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Performance of intraoperative neurocognitive tests during awake surgery for patients with diffuse low-grade glioma

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Abstract

Despite great advancements and the diffusion of awake surgery for brain tumors, the literature shows that the tests applied during the procedure are heterogeneous and non-standardized. This prospective, observational, descriptive study collected data on intraoperative brain mapping and the performance of multiple neurocognitive tests in 51 awake surgeries for diffuse low-grade glioma. Frequency of use and rate of intraoperative findings of different neurocognitive tests were analyzed. Patients mean age at the time of surgery was 35.1 (20–57) years. We performed 26 (51.0%) surgeries on the left hemisphere (LH) and 25 (49.0%) on the right hemisphere (RH). Significant differences were observed between the total number of functional findings (cortical and subcortical) identified in the LH and RH (p = 0.004). In subcortical findings alone, the differences remained significant (p = 0.0004). The RH subcortical region showed the lowest number of intraoperative findings, and this was correlated with functional outcome: Karnofsky performance scale at five days (p = 0.022), three months (p = 0.002) and one year (p = 0.002) post-surgery. On average, more tests were used to map the RH, with a lower frequency of both cortical and subcortical functional findings. Even though subcortical findings were less frequent than cortical findings, they were crucial to defining the resection margins. Based on the intraoperative findings, frequency of use, and rate of findings per use of the tests analyzed, the most relevant tests for each hemisphere for awake brain mapping were identified.

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References

  1. Rofes A, Mandonnet E, Godden J, Baron MH, Colle H, Darlix A, de Aguiar V, Duffau H, Herbet G, Klein M, Lubrano V, Martino J, Mathew R, Miceli G, Moritz-Gasser S, Pallud J, Papagno C, Rech F, Robert E, Rutten GJ, Santarius T, Satoer D, Sierpowska J, Smits A, Skrap M, Spena G, Visch E, De Witte E, Zetterling M, Wager M (2017) Survey on current cognitive practices within the European Low-Grade Glioma Network: towards a European assessment protocol. Acta Neurochir (Wien) 159(7):1167–1178. https://doi.org/10.1007/s00701-017-3192-2

    Article  PubMed  Google Scholar 

  2. Albuquerque LAF, Filho LJMM, Borges FS, Pessoa FC, Diógenes GS, Rocha CJV, Almeida JP, Joaquim AF (2023) awake craniotomy for diffuse low grade gliomas in a resource limited setting: lessons learned with a consecutive series of 51 surgeries. World Neurosurg S1878–8750(23):00879–3. https://doi.org/10.1016/j.wneu.2023.06.096

    Article  Google Scholar 

  3. Louis DN, Perry A, Reifenberger G, et al (2016) The 2016 World health organization classification of tumors of the central nervous system: a summary. Mapping of visuospatial functions during brain surgery: a new tool to prevent unilateral spatial neglect 131:803-820

  4. FernándezCoello A, Moritz-Gasser S, Martino J, Martinoni M, Matsuda R, Duffau H (2013) Selection of intraoperative tasks for awake mapping based on relationships between tumor location and functional networks. J Neurosurg 119(6):1380–94. https://doi.org/10.3171/2013.6.JNS122470

    Article  Google Scholar 

  5. Duffau H (2015) Stimulation mapping of white matter tracts to study brain functional connectivity. Nat Rev Neurol 11(5):255–65

    Article  PubMed  Google Scholar 

  6. Vilasboas T, Herbet G, Duffau H (2017) Challenging the myth of right “non-dominant” hemisphere: Lessons from cortico-subcortical stimulation mapping in awake surgery and surgical implications. World Neurosurg 103:449–456

    Article  PubMed  Google Scholar 

  7. Metz-Lutz MN, Kremin H, Deloche G (1991) Standardisation d’un test de dénomination orale: contrôle des effets de l’âge, du sexe et du niveau de scolarité chez les sujets adultes normaux. Rev Neuropsychol 1:73–95

    Google Scholar 

  8. Moritz-Gasser S, Herbet G, Duffau H (2013) Mapping the connectivity underlying multimodal (verbal and non-verbal) semantic processing: A brain electrostimulation study. Neuropsychologia 51(10):1814–22

    Article  PubMed  Google Scholar 

  9. 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. J Neurosurg 115(2):232–9. https://doi.org/10.3171/2011.3.JNS101333

  10. Howard D, Patterson K (1992) The pyramid and palm trees test: A test of semantic access from words and pictures. Bury St Edmonds: Thames Valley Test Company

  11. Zemmoura I, Herbet G, Moritz-Gasser S, Duffau H (2015) New insights into the neural network mediating reading processes provided by cortico-subcortical electrical mapping. Hum Brain Mapp 36(6):2215–30. https://doi.org/10.1002/hbm.22766

    Article  PubMed  PubMed Central  Google Scholar 

  12. Parente MAMP, Fonseca RP, Pagliarin KC, Barreto SS, Soares-Ishigaki ECS, Hübner LC, Joanette Y, Nespoulous J-L, Ortiz KZ (2016) Bateria Montreal Toulouse de Avaliação da Linguagem (MTL-Brasil). 1ª Edição. São Paulo: Vetor. Portuguese

  13. Fonseca RP, Salles JF, Parente MAMP (2009) NEUPSILIN: Instrumento de Avaliação Neuropsicológica Breve: Manual. 1ª Edição; São Paulo: Vetor. Portuguese

  14. Gras-Combe G, Moritz-Gasser S, Herbet G, Duffau H (2012) Intraoperative subcortical electrical mapping of optic radiations in awake surgery for glioma involving visual pathways. J Neurosurg 117(3):466–73

    Article  PubMed  Google Scholar 

  15. Montemurro N, Herbet G, Duffau H (2016) Right cortical and axonal structures eliciting ocular deviation during electrical stimulation mapping in awake patients. Brain Topogr 29(4):561–71. https://doi.org/10.1007/s10548-016-0490-6

    Article  PubMed  Google Scholar 

  16. Stroop JR (1935) Studies of interference in serial verbal reactions. J Exp Psychol 18:643

    Article  Google Scholar 

  17. Bartolomeo P, Thiebaut de Schotten M, Duffau H (2007) Mapping of visuospatial functions during brain surgery: a new tool to prevent unilateral spatial neglect. Neurosurgery 61(6):E1340

    Article  PubMed  Google Scholar 

  18. Herbet G, Lafargue G, Moritz-Gasser S, Bonnetblanc F, Duffau H (2015) Interfering with the neural activity of mirror-related frontal areas impairs mentalistic inferences. Brain Struct Funct 220(4):2159–69

    Article  PubMed  Google Scholar 

  19. Herbet G, Lafargue G, de Champfleur NM, Moritz-Gasser S, le Bars E, Bonnetblanc F, Duffau H (2014) Disrupting posterior cingulate connectivity disconnects consciousness from the external environment. Neuropsychologia 56:239–44. https://doi.org/10.1016/j.neuropsychologia.2014.01.020

    Article  PubMed  Google Scholar 

  20. Herbet G, Lafargue G, Duffau H (2016) The dorsal cingulate cortex as a critical gateway in the network supporting conscious awareness. Brain. 139(Pt 4):e23. https://doi.org/10.1093/brain/awv381

    Article  PubMed  Google Scholar 

  21. Rech F, Duffau H, Pinelli C, Masson A, Roublot P, Billy-Jacques A, Brissart H, Civit T (2017) Intraoperative identification of the negative motor network during awake surgery to prevent deficit following brain resection in premotor regions. Neurochirurgie 63(3):235–242

    Article  CAS  PubMed  Google Scholar 

  22. Duffau H (2022) Repeated awake surgical resection(s) for recurrent diffuse low-grade gliomas: why, when, and how to reoperate? Front Oncol 12:947933. https://doi.org/10.3389/fonc.2022.947933

    Article  PubMed  PubMed Central  Google Scholar 

  23. Pertichetti M, Corbo D, Belotti F, Saviola F, Gasparotti R, Fontanella MM, Panciani PP (2023) Neuropsychological evaluation and functional magnetic resonance imaging tasks in the preoperative assessment of patients with brain tumors: a systematic review. Brain Sci 13(10):1380. https://doi.org/10.3390/brainsci13101380

    Article  PubMed  PubMed Central  Google Scholar 

  24. Ius T, Angelini E, Thiebaut de Schotten M, Mandonnet E, Duffau H (2011) Evidence for potentials and limitations of brain plasticity using an atlas of functional resectability of WHO grade II gliomas: towards a “minimal common brain.” Neuroimage 56(3):992–1000. https://doi.org/10.1016/j.neuroimage.2011.03.022

    Article  PubMed  Google Scholar 

  25. Collée E, Vincent A, Visch-Brink E, De Witte E, Dirven C, Satoer D (2023Jan 20) Localization patterns of speech and language errors during awake brain surgery: a systematic review. Neurosurg Rev 46(1):38. https://doi.org/10.1007/s10143-022-01943-9

    Article  PubMed  PubMed Central  Google Scholar 

  26. De Witte E, Satoer D, Robert E, Colle H, Verheyen S, Visch-Brink E, Mariën P (2015Jan) The Dutch Linguistic Intraoperative Protocol: a valid linguistic approach to awake brain surgery. Brain Lang 140:35–48. https://doi.org/10.1016/j.bandl.2014.10.011

    Article  PubMed  Google Scholar 

  27. Duffau H (2018Jan) Is non-awake surgery for supratentorial adult low-grade glioma treatment still feasible? Neurosurg Rev 41(1):133–139. https://doi.org/10.1007/s10143-017-0918-9

    Article  PubMed  Google Scholar 

  28. Albuquerque LAF, Almeida JP, de Macêdo Filho LJM, Joaquim AF, Duffau H (2021Jun) Extent of resection in diffuse low-grade gliomas and the role of tumor molecular signature-a systematic review of the literature. Neurosurg Rev 44(3):1371–1389. https://doi.org/10.1007/s10143-020-01362-8

    Article  PubMed  Google Scholar 

  29. Barberis M, Poisson I, Facque V, Letrange S, Prevost-Tarabon C, Houdart E, Froelich S, Levy R, Mandonnet E (2022) Group-level stability but individual variability of neurocognitive status after awake resections of right frontal IDH-mutated glioma. Sci Rep 12(1):6126. https://doi.org/10.1038/s41598-022-08702-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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All authors whose names appear on the submission: 1. made substantial contributions to the conception or design of the work; or the acquisition, analysis, or interpretation of data; 2. drafted the work or revised it critically for important intellectual content; 3. approved the version to be published; and 4. agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

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Correspondence to Lucas Alverne F. Albuquerque.

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The authors declare no competing interests.

Ethics approval

This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of Hospital Geral de Fortaleza (Date: 07/24/2017, number 2.216.138).

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Informed consent was obtained from all individual participants included in the study.

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The authors declare no competing interests.

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The authors of the article “Performance of intraoperative neurocognitive tests during awake surgery for patients with diffuse low-grade glioma” declare that this is an original unpublished article that does not transgress any copyright or intellectual property rights of other people and it is not being evaluated for publication in other journals. Every author has contributed substantially to achieving this work. This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors. None of the authors have conflicts of interest to report.

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Albuquerque, L.A.F., de Macêdo Filho, L.J.M., Borges, F.S. et al. Performance of intraoperative neurocognitive tests during awake surgery for patients with diffuse low-grade glioma. Neurosurg Rev 47, 129 (2024). https://doi.org/10.1007/s10143-024-02364-6

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