Skip to main content

Advertisement

SpringerLink
Log in

Glioma surgery with awake language mapping versus generalized anesthesia: a systematic review

  • Review
  • Published:
Neurosurgical Review Aims and scope Submit manuscript

Abstract

Awake craniotomy with language mapping is being increasingly applied to avoid postoperative language dysfunctions worldwide. However, the effectiveness and reliability of this technique remain unclear due to the paucity of studies comparing the awake craniotomy with general anesthesia. To determine the benefit of awake craniotomy for language, motor, and neurological functions, as well as other clinical outcomes, we searched Medline, Embase, the Cochrane Library, and the Chinese Biomedical Literature Database up to December 2019. Gray literatures were also searched. We included randomized and non-randomized controlled studies comparing awake craniotomy versus general anesthetic resection and reporting the language and neurological outcomes. Ten studies with 833 patients were included in the meta-analysis. The pooled risk ratio (RR) suggested no significant differences in language and neurological outcomes between general anesthesia group and awake craniotomy group without electrical stimulation. Awake craniotomy with electrical stimulation, however, was associated with improved late language and neurological outcomes (≥ 3 months) versus general anesthesia with pooled RR of 0.44 (95% CI = 0.20–0.96) and 0.49 (95% CI = 0.30–0.79), respectively. Awake craniotomy with electrical stimulation was also associated with better extent of resection with the pooled RR of 0.81 (95%CI = 0.71–0.92) and shorter hospital stay duration with the pooled weighted mean difference (WMD) of − 1.14 (95%CI = − 1.80 to − 0.48). This meta-analysis suggested that the application of awake craniotomy with electrical stimulation during glioma resection is associated with lower risks of long-term neurological and language deficits and higher extent of tumor resection, as well as shorter hospital stay duration.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Ali MZE, Fadel NA, Abouldahab HA (2009) Awake craniotomy versus general anesthesia for managing eloquent cortex low-grade gliomas. Neurosciences 14:263–272

    PubMed  Google Scholar 

  2. Bizzi A, Blasi V, Falini A, Ferroli P, Cadioli M, Danesi U, Aquino D, Marras C, Caldiroli D, Broggi G (2008) Presurgical functional MR imaging of language and motor functions: validation with intraoperative electrocortical mapping. Radiology 248:579–589

    Article  PubMed  Google Scholar 

  3. Borchers S, Himmelbach M, Logothetis N, Karnath HO (2011) Direct electrical stimulation of human cortex - the gold standard for mapping brain functions? Nat Rev Neurosci 13:63–70. https://doi.org/10.1038/nrn3140

    Article  CAS  PubMed  Google Scholar 

  4. De Witt Hamer PC, Robles SG, Zwinderman AH, Duffau H, Berger MS (2012) Impact of intraoperative stimulation brain mapping on glioma surgery outcome: a meta-analysis. J Clin Oncol 30:2559–2565. https://doi.org/10.1200/JCO.2011.38.4818

    Article  PubMed  Google Scholar 

  5. Duffau H (2015) Stimulation mapping of white matter tracts to study brain functional connectivity. Nat Rev Neurol 11:255–265. https://doi.org/10.1038/nrneurol.2015.51

    Article  PubMed  Google Scholar 

  6. Duffau H (2016) Long-term outcomes after supratotal resection of diffuse low-grade gliomas: a consecutive series with 11-year follow-up. Acta Neurochir 158:51–58. https://doi.org/10.1007/s00701-015-2621-3

    Article  PubMed  Google Scholar 

  7. Duffau H, Capelle L, Denvil D, Sichez N, Gatignol P, Lopes M, Mitchell MC, Sichez JP, Van Effenterre R (2003) Functional recovery after surgical resection of low grade gliomas in eloquent brain: hypothesis of brain compensation. J Neurol Neurosurg Psychiatry 74:901–907. https://doi.org/10.1136/jnnp.74.7.901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Duffau H, Lopes M, Arthuis F, Bitar A, Sichez JP, Van Effenterre R, Capelle L (2005) Contribution of intraoperative electrical stimulations in surgery of low grade gliomas: a comparative study between two series without (1985-96) and with (1996-2003) functional mapping in the same institution. J Neurol Neurosurg Psychiatry 76:845–851. https://doi.org/10.1136/jnnp.2004.048520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Duncan J (2010) The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour. Trends Cogn Sci 14:172–179. https://doi.org/10.1016/j.tics.2010.01.004

    Article  PubMed  Google Scholar 

  10. Eseonu CI, Rincon-Torroella J, ReFaey K, Lee YM, Nangiana J, Vivas-Buitrago T, Quinones-Hinojosa A (2017) Awake craniotomy vs craniotomy under general anesthesia for perirolandic gliomas: evaluating perioperative complications and extent of resection. Neurosurgery 81:481–489

    Article  PubMed  Google Scholar 

  11. Fornia L, Puglisi G, Leonetti A, Bello L, Berti A, Cerri G, Garbarini F (2020) Direct electrical stimulation of the premotor cortex shuts down awareness of voluntary actions. Nat Commun 11:705. https://doi.org/10.1038/s41467-020-14517-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Gasquoine PG (2014) Contributions of the insula to cognition and emotion. Neuropsychol Rev 24:77–87. https://doi.org/10.1007/s11065-014-9246-9

    Article  PubMed  Google Scholar 

  13. Gupta DK, Chandra PS, Ojha BK, Sharma BS, Mahapatra AK, Mehta VS (2007) Awake craniotomy versus surgery under general anesthesia for resection of intrinsic lesions of eloquent cortex--a prospective randomised study. Clin Neurol Neurosurg 109:335–343. https://doi.org/10.1016/j.clineuro.2007.01.008

    Article  PubMed  Google Scholar 

  14. Hart MG, Garside R, Rogers G, Stein K, Grant R (2013) Temozolomide for high grade glioma. Cochrane Database Syst Rev:CD007415. https://doi.org/10.1002/14651858.CD007415.pub2

  15. Herbet G, Duffau H (2020) Revisiting the functional anatomy of the human brain: toward a meta-networking theory of cerebral functions. Physiol Rev 100:1181–1228. https://doi.org/10.1152/physrev.00033.2019

    Article  PubMed  Google Scholar 

  16. Hervey-Jumper SL, Li J, Lau D, Molinaro AM, Perry DW, Meng L, Berger MS (2015) Awake craniotomy to maximize glioma resection: methods and technical nuances over a 27-year period. J Neurosurg 123:325–339. https://doi.org/10.3171/2014.10.JNS141520

    Article  PubMed  Google Scholar 

  17. Hickok G (2012) Computational neuroanatomy of speech production. Nat Rev Neurosci 13:135–145. https://doi.org/10.1038/nrn3158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Hickok G, Poeppel D (2007) The cortical organization of speech processing. Nat Rev Neurosci 8:393–402. https://doi.org/10.1038/nrn2113

    Article  CAS  PubMed  Google Scholar 

  19. Higgins JP, Altman DG, Gotzsche PC, Juni P, Moher D, Oxman AD, Savovic J, Schulz KF, Weeks L, Sterne JA, Cochrane Bias Methods G, Cochrane Statistical Methods G (2011) The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. Bmj 343:d5928. https://doi.org/10.1136/bmj.d5928

    Article  PubMed  PubMed Central  Google Scholar 

  20. Hu JM, Qian MZ, Tanigawa H, Song XM, Roe AW (2020) Focal electrical stimulation of cortical functional networks. Cereb Cortex. https://doi.org/10.1093/cercor/bhaa136

  21. Kuchcinski G, Mellerio C, Pallud J, Dezamis E, Turc G, Rigaux-Viode O, Malherbe C, Roca P, Leclerc X, Varlet P, Chretien F, Devaux B, Meder JF, Oppenheim C (2015) Three-Tesla functional MR language mapping: comparison with direct cortical stimulation in gliomas. Neurology 84:560–568. https://doi.org/10.1212/WNL.0000000000001226

    Article  CAS  PubMed  Google Scholar 

  22. Lee DK, Fedorenko E, Simon MV, Curry WT, Nahed BV, Cahill DP, Williams ZM (2018) Neural encoding and production of functional morphemes in the posterior temporal lobe. Nat Commun 9:1877. https://doi.org/10.1038/s41467-018-04235-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114:97–109. https://doi.org/10.1007/s00401-007-0243-4

    Article  PubMed  PubMed Central  Google Scholar 

  24. Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, Ellison DW (2016) The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary. Acta Neuropathol 131:803–820. https://doi.org/10.1007/s00401-016-1545-1

    Article  PubMed  Google Scholar 

  25. Mandelli ML, Vitali P, Santos M, Henry M, Gola K, Rosenberg L, Dronkers N, Miller B, Seeley WW, Gorno-Tempini ML (2016) Two insular regions are differentially involved in behavioral variant FTD and nonfluent/agrammatic variant PPA. Cortex 74:149–157. https://doi.org/10.1016/j.cortex.2015.10.012

    Article  PubMed  Google Scholar 

  26. Martino J, Gomez E, Bilbao JL, Duenas JC, Vazquez-Barquero A (2013) Cost-utility of maximal safe resection of WHO grade II gliomas within eloquent areas. Acta Neurochir 155:41–50

    Article  PubMed  Google Scholar 

  27. McGirt MJ, Chaichana KL, Attenello FJ, Weingart JD, Than K, Burger PC, Olivi A, Brem H, Quinones-Hinojosa A (2008) Extent of surgical resection is independently associated with survival in patients with hemispheric infiltrating low-grade gliomas. Neurosurgery 63:700–707; author reply 707-708. https://doi.org/10.1227/01.NEU.0000325729.41085.73

    Article  PubMed  Google Scholar 

  28. Moher D, Liberati A, Tetzlaff J, Altman DG, Group P (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6:e1000097. https://doi.org/10.1371/journal.pmed.1000097

    Article  PubMed  PubMed Central  Google Scholar 

  29. Motomura K, Chalise L, Ohka F, Aoki K, Tanahashi K, Hirano M, Nishikawa T, Wakabayashi T, Natsume A (2018) Supratotal resection of diffuse frontal lower grade gliomas with awake brain mapping, preserving motor, language, and neurocognitive functions. World Neurosurg 119:30–39. https://doi.org/10.1016/j.wneu.2018.07.193

    Article  PubMed  Google Scholar 

  30. Motomura K, Natsume A, Iijima K, Kuramitsu S, Fujii M, Yamamoto T, Maesawa S, Sugiura J, Wakabayashi T (2017) Surgical benefits of combined awake craniotomy and intraoperative magnetic resonance imaging for gliomas associated with eloquent areas. J Neurosurg 127:790–797. https://doi.org/10.3171/2016.9.JNS16152

    Article  PubMed  Google Scholar 

  31. 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; discussion 140. https://doi.org/10.1227/01.neu.0000429847.91707.97

    Article  PubMed  Google Scholar 

  32. 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

    Article  PubMed  Google Scholar 

  33. Oh A, Duerden EG, Pang EW (2014) The role of the insula in speech and language processing. Brain Lang 135:96–103. https://doi.org/10.1016/j.bandl.2014.06.003

    Article  PubMed  PubMed Central  Google Scholar 

  34. Ojemann G, Mateer C (1979) Human language cortex: localization of memory, syntax, and sequential motor-phoneme identification systems. Science 205:1401–1403. https://doi.org/10.1126/science.472757

    Article  CAS  PubMed  Google Scholar 

  35. Pallud J, Varlet P, Devaux B, Geha S, Badoual M, Deroulers C, Page P, Dezamis E, Daumas-Duport C, Roux FX (2010) Diffuse low-grade oligodendrogliomas extend beyond MRI-defined abnormalities. Neurology 74:1724–1731. https://doi.org/10.1212/WNL.0b013e3181e04264

    Article  CAS  PubMed  Google Scholar 

  36. Patsopoulos NA, Evangelou E, Ioannidis JP (2008) Sensitivity of between-study heterogeneity in meta-analysis: proposed metrics and empirical evaluation. Int J Epidemiol 37:1148–1157. https://doi.org/10.1093/ije/dyn065

    Article  PubMed  PubMed Central  Google Scholar 

  37. Penfield W (1954) Combined regional and general anesthesia for craniotomy and cortical exploration. I. Neurosurgical considerations. Curr Res Anesth Analg 33:145–155

    Article  CAS  PubMed  Google Scholar 

  38. Peraud A, Ilmberger J, Reulen HJ, Gerosa M, Akalan N, Baehring JM (2004) Surgical resection of gliomas WHO grade II and III located in the opercular region. Acta Neurochir 146:9–18

    Article  CAS  PubMed  Google Scholar 

  39. Peruzzi P, Bergese SD, Viloria A, Puente EG, Abdel-Rasoul M, Chiocca EA (2011) A retrospective cohort-matched comparison of conscious sedation versus general anesthesia for supratentorial glioma resection. Clinical article. J Neurosurg 114:633–639. https://doi.org/10.3171/2010.5.JNS1041

    Article  PubMed  Google Scholar 

  40. Pichierri A, Bradley M, Iyer V (2019) Intraoperative magnetic resonance imaging-guided glioma resections in awake or asleep settings and feasibility in the context of a public health system. World Neurosurg X 3:100022. https://doi.org/10.1016/j.wnsx.2019.100022

    Article  PubMed  PubMed Central  Google Scholar 

  41. 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

    Article  PubMed  Google Scholar 

  42. Sanai N, Berger MS (2018) Surgical oncology for gliomas: the state of the art. Nat Rev Clin Oncol 15:112–125. https://doi.org/10.1038/nrclinonc.2017.171

    Article  PubMed  Google Scholar 

  43. 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 

  44. 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 

  45. Skrap M, Marin D, Ius T, Fabbro F, Tomasino B (2016) Brain mapping: a novel intraoperative neuropsychological approach. J Neurosurg 125:877–887. https://doi.org/10.3171/2015.10.JNS15740

    Article  PubMed  Google Scholar 

  46. Taggart DP, Banning AP (2011) Stents and failing vein grafts: are we any wiser after ISAR? Lancet 378:1054–1055. https://doi.org/10.1016/S0140-6736(11)61340-8

    Article  PubMed  Google Scholar 

  47. Thiebaut de Schotten M, Urbanski M, Duffau H, Volle E, Levy R, Dubois B, Bartolomeo P (2005) Direct evidence for a parietal-frontal pathway subserving spatial awareness in humans. Science 309:2226–2228. https://doi.org/10.1126/science.1116251

    Article  CAS  PubMed  Google Scholar 

  48. Thulborn KR, Carpenter PA, Just MA (1999) Plasticity of language-related brain function during recovery from stroke. Stroke 30:749–754

    Article  CAS  PubMed  Google Scholar 

  49. Tsitlakidis A, Foroglou N, Venetis CA, Patsalas I, Hatzisotiriou A, Selviaridis P (2010) Biopsy versus resection in the management of malignant gliomas: a systematic review and meta-analysis. J Neurosurg 112:1020–1032. https://doi.org/10.3171/2009.7.JNS09758

    Article  PubMed  Google Scholar 

  50. Tuominen J, Yrjana S, Ukkonen A, Koivukangas J (2013) Awake craniotomy may further improve neurological outcome of intraoperative MRI-guided brain tumor surgery. Acta Neurochir 155:1805–1812. https://doi.org/10.1007/s00701-013-1837-3

    Article  PubMed  Google Scholar 

  51. Whittle IR, Pringle AM, Taylor R (1998) Effects of resective surgery for left-sided intracranial tumours on language function: a prospective study. Lancet 351:1014–1018. https://doi.org/10.1016/S0140-6736(97)08295-0

    Article  CAS  PubMed  Google Scholar 

  52. Woolnough O, Forseth KJ, Rollo PS, Tandon N (2019) Uncovering the functional anatomy of the human insula during speech. Elife 8. https://doi.org/10.7554/eLife.53086

  53. Wu JS, Gong X, Song YY, Zhuang DX, Yao CJ, Qiu TM, Lu JF, Zhang J, Zhu W, Mao Y, Zhou LF (2014) 3.0-T intraoperative magnetic resonance imaging-guided resection in cerebral glioma surgery: interim analysis of a prospective, randomized, triple-blind, parallel-controlled trial. Neurosurgery 61 Suppl 1:145–154. https://doi.org/10.1227/NEU.0000000000000372

    Article  PubMed  Google Scholar 

  54. Xia H, Huang W, Wu L, Ma H, Wang X, Chen X, Sun S, Jia X (2012) Preoperative functional MRI localization of language areas in Chinese patients with brain tumors: validation with intraoperative electrocortical mapping. Neural Regen Res 7:1563–1569. https://doi.org/10.3969/j.issn.1673-5374.2012.20.006

    Article  PubMed  PubMed Central  Google Scholar 

  55. 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 115:232–239. https://doi.org/10.3171/2011.3.JNS101333

    Article  PubMed  Google Scholar 

  56. Zelitzki R, Korn A, Arial E, Ben-Harosh C, Ram Z, Grossman R (2019) Comparison of motor outcome in patients undergoing awake vs general anesthesia surgery for brain tumors located within or adjacent to the motor pathways. Neurosurgery 85:E470–E476

    Article  PubMed  Google Scholar 

  57. Zhuang DX, Wu JS, Yao CJ, Qiu TM, Lu JF, Zhu FP, Xu G, Zhu W, Zhou LF (2016) Intraoperative multi-information-guided resection of dominant-sided insular gliomas in a 3-T intraoperative magnetic resonance imaging integrated neurosurgical suite. World Neurosurg 89:84–92. https://doi.org/10.1016/j.wneu.2016.01.067

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank the Cochrane Gynaecological and Orphan Cancer Review Group, especially Clare Jess, Managing Editor, for her support and guidance; Jane Hayes, Information Manager, for helping develop the search strategy

Funding

This study was funded by the National Natural Science Foundation of China (Project No. 81701289), Shanghai Shenkang Hospital Development Center (SHDC12018114) and Shanghai Municipal Science and Technology Major Project (No.2018SHZDZX01), and ZJLab.

Author information

Authors and Affiliations

  1. Department of Neurosurgery, Huashan Hospital, Fudan University, Shanghai, 200040, China

    Ling-Hao Bu, Jie Zhang, Jun-Feng Lu & Jin-Song Wu

  2. Institute of Neurosurgery, Fudan University, Shanghai, 200040, China

    Ling-Hao Bu, Jie Zhang, Jun-Feng Lu & Jin-Song Wu

  3. Shanghai Key Laboratory of Brain Function Restoration and Neural Regeneration, Shanghai, 200040, China

    Ling-Hao Bu, Jie Zhang, Jun-Feng Lu & Jin-Song Wu

Authors
  1. Ling-Hao Bu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jie Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jun-Feng Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jin-Song Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Wu J-S designed this study. Wu J-S and Bu L-H are responsible for the execution, study coordination, manuscript writing, and data analysis. Zhang J and Lu J-F will be involved in data collection and analysis. Wu J-S supervised the study design and data analysis, and reviewed the data and the paper.

Corresponding author

Correspondence to Jie Zhang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

Not applicable as no new patients were involved in this research.

Informed consent

Not applicable as no new patients were involved in this research

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 19 kb).

ESM 2

(DOCX 14 kb).

ESM 3

(DOC 43 kb).

ESM 4

(DOC 64 kb).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bu, LH., Zhang, J., Lu, JF. et al. Glioma surgery with awake language mapping versus generalized anesthesia: a systematic review. Neurosurg Rev 44, 1997–2011 (2021). https://doi.org/10.1007/s10143-020-01418-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10143-020-01418-9

Keywords

Search

Navigation