Skip to main content

Advertisement

Log in

Awake surgery for right frontal lobe glioma can preserve visuospatial cognition and spatial working memory

  • Clinical Study
  • Published:
Journal of Neuro-Oncology Aims and scope Submit manuscript

Abstract

Purpose

Awake surgery is the standard treatment to preserve motor and language functions. This longitudinal study aimed to evaluate the resection rate and preservation of neurocognitive functions in patients with right frontal lobe glioma who underwent awake surgery.

Methods

Thirty-three patients (mean age, 48.0 years) with right frontal lobe glioma who underwent awake surgery at our hospital between 2013 and 2019 were included. Fourteen, thirteen, and six cases had WHO classification grades of II, III, and IV, respectively. We evaluated visuospatial cognition (VSC) and spatial working memory (SWM) before and three months after surgery. Relevant brain areas for VSC and SWM were intraoperatively mapped, whenever the task was successfully accomplished. Therefore, patients were divided into an intraoperative evaluation group and a non-evaluation group for each function, and the resection rate and functional outcomes were compared.

Results

The removal rate in the evaluation group for VSC and SWM were similar to that in the non-evaluation group. Chronic impairment rate of VSC was significantly lower in the evaluation than in the non-evaluation group (5.6% vs. 33.3%, p = 0.034). No patient showed postoperative SWM impairment in the evaluation group as opposed to the non-evaluation group (16.7%, p = 0.049). The probability of resection of the deeper posterior part of the middle frontal gyrus, the relevant area of VSC, was higher in the non-evaluation group than in the evaluation group.

Conclusions

We statistically verified that awake surgery for right frontal lobe glioma results in successful preservation of VSC and SWM with satisfying resection rates.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Surbeck W, Hildebrandt G, Duffau H (2015) The evolution of brain surgery on awake patients. Acta Neurochir 157:77–84. https://doi.org/10.1007/s00701-014-2249-8

    Article  PubMed  Google Scholar 

  2. 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 

  3. Mandonnet E, Sarubbo S, Duffau H (2017) Proposal of an optimized strategy for intraoperative testing of speech and language during awake mapping. Neurosurg Rev 40:29–35. https://doi.org/10.1007/s10143-016-0723-x

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  5. 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 148:97–108. https://doi.org/10.1007/s11060-020-03494-9

    Article  PubMed  Google Scholar 

  6. Suarez-Meade P, Marenco-Hillembrand L, Prevatt C, Murguia-Fuentes R, Mohamed A, Alsaeed T, Lehrer EJ, Brigham T, Ruiz-Garcia H, Sabsevitz D, Middlebrooks EH, Bechtle PS, Quinones-Hinojosa A, Chaichana KL (2020) Awake vs. asleep motor mapping for glioma resection: a systematic review and meta-analysis. Acta Neurochir 162:1709–1720. https://doi.org/10.1007/s00701-020-04357-y

    Article  PubMed  Google Scholar 

  7. Gogos AJ, Young JS, Morshed RA, Hervey-Jumper SL, Berger MS (2020) Awake glioma surgery: technical evolution and nuances. J Neurooncol 147:515–524. https://doi.org/10.1007/s11060-020-03482-z

    Article  CAS  PubMed  Google Scholar 

  8. Nakajima R, Kinoshita M, Okita H, Yahata T, Nakada M (2019a) Awake surgery for glioblastoma can preserve independence level, but is dependent on age and the preoperative condition. J Neurooncol 144:155–163. https://doi.org/10.1007/s11060-019-03216-w

    Article  PubMed  Google Scholar 

  9. Saito T, Muragaki Y, Tamura M, Maruyama T, Nitta M, Tsuzuki S, Fukui A, Kawamata T (2020) Correlation between localization of supratentorial glioma to the precentral gyrus and difficulty in identification of the motor area during awake craniotomy. J Neurosurg. https://doi.org/10.3171/2020.2.JNS193471

    Article  PubMed  Google Scholar 

  10. Klein M, Duffau H, De Witt Hamer PC (2012) Cognition and resective surgery for diffuse infiltrative glioma: an overview. J Neurooncol 108:309–318. https://doi.org/10.1007/s11060-012-0811-x

    Article  PubMed  PubMed Central  Google Scholar 

  11. Racine CA, Li J, Molinaro AM, Butowski N, Berger MS (2015) Neurocognitive function in newly diagnosed low-grade glioma patients undergoing surgical resection with awake mapping techniques. Neurosurgery 77:371–379. https://doi.org/10.1227/NEU.0000000000000779

    Article  PubMed  Google Scholar 

  12. Drewes C, Sagberg LM, Jakola AS, Solheim O (2016) Quality of life in patients with intracranial tumors: does tumor laterality matter? J Neurosurg 125:1400–1407. https://doi.org/10.3171/2015.12.JNS152252

    Article  PubMed  Google Scholar 

  13. Vilasboas T, Herbet G, Duffau H (2017) Challenging the myth of right nondominant hemisphere: lessons from corticosubcortical stimulation mapping in awake surgery and surgical implications. World Neurosurg 103:449–456. https://doi.org/10.1016/j.wneu.2017.04.021

    Article  PubMed  Google Scholar 

  14. Duffau H (2018) Awake mapping is not an additional surgical technique but an alternative philosophy in the management of low-grade glioma patients. Neurosurg Rev 41:689–691. https://doi.org/10.1007/s10143-017-0937-6

    Article  PubMed  Google Scholar 

  15. Yoshida A, Motomura K, Natsume A, Chalise L, Iijima K, Hara D, Kadono I, Wakai K, Wakabayashi T (2020) Preoperative predictive factors affecting return to work in patients with gliomas undergoing awake brain mapping. J Neurooncol 146:195–205. https://doi.org/10.1007/s11060-019-03371-0

    Article  PubMed  Google Scholar 

  16. Ng S, Herbet G, Moritz-Gasser S, Duffau H (2019) Return to work following surgery for incidental diffuse low-grade glioma: a prospective series with 74 patients. Neurosurgery. https://doi.org/10.1093/neuros/nyz513

    Article  Google Scholar 

  17. Charras P, Herbet G, Deverdun J, de Champfleur NM, Duffau H, Bartolomeo P, Bonnetblanc F (2014) Functional reorganization of the attentional networks in low-grade glioma patients: a longitudinal study. Cortex 63:27–41. https://doi.org/10.1016/j.cortex.2014.08.010

    Article  PubMed  Google Scholar 

  18. Bernard F, Lemee JM, 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 

  19. Herbet G, Moritz-Gasser S, Duffau H (2018) Electrical stimulation of the dorsolateral prefrontal cortex impairs semantic cognition. Neurology 90:e1077–e1084. https://doi.org/10.1212/WNL.0000000000005174

    Article  PubMed  Google Scholar 

  20. 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 

  21. Motomura K, Chalise L, Ohka F, Aoki K, Tanahashi K, Hirano M, Nishikawa T, Yamaguchi J, Shimizu H, Wakabayashi T, Natsume A (2019) Neurocognitive and functional outcomes in patients with diffuse frontal lower-grade gliomas undergoing intraoperative awake brain mapping. J Neurosurg. https://doi.org/10.3171/2019.3.JNS19211

    Article  PubMed  Google Scholar 

  22. Nakajima R, Kinoshita M, Miyashita K, Okita H, Genda R, Yahata T, Hayashi Y, Nakada M (2017) Damage of the right dorsal superior longitudinal fascicle by awake surgery for glioma causes persistent visuospatial dysfunction. Sci Rep 7:17158. https://doi.org/10.1038/s41598-017-17461-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Nakajima R, Kinoshita M, Okita H, Yahata T, Matsui M, Nakada M (2018) Neural networks mediating high-level mentalizing in patients with right cerebral hemispheric gliomas. Front Behav Neurosci 12:33. https://doi.org/10.3389/fnbeh.2018.00033

    Article  PubMed  PubMed Central  Google Scholar 

  24. Kinoshita M, Nakajima R, Shinohara H, Miyashita K, Tanaka S, Okita H, Nakada M, Hayashi Y (2016) Chronic spatial working memory deficit associated with the superior longitudinal fasciculus: a study using voxel-based lesion-symptom mapping and intraoperative direct stimulation in right prefrontal glioma surgery. J Neurosurg 125:1024–1032. https://doi.org/10.3171/2015.10.JNS1591

    Article  PubMed  Google Scholar 

  25. Duffau H, Capelle L, Sichez N, Denvil D, Lopes M, Sichez JP, Bitar A, Fohanno D (2002) Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomo-functional study. Brain 125:199–214. https://doi.org/10.1093/brain/awf016

    Article  PubMed  Google Scholar 

  26. 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 

  27. Kayama T (2012) The guidelines for awake craniotomy guidelines committee of the Japan awake surgery conference. Neurol Med Chir (Tokyo) 52:119–141. https://doi.org/10.2176/nmc.52.119

    Article  Google Scholar 

  28. 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 

  29. Esquenazi Y, Friedman E, Liu Z, Zhu JJ, Hsu S, Tandon N (2017) The survival advantage of “supratotal” resection of glioblastoma using selective cortical mapping and the subpial technique. Neurosurgery 81:275–288. https://doi.org/10.1093/neuros/nyw174

    Article  PubMed  Google Scholar 

  30. Azouvi P, Samuel C, Louis-Dreyfus A, Bernati T, Bartolomeo P, Beis JM, Chokron S, Leclercq M, Marchal F, Martin Y, De Montety G, Olivier S, Perennou D, Pradat-Diehl P, Prairial C, Rode G, Sieroff E, Wiart L, Rousseaux M, French Collaborative Study Group on Assessment of Unilateral N (2002) Sensitivity of clinical and behavioural tests of spatial neglect after right hemisphere stroke. J Neurol Neurosurg Psychiatry 73:160–166. https://doi.org/10.1136/jnnp.73.2.160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Verdon V, Schwartz S, Lovblad KO, Hauert CA, Vuilleumier P (2010) Neuroanatomy of hemispatial neglect and its functional components: a study using voxel-based lesion-symptom mapping. Brain 133:880–894. https://doi.org/10.1093/brain/awp305

    Article  PubMed  Google Scholar 

  32. Owen AM, McMillan KM, Laird AR, Bullmore E (2005) N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Hum Brain Map 25:46–59. https://doi.org/10.1002/hbm.20131

    Article  Google Scholar 

  33. Nakajima R, Yordanova YN, Duffau H, Herbet G (2018) Neuropsychological evidence for the crucial role of the right arcuate fasciculus in the face-based mentalizing network: a disconnection analysis. Neuropsychologia 115:179–187. https://doi.org/10.1016/j.neuropsychologia.2018.01.024

    Article  PubMed  Google Scholar 

  34. Nakajima R, Kinoshita M, Okita H, Yahata T, Nakada M (2019b) Glioma surgery under awake condition can lead to good independence and functional outcome excluding deep sensation and visuospatial cognition. Neurooncol Pract 6:354–363. https://doi.org/10.1093/nop/npy054

    Article  PubMed  Google Scholar 

  35. van Kessel E, Snijders TJ, Baumfalk AE, Ruis C, van Baarsen KM, Broekman ML, van Zandvoort MJE, Robe PA (2020) Neurocognitive changes after awake surgery in glioma patients: a retrospective cohort study. J Neurooncol 146:97–109. https://doi.org/10.1007/s11060-019-03341-6

    Article  PubMed  Google Scholar 

  36. Nakajima R, Kinoshita M, Shinohara H, Nakada M (2019) The superior longitudinal fascicle: reconsidering the fronto-parietal neural network based on anatomy and function. Brain Imag Behav. https://doi.org/10.1007/s11682-019-00187-4

    Article  Google Scholar 

  37. Lacroix M, Abi-Said D, Fourney DR, Gokaslan ZL, Shi W, DeMonte F, Lang FF, McCutcheon IE, Hassenbusch SJ, Holland E, Hess K, Michael C, Miller D, Sawaya R (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 

  38. Karnath HO, Rennig J, Johannsen L, Rorden C (2011) The anatomy underlying acute versus chronic spatial neglect: a longitudinal study. Brain 134:903–912. https://doi.org/10.1093/brain/awq355

    Article  PubMed  Google Scholar 

  39. Karnath HO, Rorden C (2012) The anatomy of spatial neglect. Neuropsychologia 50:1010–1017. https://doi.org/10.1016/j.neuropsychologia.2011.06.027

    Article  PubMed  Google Scholar 

  40. Kitabayashi T, Nakada M, Kinoshita M, Sakurai H, Kobayashi S, Okita H, Nanbu Y, Hayashi Y, Hamada J (2012) Awake surgery with line bisection task for two cases of parietal glioma in the non-dominant hemisphere. No Shinkei Geka 40:1087–1093

    PubMed  Google Scholar 

  41. Vallar G, Bello L, Bricolo E, Castellano A, Casarotti A, Falini A, Riva M, Fava E, Papagno C (2014) Cerebral correlates of visuospatial neglect: a direct cerebral stimulation study. Hum Brain Mapp 35:1334–1350. https://doi.org/10.1002/hbm.22257

    Article  PubMed  Google Scholar 

  42. Nagel BJ, Herting MM, Maxwell EC, Bruno R, Fair D (2013) Hemispheric lateralization of verbal and spatial working memory during adolescence. Brain Cogn 82:58–68. https://doi.org/10.1016/j.bandc.2013.02.007

    Article  PubMed  PubMed Central  Google Scholar 

  43. de Wilde A, Koot HM, van Lier PA (2016) Developmental links between children’s working memory and their social relations with teachers and peers in the early school years. J Abnorm Child Psychol 44:19–30. https://doi.org/10.1007/s10802-015-0053-4

    Article  PubMed  Google Scholar 

  44. Brodziak A, Brewczynski A, Bajor G (2013) Clinical significance of knowledge about the structure, function, and impairments of working memory. Med Sci Monit 19:327–338. https://doi.org/10.12659/MSM.883900

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by JSPS KAKENHI Grant Number 18K19606, 19K22801 and 20K21649.

Author information

Authors and Affiliations

Authors

Contributions

Conception and design: MN. Acquisition of data: MK, HO, YN, TY, ST, RN. Analysis and interpretation of data: MN, RN. Drafting article: MN, RN. Critically revising the article: all authors. Reviewed final version of the manuscript and approved it for submission: all authors. Study supervision: MN.

Corresponding author

Correspondence to Mitsutoshi Nakada.

Ethics declarations

Conflict of interest

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Additional information

Publisher's Note

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

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Supplementary Fig. 1 Inclusion criteria for patient selection (tiff 351 kb)

11060_2020_3656_MOESM2_ESM.tiff

Supplementary Fig. 2 Schema of intraoperative functional assessment. A, visuospatial cognition; B, spatial working memory; DES, direct electrical stimulation (tiff 749 kb)

11060_2020_3656_MOESM3_ESM.tiff

Supplementary Fig. 3 Overlap map of resection cavities showing that the dorsolateral prefrontal cortex to the posterior medial prefrontal cortex and its deep part had the greatest degree of overlap. Numbers at the upper left of the slice images indicate coordinates of the MNI template (tiff 6527 kb)

11060_2020_3656_MOESM4_ESM.tiff

Supplementary Fig. 4 Postoperative neuropsychological function including visuospatial cognition (A) and spatial working memory (B) were compared between low- and high- grade gliomas with and without postoperative treatment, respectively. Using the chi-squared test, no significant (ns) differences were observed. Red, impaired patients; blue, unimpaired patients (tiff 286 kb)

(DOCX 14 kb)

Supplementary video 1. Method for assessing visuospatial cognition via intraoperative line bisection test is shown. The audio has been translated into English (mp4 8917)

Supplementary video 2. Intraoperative assessment of spatial working memory using spatial 2-back test is shown. The audio has been translated into English (mp4 21385)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nakada, M., Nakajima, R., Okita, H. et al. Awake surgery for right frontal lobe glioma can preserve visuospatial cognition and spatial working memory. J Neurooncol 151, 221–230 (2021). https://doi.org/10.1007/s11060-020-03656-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11060-020-03656-9

Keywords

Navigation