stupp R (2011) Current concepts and management of glioblastoma. Ann Neurol 70(1):9–21. https://doi.org/10.1002/ana.22425
doi: 10.1002/ana.22425 pubmed: 21786296
Stummer W, Reulen HJ, Meinel T, Pichlmeier U, Schumacher W, Tonn JC, Rohde V, Oppel F, Turowski B, Woiciechowsky C, Franz K, Pietsch T, Group AL-GS (2008) Extent of resection and survival in glioblastoma multiforme: identification of and adjustment for bias. Neurosurgery 62 (3):564–576; discussion 564–576. https://doi.org/ https://doi.org/10.1227/01.neu.0000317304.31579.17
Pyonteck SM, Akkari L, Schuhmacher AJ, Bowman RL, Sevenich L, Quail DF, Olson OC, Quick ML, Huse JT, Teijeiro V, Setty M, Leslie CS, Oei Y, Pedraza A, Zhang J, Brennan CW, Sutton JC, Holland EC, Daniel D, Joyce JA (2013) CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat Med 19(10):1264–1272. https://doi.org/10.1038/nm.3337
doi: 10.1038/nm.3337 pubmed: 24056773 pmcid: 3840724
Incekara F, Koene S, Vincent A, van den Bent MJ, Smits M (2019) Association between supratotal glioblastoma resection and patient survival: a systematic review and meta-analysis. World Neurosurg 127(617–624):e612. https://doi.org/10.1016/j.wneu.2019.04.092
doi: 10.1016/j.wneu.2019.04.092
Brown TJ, Brennan MC, Li M, Church EW, Brandmeir NJ, Rakszawski KL, Patel AS, Rizk EB, Suki D, Sawaya R, Glantz M (2016) Association of the extent of resection with survival in glioblastoma: a systematic review and meta-analysis. JAMA Oncol 2(11):1460–1469. https://doi.org/10.1001/jamaoncol.2016.1373
doi: 10.1001/jamaoncol.2016.1373 pubmed: 27310651 pmcid: 6438173
McGirt MJ, Chaichana KL, Gathinji M, Attenello FJ, Than K, Olivi A, Weingart JD, Brem H, Quinones-Hinojosa AR (2009) Independent association of extent of resection with survival in patients with malignant brain astrocytoma. J Neurosurg 110(1):156–162. https://doi.org/10.3171/2008.4.17536
doi: 10.3171/2008.4.17536 pubmed: 18847342
Schneider M, Potthoff AL, Keil VC, Güresir A, Weller J, Borger V, Hamed M, Waha A, Vatter H, Güresir E, Herrlinger U, Schuss P (2019) Surgery for temporal glioblastoma: lobectomy outranks oncosurgical-based gross-total resection. J Neurooncol 145(1):143–150. https://doi.org/10.1007/s11060-019-03281-1
doi: 10.1007/s11060-019-03281-1 pubmed: 31485921
Englot DJ, Han SJ, Berger MS, Barbaro NM, Chang EF (2012) Extent of surgical resection predicts seizure freedom in low-grade temporal lobe brain tumors. Neurosurgery 70 (4):921–928; discussion 928. doi: https://doi.org/10.1227/NEU.0b013e31823c3a30
Wiebe S, Blume WT, Girvin JP, Eliasziw M, Effectiveness, Efficiency of Surgery for Temporal Lobe Epilepsy Study G (2001) A randomized, controlled trial of surgery for temporal-lobe epilepsy. N Engl J Med 345(5):311–318. https://doi.org/10.1056/NEJM200108023450501
doi: 10.1056/NEJM200108023450501 pubmed: 11484687
Schneider M, Ilic I, Potthoff AL, Hamed M, Schäfer N, Velten M, Güresir E, Herrlinger U, Borger V, Vatter H, Schuss P (2020) Safety metric profiling in surgery for temporal glioblastoma: lobectomy as a supra-total resection regime preserves perioperative standard quality rates. J Neurooncol 149(3):455–461. https://doi.org/10.1007/s11060-020-03629-y
doi: 10.1007/s11060-020-03629-y pubmed: 32990861 pmcid: 7609430
Herrlinger U, Tzaridis T, Mack F, Steinbach JP, Schlegel U, Sabel M, Hau P, Kortmann RD, Krex D, Grauer O, Goldbrunner R, Schnell O, Bahr O, Uhl M, Seidel C, Tabatabai G, Kowalski T, Ringel F, Schmidt-Graf F, Suchorska B, Brehmer S, Weyerbrock A, Renovanz M, Bullinger L, Galldiks N, Vajkoczy P, Misch M, Vatter H, Stuplich M, Schäfer N, Kebir S, Weller J, Schaub C, Stummer W, Tonn JC, Simon M, Keil VC, Nelles M, Urbach H, Coenen M, Wick W, Weller M, Fimmers R, Schmid M, Hattingen E, Pietsch T, Coch C, Glas M, Neurooncology Working Group of the German Cancer S (2019) Lomustine-temozolomide combination therapy versus standard temozolomide therapy in patients with newly diagnosed glioblastoma with methylated MGMT promoter (CeTeG/NOA-09): a randomised, open-label, phase 3 trial. Lancet 393(10172):678–688. https://doi.org/10.1016/S0140-6736(18)31791-4
doi: 10.1016/S0140-6736(18)31791-4 pubmed: 30782343
Chaichana KL, Parker SL, Olivi A, Quinones-Hinojosa A (2009) Long-term seizure outcomes in adult patients undergoing primary resection of malignant brain astrocytomas. Clinical article. J Neurosurg 111(2):282–292. https://doi.org/10.3171/2009.2.JNS081132
doi: 10.3171/2009.2.JNS081132 pubmed: 19344222
Vecht CJ, Kerkhof M, Duran-Pena A (2014) Seizure prognosis in brain tumors: new insights and evidence-based management. Oncologist 19(7):751–759. https://doi.org/10.1634/theoncologist.2014-0060
doi: 10.1634/theoncologist.2014-0060 pubmed: 24899645 pmcid: 4077452
van Breemen MS, Wilms EB, Vecht CJ (2007) Epilepsy in patients with brain tumours: epidemiology, mechanisms, and management. Lancet Neurol 6(5):421–430. https://doi.org/10.1016/S1474-4422(07)70103-5
doi: 10.1016/S1474-4422(07)70103-5 pubmed: 17434097
Shin JY, Kizilbash SH, Robinson SI, Uhm JH, Hammack JE, Lachance DH, Buckner JC, Jatoi A (2016) Seizures in patients with primary brain tumors: what is their psychosocial impact? J Neurooncol 128(2):285–291. https://doi.org/10.1007/s11060-016-2108-y
doi: 10.1007/s11060-016-2108-y pubmed: 26979915
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 Oncol 15(7):961–967. https://doi.org/10.1093/neuonc/not057
doi: 10.1093/neuonc/not057 pubmed: 23680820 pmcid: 3688020
Redjal N, Reinshagen C, Le A, Walcott BP, McDonnell E, Dietrich J, Nahed BV (2016) Valproic acid, compared to other antiepileptic drugs, is associated with improved overall and progression-free survival in glioblastoma but worse outcome in grade II/III gliomas treated with temozolomide. J Neurooncol 127(3):505–514. https://doi.org/10.1007/s11060-016-2054-8
doi: 10.1007/s11060-016-2054-8 pubmed: 26830093
Kim YH, Kim T, Joo JD, Han JH, Kim YJ, Kim IA, Yun CH, Kim CY (2015) Survival benefit of levetiracetam in patients treated with concomitant chemoradiotherapy and adjuvant chemotherapy with temozolomide for glioblastoma multiforme. Cancer 121(17):2926–2932. https://doi.org/10.1002/cncr.29439
doi: 10.1002/cncr.29439 pubmed: 25975354
de Groot M, Douw L, Sizoo EM, Bosma I, Froklage FE, Heimans JJ, Postma TJ, Klein M, Reijneveld JC (2013) Levetiracetam improves verbal memory in high-grade glioma patients. Neuro Oncol 15(2):216–223. https://doi.org/10.1093/neuonc/nos288
doi: 10.1093/neuonc/nos288 pubmed: 23233537
Merrell RT, Anderson SK, Meyer FB, Lachance DH (2010) Seizures in patients with glioma treated with phenytoin and levetiracetam. J Neurosurg 113(6):1176–1181. https://doi.org/10.3171/2010.5.JNS091367
doi: 10.3171/2010.5.JNS091367 pubmed: 20560728
Pallud J, Audureau E, Blonski M, Sanai N, Bauchet L, Fontaine D, Mandonnet E, Dezamis E, Psimaras D, Guyotat J, Peruzzi P, Page P, Gal B, Parraga E, Baron MH, Vlaicu M, Guillevin R, Devaux B, Duffau H, Taillandier L, Capelle L, Huberfeld G (2014) Epileptic seizures in diffuse low-grade gliomas in adults. Brain 137(Pt 2):449–462. https://doi.org/10.1093/brain/awt345
doi: 10.1093/brain/awt345 pubmed: 24374407
Yordanova YN, Moritz-Gasser S, Duffau H (2011) Awake surgery for WHO Grade II gliomas within “noneloquent” areas in the left dominant hemisphere: toward a “supratotal” resection. Clinical article. J Neurosurg 115(2):232–239. https://doi.org/10.3171/2011.3.JNS101333
doi: 10.3171/2011.3.JNS101333 pubmed: 21548750
Bate H, Eldridge P, Varma T, Wieshmann UC (2007) The seizure outcome after amygdalohippocampectomy and temporal lobectomy. Eur J Neurol 14(1):90–94. https://doi.org/10.1111/j.1468-1331.2006.01565.x
doi: 10.1111/j.1468-1331.2006.01565.x pubmed: 17222120
Duncan JS, Sagar HJ (1987) Seizure characteristics, pathology, and outcome after temporal lobectomy. Neurology 37(3):405–409. https://doi.org/10.1212/wnl.37.3.405
doi: 10.1212/wnl.37.3.405 pubmed: 3822133
Xu DS, Awad AW, Mehalechko C, Wilson JR, Ashby LS, Coons SW, Sanai N (2018) An extent of resection threshold for seizure freedom in patients with low-grade gliomas. J Neurosurg 128(4):1084–1090. https://doi.org/10.3171/2016.12.JNS161682
doi: 10.3171/2016.12.JNS161682 pubmed: 28548599
Jackson C, Westphal M, Quinones-Hinojosa A (2016) Complications of glioma surgery. Handb Clin Neurol 134:201–218. https://doi.org/10.1016/B978-0-12-802997-8.00012-8
doi: 10.1016/B978-0-12-802997-8.00012-8 pubmed: 26948356
McGirt MJ, Mukherjee D, Chaichana KL, Than KD, Weingart JD, Quinones-Hinojosa A (2009) Association of surgically acquired motor and language deficits on overall survival after resection of glioblastoma multiforme. Neurosurgery 65 (3):463–469; discussion 469–470. doi: https://doi.org/10.1227/01.NEU.0000349763.42238.E9
Zigiotto L, Annicchiarico L, Corsini F, Vitali L, Falchi R, Dalpiaz C, Rozzanigo U, Barbareschi M, Avesani P, Papagno C, Duffau H, Chioffi F, Sarubbo S (2020) Effects of supra-total resection in neurocognitive and oncological outcome of high-grade gliomas comparing asleep and awake surgery. J Neurooncol 148(1):97–108. https://doi.org/10.1007/s11060-020-03494-9
doi: 10.1007/s11060-020-03494-9 pubmed: 32303975
Schneider M, Güresir A, Borger V, Hamed M, Racz A, Vatter H, Güresir E, Schuss P (2019) Preoperative tumor-associated epilepsy in patients with supratentorial meningioma: factors influencing seizure outcome after meningioma surgery. J Neurosurg. https://doi.org/10.3171/2019.7.JNS19455
doi: 10.3171/2019.7.JNS19455 pubmed: 31604333

Auteurs

Valeri Borger (V)

Department of Neurosurgery, University Hospital Bonn, Venusberg-Campus 1, 53127, Bonn, Germany. valeri.borger@ukbonn.de.

Motaz Hamed (M)

Department of Neurosurgery, University Hospital Bonn, Venusberg-Campus 1, 53127, Bonn, Germany.

Inja Ilic (I)

Department of Neurosurgery, University Hospital Bonn, Venusberg-Campus 1, 53127, Bonn, Germany.

Anna-Laura Potthoff (AL)

Department of Neurosurgery, University Hospital Bonn, Venusberg-Campus 1, 53127, Bonn, Germany.

Attila Racz (A)

Department of Epileptology, University Hospital Bonn, Bonn, Germany.

Niklas Schäfer (N)

Division of Clinical Oncology, Department of Neurology, University Hospital Bonn, Bonn, Germany.

Erdem Güresir (E)

Department of Neurosurgery, University Hospital Bonn, Venusberg-Campus 1, 53127, Bonn, Germany.

Rainer Surges (R)

Department of Epileptology, University Hospital Bonn, Bonn, Germany.

Ulrich Herrlinger (U)

Division of Clinical Oncology, Department of Neurology, University Hospital Bonn, Bonn, Germany.

Hartmut Vatter (H)

Department of Neurosurgery, University Hospital Bonn, Venusberg-Campus 1, 53127, Bonn, Germany.

Matthias Schneider (M)

Department of Neurosurgery, University Hospital Bonn, Venusberg-Campus 1, 53127, Bonn, Germany.

Patrick Schuss (P)

Department of Neurosurgery, University Hospital Bonn, Venusberg-Campus 1, 53127, Bonn, Germany.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH