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What surgical approach for left-sided eloquent glioblastoma: biopsy, resection under general anesthesia or awake craniotomy?

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Abstract

Purpose

Neurosurgeons use three main surgical approaches for left-sided glioblastoma (GB) in eloquent areas: biopsy, tumor resection under general anesthesia (GA), and awake craniotomy (AC) with brain mapping for maximal safe resection. We performed a retrospective study of functional and survival outcomes for left-sided eloquent GB, comparing these surgical approaches.

Methods

We included 87 patients with primary left-sided eloquent GB from two centers, one performing AC and the other biopsy or resection under GA. We assessed Karnofsky performance score (KPS), language and motor deficits one month after surgery, progression-free survival (PFS) and overall survival (OS).

Results

The 87 patients had a median PFS of 8.6 months [95% CI: 7.3–11.6] and a median OS of 20.2 months [17-3-24.4], with no significant differences between the three surgical approaches. One month after surgery, functional outcomes for language were similar for all approaches, but motor function was poorer in the biopsy group than in other patients. The proportion of patients with a KPS score > 80 was higher in the resection with AC group than in the other patients at this timepoint.

Conclusion

We detected no real benefit of a resection with AC over resection under GA for left-sided eloquent GB in terms of survival or functional outcomes for language. However, given the poorer motor function of biopsy patients, resection with AC should be proposed, when possible, to patients ineligible for surgical resection under GA, to improve functional outcomes and patient autonomy.

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Abbreviations

AC:

awake craniotomy

EOR:

extent of resection

GA:

general anesthesia

GB:

glioblastoma

GTR:

gross total resection

KPS:

Karnofsky performance score

PFS:

progression-free survival

STR:

subtotal resection

References

  1. Miller KD, Ostrom QT, Kruchko C et al (2021) Brain and other central nervous system tumor statistics, 2021. CA Cancer J Clin 71:381–406. https://doi.org/10.3322/caac.21693

    Article  PubMed  Google Scholar 

  2. Grochans S, Cybulska AM, Simińska D et al (2022) Epidemiology of Glioblastoma Multiforme-Literature Review. https://doi.org/10.3390/cancers14102412. Cancers 14:

  3. Stupp R, Hegi ME, Mason WP et al (2009) Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 10:459–466. https://doi.org/10.1016/S1470-2045(09)70025-7

    Article  CAS  PubMed  Google Scholar 

  4. Chaichana KL, Jusue-Torres I, Navarro-Ramirez R et al (2014) Establishing percent resection and residual volume thresholds affecting survival and recurrence for patients with newly diagnosed intracranial glioblastoma. Neuro-Oncol 16:113–122. https://doi.org/10.1093/neuonc/not137

    Article  PubMed  Google Scholar 

  5. Keime-Guibert F, Chinot O, Taillandier L et al (2007) Radiotherapy for glioblastoma in the elderly. N Engl J Med 356:1527–1535. https://doi.org/10.1056/NEJMoa065901

    Article  CAS  PubMed  Google Scholar 

  6. Lacroix M, Abi-Said D, Fourney DR et al (2001) A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 95:190–198. https://doi.org/10.3171/jns.2001.95.2.0190

    Article  CAS  PubMed  Google Scholar 

  7. Li YM, Suki D, Hess K, Sawaya R (2016) The influence of maximum safe resection of glioblastoma on survival in 1229 patients: Can we do better than gross-total resection? J Neurosurg 124:977–988. https://doi.org/10.3171/2015.5.JNS142087

    Article  PubMed  Google Scholar 

  8. Orringer D, Lau D, Khatri S et al (2012) Extent of resection in patients with glioblastoma: limiting factors, perception of resectability, and effect on survival. J Neurosurg 117:851–859. https://doi.org/10.3171/2012.8.JNS12234

    Article  PubMed  Google Scholar 

  9. Stummer W, van den Bent MJ, Westphal M (2011) Cytoreductive surgery of glioblastoma as the key to successful adjuvant therapies: new arguments in an old discussion. Acta Neurochir (Wien) 153:1211–1218. https://doi.org/10.1007/s00701-011-1001-x

    Article  PubMed  Google Scholar 

  10. Giussani C, Di Cristofori A (2020) Awake craniotomy for glioblastomas: is it worth it? Considerations about the article entitled “Impact of intraoperative stimulation mapping on high-grade glioma surgery outcome: a meta-analysis”. Acta Neurochir (Wien) 162:427–428. https://doi.org/10.1007/s00701-019-04173-z

    Article  PubMed  Google Scholar 

  11. Müller DMJ, Robe PAJT, Eijgelaar RS et al (2019) Comparing Glioblastoma Surgery Decisions Between Teams Using Brain Maps of Tumor Locations, Biopsies, and Resections. JCO Clin Cancer Inform 3:1–12. https://doi.org/10.1200/CCI.18.00089

    Article  PubMed  Google Scholar 

  12. BROWN JW, HÉCAEN H (1976) Lateralization and language representation. Neurology 26:183. https://doi.org/10.1212/WNL.26.2.183

    Article  CAS  PubMed  Google Scholar 

  13. Lemée J-M, Berro DH, Bernard F et al (2019) Resting-state functional magnetic resonance imaging versus task-based activity for language mapping and correlation with perioperative cortical mapping. Brain Behav 9:e01362. https://doi.org/10.1002/brb3.1362

    Article  PubMed  PubMed Central  Google Scholar 

  14. Bernard F, Lemée J-M, Ter Minassian A, Menei P (2018) Right Hemisphere Cognitive Functions: From Clinical and Anatomic Bases to Brain Mapping During Awake Craniotomy Part I: Clinical and Functional Anatomy. World Neurosurg 118:348–359. https://doi.org/10.1016/j.wneu.2018.05.024

    Article  PubMed  Google Scholar 

  15. Lemée J-M, Bernard F, Ter Minassian A, Menei P (2018) Right Hemisphere Cognitive Functions: From Clinical and Anatomical Bases to Brain Mapping During Awake Craniotomy. Part II: Neuropsychological Tasks and Brain Mapping. World Neurosurg 118:360–367. https://doi.org/10.1016/j.wneu.2018.07.099

    Article  PubMed  Google Scholar 

  16. Duffau H (2018) Is non-awake surgery for supratentorial adult low-grade glioma treatment still feasible? Neurosurg Rev 41:133–139. https://doi.org/10.1007/s10143-017-0918-9

    Article  PubMed  Google Scholar 

  17. Clavreul A, Aubin G, Delion M et al (2021) What effects does awake craniotomy have on functional and survival outcomes for glioblastoma patients? J Neurooncol 151:113–121. https://doi.org/10.1007/s11060-020-03666-7

    Article  PubMed  Google Scholar 

  18. Gerritsen JKW, Viëtor CL, Rizopoulos D et al (2019) Awake craniotomy versus craniotomy under general anesthesia without surgery adjuncts for supratentorial glioblastoma in eloquent areas: a retrospective matched case-control study. Acta Neurochir (Wien) 161:307–315. https://doi.org/10.1007/s00701-018-03788-y

    Article  PubMed  Google Scholar 

  19. Gerritsen JKW, Arends L, Klimek M et al (2019) Impact of intraoperative stimulation mapping on high-grade glioma surgery outcome: a meta-analysis. Acta Neurochir (Wien) 161:99–107. https://doi.org/10.1007/s00701-018-3732-4

    Article  PubMed  Google Scholar 

  20. Li Y-C, Chiu H-Y, Lin Y-J et al (2021) The Merits of Awake Craniotomy for Glioblastoma in the Left Hemispheric Eloquent Area: One Institution Experience. Clin Neurol Neurosurg 200:106343. https://doi.org/10.1016/j.clineuro.2020.106343

    Article  PubMed  Google Scholar 

  21. Moiraghi A, Roux A, Peeters S et al (2021) Feasibility, Safety and Impact on Overall Survival of Awake Resection for Newly Diagnosed Supratentorial IDH-Wildtype Glioblastomas in Adults. Cancers 13. https://doi.org/10.3390/cancers13122911

  22. Nakajima R, Kinoshita M, Okita H et al (2019) Awake surgery for glioblastoma can preserve independence level, but is dependent on age and the preoperative condition. J Neurooncol. https://doi.org/10.1007/s11060-019-03216-w

    Article  PubMed  Google Scholar 

  23. Zhang JJY, Lee KS, Voisin MR et al (2020) Awake craniotomy for resection of supratentorial glioblastoma: a systematic review and meta-analysis. Neuro-Oncol Adv 2:vdaa111. https://doi.org/10.1093/noajnl/vdaa111

    Article  Google Scholar 

  24. Zigiotto L, Annicchiarico L, Corsini F et al (2020) Effects of supra-total resection in neurocognitive and oncological outcome of high-grade gliomas comparing asleep and awake surgery. J Neurooncol 148:97–108. https://doi.org/10.1007/s11060-020-03494-9

    Article  PubMed  Google Scholar 

  25. Delion M, Klinger E, Bernard F et al (2020) Immersing Patients in a Virtual Reality Environment for Brain Mapping During Awake Surgery: Safety Study. World Neurosurg 134:e937–e943. https://doi.org/10.1016/j.wneu.2019.11.047

    Article  PubMed  Google Scholar 

  26. Wen PY, Macdonald DR, Reardon DA et al (2010) Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J Clin Oncol Off J Am Soc Clin Oncol 28:1963–1972. https://doi.org/10.1200/JCO.2009.26.3541

    Article  Google Scholar 

  27. Coluccia D, Roth T, Marbacher S, Fandino J (2018) Impact of Laterality on Surgical Outcome of Glioblastoma Patients: A Retrospective Single-Center Study. World Neurosurg 114:e121–e128. https://doi.org/10.1016/j.wneu.2018.02.084

    Article  PubMed  Google Scholar 

  28. Hrabalek L, Kalita O, Vaverka M et al (2015) Resection versus biopsy of glioblastomas in eloquent brain areas. Biomed Pap Med Fac Univ Palacky Olomouc Czechoslov 159:150–155. https://doi.org/10.5507/bp.2013.052

    Article  Google Scholar 

  29. McGirt MJ, Mukherjee D, Chaichana KL et al (2009) Association of surgically acquired motor and language deficits on overall survival after resection of glioblastoma multiforme. Neurosurgery 65:463–469 discussion 469–470. https://doi.org/10.1227/01.NEU.0000349763.42238.E9

    Article  PubMed  Google Scholar 

  30. Rahman M, Abbatematteo J, De Leo EK et al (2017) The effects of new or worsened postoperative neurological deficits on survival of patients with glioblastoma. J Neurosurg 127:123–131. https://doi.org/10.3171/2016.7.JNS16396

    Article  PubMed  Google Scholar 

  31. Sanai N, Martino J, Berger MS (2012) Morbidity profile following aggressive resection of parietal lobe gliomas. J Neurosurg 116:1182–1186. https://doi.org/10.3171/2012.2.JNS111228

    Article  PubMed  Google Scholar 

  32. Kim Y-J, Lee DJ, Park C-K, Kim IA (2019) Optimal extent of resection for glioblastoma according to site, extension, and size: a population-based study in the temozolomide era. Neurosurg Rev 42:937–950. https://doi.org/10.1007/s10143-018-01071-3

    Article  PubMed  Google Scholar 

  33. Paiva WS, Fonoff ET, Beer-Furlan A et al (2019) Evaluation of Postoperative Deficits following Motor Cortex Tumor Resection using Small Craniotomy. Surg J N Y N 5:e8–e13. https://doi.org/10.1055/s-0039-1679931

    Article  Google Scholar 

  34. Serletis D, Bernstein M (2007) Prospective study of awake craniotomy used routinely and nonselectively for supratentorial tumors. J Neurosurg 107:1–6. https://doi.org/10.3171/JNS-07/07/0001

    Article  PubMed  Google Scholar 

  35. De Witt Hamer PC, Robles SG, Zwinderman AH et al (2012) Impact of intraoperative stimulation brain mapping on glioma surgery outcome: a meta-analysis. J Clin Oncol Off J Am Soc Clin Oncol 30:2559–2565. https://doi.org/10.1200/JCO.2011.38.4818

    Article  Google Scholar 

  36. Duffau H (2005) Lessons from brain mapping in surgery for low-grade glioma: insights into associations between tumour and brain plasticity. Lancet Neurol 4:476–486. https://doi.org/10.1016/S1474-4422(05)70140-X

    Article  PubMed  Google Scholar 

  37. Eseonu CI, Rincon-Torroella J, ReFaey K et al (2017) Awake Craniotomy vs Craniotomy Under General Anesthesia for Perirolandic Gliomas: Evaluating Perioperative Complications and Extent of Resection. Neurosurgery 81:481–489. https://doi.org/10.1093/neuros/nyx023

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  39. Berger MS, Ojemann GA, Lettich E (1990) Neurophysiological monitoring during astrocytoma surgery. Neurosurg Clin N Am 1:65–80

    Article  CAS  PubMed  Google Scholar 

  40. Ojemann JG, Miller JW, Silbergeld DL (1996) Preserved function in brain invaded by tumor. Neurosurgery 39:253–258 discussion 258–259. https://doi.org/10.1097/00006123-199608000-00003

    Article  CAS  PubMed  Google Scholar 

  41. Schupper AJ, Rao M, Mohammadi N et al (2021) Fluorescence-Guided Surgery: A Review on Timing and Use in Brain Tumor Surgery. Front Neurol 12:682151. https://doi.org/10.3389/fneur.2021.682151

    Article  PubMed  PubMed Central  Google Scholar 

  42. Sanai N, Mirzadeh Z, Berger MS (2008) Functional outcome after language mapping for glioma resection. N Engl J Med 358:18–27. https://doi.org/10.1056/NEJMoa067819

    Article  CAS  PubMed  Google Scholar 

  43. Saito T, Muragaki Y, Tamura M et al (2022) Awake craniotomy with transcortical motor evoked potential monitoring for resection of gliomas within or close to motor-related areas: validation of utility for predicting motor function. J Neurosurg 136:1052–1061. https://doi.org/10.3171/2021.3.JNS21374

    Article  PubMed  Google Scholar 

  44. Szelényi A, Hattingen E, Weidauer S et al (2010) Intraoperative motor evoked potential alteration in intracranial tumor surgery and its relation to signal alteration in postoperative magnetic resonance imaging. Neurosurgery 67:302–313. https://doi.org/10.1227/01.NEU.0000371973.46234.46

    Article  PubMed  Google Scholar 

  45. Brown TJ, Glantz M (2016) Extent of Resection and Survival in Glioblastoma Multiforme-Reply. JAMA Oncol 2:1509–1510. https://doi.org/10.1001/jamaoncol.2016.3812

    Article  PubMed  Google Scholar 

  46. Incekara F, Smits M, van der Voort SR et al (2020) The Association Between the Extent of Glioblastoma Resection and Survival in Light of MGMT Promoter Methylation in 326 Patients With Newly Diagnosed IDH-Wildtype Glioblastoma. Front Oncol 10:1087. https://doi.org/10.3389/fonc.2020.01087

    Article  PubMed  PubMed Central  Google Scholar 

  47. Revilla-Pacheco F, Rodríguez-Salgado P, Barrera-Ramírez M et al (2021) Extent of resection and survival in patients with glioblastoma multiforme: Systematic review and meta-analysis. Med (Baltim) 100:e26432. https://doi.org/10.1097/MD.0000000000026432

    Article  CAS  Google Scholar 

  48. Clavreul A, Soulard G, Lemée J-M et al (2019) The French glioblastoma biobank (FGB): a national clinicobiological database. J Transl Med 17:133. https://doi.org/10.1186/s12967-019-1859-6

    Article  PubMed  PubMed Central  Google Scholar 

  49. Jakola AS, Gulati S, Weber C et al (2011) Postoperative deterioration in health related quality of life as predictor for survival in patients with glioblastoma: a prospective study. PLoS ONE 6:e28592. https://doi.org/10.1371/journal.pone.0028592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Gerritsen JKW, Klimek M, Dirven CMF et al (2019) The SAFE-trial: Safe surgery for glioblastoma multiforme: Awake craniotomy versus surgery under general anesthesia. Study protocol for a multicenter prospective randomized controlled trial. Contemp Clin Trials 88:105876. https://doi.org/10.1016/j.cct.2019.105876

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank the neuroradiologists, neuropathologists, radiation oncologists and medical oncologists who followed patients. We also thank Ghislaine Aubin and Gwénaëlle Soulard for their help in data recovery and exploitation and Alex Edelman and Associates for correcting the manuscript. We would like also to thank the French Glioblastoma Biobank (CHU Angers, Angers, France).

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Authors and Affiliations

  1. Département de Neurochirurgie, CHU Angers, 4 rue Larrey, 49 933 Angers Cedex 9, Angers, France

    Clémentine Gallet, Anne Clavreul, Matthieu Delion, Nolwenn Madec, Philippe Menei & Jean-Michel Lemée

  2. Université d’Angers, Inserm UMR 1307, CNRS UMR 6075, Nantes Université, CRCI2NA, Angers, France

    Anne Clavreul, Philippe Menei & Jean-Michel Lemée

  3. Département de Neurochirurgie, CHU Rennes, Rennes, France

    Xavier Morandi

  4. Laboratoire d’Anatomie et d’Organogenèse, Faculté de Médecine, CHU Rennes, Rennes, France

    Xavier Morandi

  5. Les Capucins, centre de rééducation et réadaptation fonctionnelle adulte et pédiatrique, Angers, France

    Nolwenn Madec

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  1. Clémentine Gallet
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  2. Anne Clavreul
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Contributions

All authors contributed to study conception and design. The data were collected and analyzed by Clémentine Gallet, Anne Clavreul and Jean-Michel Lemée. The first draft of the manuscript was written by Clémentine Gallet and all the authors commented on intermediate versions of the manuscript. All the authors have read and approved the final manuscript.

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Correspondence to Jean-Michel Lemée.

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Gallet, C., Clavreul, A., Morandi, X. et al. What surgical approach for left-sided eloquent glioblastoma: biopsy, resection under general anesthesia or awake craniotomy?. J Neurooncol 160, 445–454 (2022). https://doi.org/10.1007/s11060-022-04163-9

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