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Functional and oncological outcomes after right hemisphere glioma resection in awake versus asleep patients: a systematic review and meta-analysis

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Abstract

The right hemisphere has been underestimated by being considered as the non-dominant hemisphere. However, it is involved in many functions, including movement, language, cognition, and emotion. Therefore, because lesions on this side are usually not resected under awake mapping, there is a risk of unfavorable neurological outcomes. The goal of this study is to compare the functional and oncological outcomes of awake surgery (AwS) versus surgery under general anesthesia (GA) in supratentorial right-sided gliomas. A systematic review of the literature according to PRISMA guidelines was performed up to March 2023. Four databases were screened. Primary outcome to assess was return to work (RTW). Secondary outcomes included the rate of postoperative neurological deficit, postoperative Karnofsky Performance Status (KPS) score and the extent of resection (EOR). A total of 32 articles were included with 543 patients who underwent right hemisphere tumor resection under awake surgery and 294 under general anesthesia. There were no significant differences between groups regarding age, gender, handedness, perioperative KPS, tumor location or preoperative seizures. Preoperative and long-term postoperative neurological deficits were statistically lower after AwS (p = 0.03 and p < 0.01, respectively), even though no difference was found regarding early postoperative course (p = 0.32). A subsequent analysis regarding type of postoperative impairment was performed. Severe postoperative language deficits were not different (p = 0.74), but there were fewer long-term mild motor and high-order cognitive deficits (p < 0.05) in AwS group. A higher rate of RTW (p < 0.05) was documented after AwS. The EOR was similar in both groups. Glioma resection of the right hemisphere under awake mapping is a safer procedure with a better preservation of high-order cognitive functions and a higher rate of RTW than resection under general anesthesia, despite similar EOR.

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References

  1. Duffau H (2017) Hodotopy, neuroplasticity and diffuse gliomas. Neurochirurgie 63(3):259–265. https://doi.org/10.1016/j.neuchi.2016.12.001

    Article  CAS  PubMed  Google Scholar 

  2. Thiebaut de Schotten M, Urbanski M, Duffau H et al (2005) Direct evidence for a parietal frontal pathway subserving spatial awareness in humans. Science (1979) 309(5744):2222–2226. https://doi.org/10.1126/science.1114362

    Article  CAS  Google Scholar 

  3. Zhao M, Marino M, Samogin J, Swinnen SP, Mantini D (2019) Hand, foot and lip representations in primary sensorimotor cortex: a high-density electroencephalography study. Sci Rep 9(1). https://doi.org/10.1038/s41598-019-55369-3

  4. Prat-Acín R, Galeano-Senabre I, López-Ruiz P, Ayuso-Sacido A, Espert-Tortajada R (2021) Intraoperative brain mapping of language, cognitive functions, and social cognition in awake surgery of low-grade gliomas located in the right non-dominant hemisphere. Clin Neurol Neurosurg 200:106363. https://doi.org/10.1016/j.clineuro.2020.106363

    Article  PubMed  Google Scholar 

  5. Ohyama M, Senda M, Kitamura S, Ishii K, Mishina M, Terashi A (1996) Role of the nondominant hemisphere and undamaged area during word repetition in poststroke aphasics. Stroke 27:897–903

    Article  CAS  PubMed  Google Scholar 

  6. Bu LH, Zhang J, Lu JF, Wu JS (2021) Glioma surgery with awake language mapping versus generalized anesthesia: a systematic review. Neurosurg Rev 44(4):1997–2011. https://doi.org/10.1007/s10143-020-01418-9

    Article  PubMed  Google Scholar 

  7. Ius T, Isola M, Budai R et al (2012) Low-grade glioma surgery in eloquent areas: Volumetric analysis of extent of resection and its impact on overall survival. A single-institution experience in 190 patients - Clinical article. J Neurosurg 117(6):1039–1052. https://doi.org/10.3171/2012.8.JNS12393

    Article  PubMed  Google Scholar 

  8. 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

    Article  PubMed  Google Scholar 

  9. Duffau H (2016) Long-term outcomes after supratotal resection of diffuse low-grade gliomas: a consecutive series with 11-year follow-up. Acta Neurochir (Wien) 158(1):51–58. https://doi.org/10.1007/s00701-015-2621-3

    Article  PubMed  Google Scholar 

  10. 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 

  11. Shinoura N, Midorikawa A, Yamada R et al (2013) Awake craniotomy for brain lesions within and near the primary motor area: a retrospective analysis of factors associated with worsened paresis in 102 consecutive patients. Surg Neurol Int 4(1):149. https://doi.org/10.4103/2152-7806.122003

    Article  PubMed  PubMed Central  Google Scholar 

  12. Hulou MM, Cote DJ, Olubiyi OI, Smith TR, Chiocca EA, Johnson MD (2015) Awake right hemisphere brain surgery. J Clin Neurosci 22(12):1921–1927. https://doi.org/10.1016/j.jocn.2015.06.009

    Article  PubMed  Google Scholar 

  13. Kleinman JT, Sepkuty JP, Hillis AE et al (2007) Spatial neglect during electrocortical stimulation mapping in the right hemisphere. Epilepsia 48(12):2365–2368. https://doi.org/10.1111/j.1528-1167.2007.01196.x

    Article  PubMed  Google Scholar 

  14. Stone JJ, Reynolds MR, Leuthardt EC (2011) Transient hemispatial neglect after surgical resection of a right frontal lobe mass. World Neurosurg 76(3–4):361.e7-361.e10. https://doi.org/10.1016/j.wneu.2010.03.018

    Article  PubMed  Google Scholar 

  15. 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. https://doi.org/10.3389/fnbeh.2018.00033

  16. Scarone P, Gatignol P, Guillaume S, Denvil D, Capelle L, Duffau H (2009) Agraphia after awake surgery for brain tumor: new insights into the anatomo-functional network of writing. Surg Neurol 72(3):223–241. https://doi.org/10.1016/j.surneu.2008.10.074

    Article  PubMed  Google Scholar 

  17. Sarubbo S, Latini F, Panajia A et al (2011) Awake surgery in low-grade gliomas harboring eloquent areas: 3-year mean follow-up. Neurol Sci 32(5):801–810. https://doi.org/10.1007/s10072-011-0587-3

    Article  CAS  PubMed  Google Scholar 

  18. Fischer DB, Perez DL, Prasad S et al (2016) Right inferior longitudinal fasciculus lesions disrupt visual-emotional integration. Soc Cogn Affect Neurosci 11(6):945–951. https://doi.org/10.1093/scan/nsw011

    Article  PubMed  PubMed Central  Google Scholar 

  19. Giussani C, Roux FE, Bello L et al (2009) Who is who: areas of the brain associated with recognizing and naming famous faces - Clinical article. J Neurosurg 110(2):289–299. https://doi.org/10.3171/2007.8.17566

    Article  PubMed  Google Scholar 

  20. Duffau H (2020) What direct electrostimulation of the brain taught us about the human connectome: a three-level model of neural disruption. Front Hum Neurosci 14. https://doi.org/10.3389/fnhum.2020.00315

  21. Yordanova YN, Cochereau J, Duffau H, Herbet G (2019) Combining resting state functional MRI with intraoperative cortical stimulation to map the mentalizing network. Neuroimage 186:628–636. https://doi.org/10.1016/j.neuroimage.2018.11.046

    Article  PubMed  Google Scholar 

  22. Nakada M, Nakajima R, Okita H et al (2021) Awake surgery for right frontal lobe glioma can preserve visuospatial cognition and spatial working memory. J Neurooncol 151(2):221–230. https://doi.org/10.1007/s11060-020-03656-9

    Article  PubMed  Google Scholar 

  23. Ouzzani M, Hammady H, Fedorowicz Z, Elmagarmid A (2016) Rayyan-a web and mobile app for systematic reviews. Syst Rev 5(1). https://doi.org/10.1186/s13643-016-0384-4

  24. Puglisi G, Howells H, Sciortino T (2019) Frontal pathways in cognitive control: direct evidence from intraoperative stimulation and diffusion tractography. Brain 142(8):2451–2465. https://doi.org/10.1093/brain/awz197

    Article  PubMed  PubMed Central  Google Scholar 

  25. 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(20):2559–2565. https://doi.org/10.1200/JCO.2011.38.4818

    Article  PubMed  Google Scholar 

  26. Catani M (2017) A little man of some importance. Brain 140(11):3055–3061. https://doi.org/10.1093/brain/awx270

    Article  PubMed  PubMed Central  Google Scholar 

  27. Mazoyer B, Zago L, Jobard G et al (2014) Gaussian mixture modeling of hemispheric lateralization for language in a large sample of healthy individuals balanced for handedness. PLoS One 9(6):e101165. https://doi.org/10.1371/journal.pone.0101165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Sacko Oumar, Lauwers-Cances Valérie, Brauge D, Sesay M, Brenner A, Roux FE (2011) Awake craniotomy vs surgery under general anesthesia for resection of supratentorial lesions73923. Neurosurgery 68(5):1198

    Article  Google Scholar 

  29. Baurès R, Fourteau M, Thébault S (2021) Time-to-contact perception in the brain. J Neurosci Res 99(2):455–466

    Article  PubMed  Google Scholar 

  30. Giussani C, Pirillo D, Roux FE (2010) Mirror of the soul: a cortical stimulation study on recognition of facial emotions: clinical article. J Neurosurg 112(3):520–527. https://doi.org/10.3171/2009.5.JNS081522

    Article  PubMed  Google Scholar 

  31. Duffau H (2022) Awake mapping with transopercular approach in right insular-centered low-grade gliomas improves neurological outcomes and return to work. Neurosurgery 91(1):182–190. https://doi.org/10.1227/neu.0000000000001966

    Article  PubMed  Google Scholar 

  32. Mandonnet E, Cerliani L, Siuda-Krzywicka K et al (2017) A network-level approach of cognitive flexibility impairment after surgery of a right temporo-parietal glioma. Neurochirurgie 63(4):308–313. https://doi.org/10.1016/j.neuchi.2017.03.003

    Article  CAS  PubMed  Google Scholar 

  33. Duffau H, Leroy M, Gatignol P (2008) Cortico-subcortical organization of language networks in the right hemisphere: an electrostimulation study in left-handers. Neuropsychologia 46(14):3197–3209. https://doi.org/10.1016/j.neuropsychologia.2008.07.017

    Article  PubMed  Google Scholar 

  34. Papagno C, Mattavelli G, Casarotti A, Bello L, Gainotti G (2018) Defective recognition and naming of famous people from voice in patients with unilateral temporal lobe tumours. Neuropsychologia 116:194–204. https://doi.org/10.1016/j.neuropsychologia.2017.07.021

    Article  CAS  PubMed  Google Scholar 

  35. Emanuele B, Santini B, Talacchi A, Gerosa M, Savazzi S (2012) Pre- and post-operative assessment of visuo-spatial functions in right hemisphere tumour patients: a pilot study. J Neurooncol 108(2):261–267. https://doi.org/10.1007/s11060-012-0820-9

    Article  PubMed  Google Scholar 

  36. Motomura K, Chalise L, Ohka F et al (2020) Neurocognitive and functional outcomes in patients with diffuse frontal lower-grade gliomas undergoing intraoperative awake brain mapping. J Neurosurg 132(6):1683–1691. https://doi.org/10.3171/2019.3.JNS19211

    Article  Google Scholar 

  37. Herbet G, Moritz-Gasser S (2019) Beyond language: mapping cognition and emotion. Neurosurg Clin N Am 30(1):75–83. https://doi.org/10.1016/j.nec.2018.08.004

    Article  PubMed  Google Scholar 

  38. 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):2159–2169. https://doi.org/10.1007/s00429-014-0777-x

    Article  PubMed  Google Scholar 

  39. Zhao K, Zhao J, Zhang M, Cui Q, Fu X (2017) Neural responses to rapid facial expressions of fear and surprise. Front Psychol 8(MAY). https://doi.org/10.3389/fpsyg.2017.00761

  40. Hartung SL, Mandonnet E, de Witt Hamer P et al (2021) Impaired set-shifting from dorsal stream disconnection: Insights from a european series of right parietal lower-grade glioma resection. Cancers (Basel) 13(13):3337. https://doi.org/10.3390/cancers13133337

    Article  PubMed  Google Scholar 

  41. Vallar G, Bello L, Bricolo E et al (2014) Cerebral correlates of visuospatial neglect: A direct cerebral stimulation study. Hum Brain Mapp 35(4):1334–1350. https://doi.org/10.1002/hbm.22257

    Article  PubMed  Google Scholar 

  42. Casanova M, Clavreul A, Soulard G et al (2021) Immersive virtual reality and ocular tracking for brain mapping during awake surgery: prospective evaluation study. J Med Internet Res 23(3):e24373. https://doi.org/10.2196/24373

    Article  PubMed  PubMed Central  Google Scholar 

  43. Bernard F, Lemée 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 

  44. Lemée JM, 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 

  45. Halligan PW, Marshall JC (1992) Left visuospatial neglect: a meaningless entity? Cortex 28(4):525–535

    Article  CAS  PubMed  Google Scholar 

  46. Patel S, Oishi K, Wright A et al (2018) Right hemisphere regions critical for expression of emotion through prosody. Front Neurol 9(APR). https://doi.org/10.3389/fneur.2018.00224

  47. Gainotti G (2019) The role of the right hemisphere in emotional and behavioral disorders of patients with frontotemporal lobar degeneration: an updated review. Front Aging Neurosci 11. https://doi.org/10.3389/fnagi.2019.00055

  48. Herbet G, Lafargue G, Bonnetblanc F, Moritz-Gasser S, Menjot De Champfleur N, Duffau H (2014) Inferring a dual-stream model of mentalizing from associative white matter fibres disconnection. Brain 137(3):944–959. https://doi.org/10.1093/brain/awt370

    Article  PubMed  Google Scholar 

  49. Tompkins CA, Scharp VL, Fassbinder W, Meigh KM, Armstrong EM (2008) A different story on “Theory of Mind” deficit in adults with right hemisphere brain damage. Aphasiology 22(1):42–61. https://doi.org/10.1080/02687030600830999

    Article  PubMed  PubMed Central  Google Scholar 

  50. Loayza FR, Obeso I, Redondo RG et al (2022) The motor inhibitory network in patients with asymmetrical Parkinson’s disease: An fMRI study. Brain Imaging Behav 16(3):1349–1361. https://doi.org/10.1007/s11682-021-00587-5

    Article  PubMed  PubMed Central  Google Scholar 

  51. Rech F, Duffau H, Pinelli C et al (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. https://doi.org/10.1016/j.neuchi.2016.08.006

    Article  CAS  PubMed  Google Scholar 

  52. Gandola M, Invernizzi P, Sedda A et al (2012) An anatomical account of somatoparaphrenia. Cortex 48(9):1165–1178. https://doi.org/10.1016/j.cortex.2011.06.012

    Article  PubMed  Google Scholar 

  53. Meador KJ, Allen ME, Adams RJ, Loring DW (n.d.) Allochiria vs allesthesia is there a misperception? http://archneur.jamanetwork.com/. Accessed 7 Nov 2023

  54. Russell C, Deidda C, Malhotra P, Crinion JT, Merola S, Husain M (2010) A deficit of spatial remapping in constructional apraxia after right-hemisphere stroke. Brain 133(4):1239–1251. https://doi.org/10.1093/brain/awq052

    Article  PubMed  Google Scholar 

  55. Barrett AM (2021) Spatial neglect and anosognosia after right brain stroke. CONTINUUM Lifelong Learn Neurol 27(6):1624–1645. https://doi.org/10.1212/CON.0000000000001076

    Article  CAS  Google Scholar 

  56. Herbet G, Duffau H (2020) Revisiting the functional anatomy of the human brain: Toward a meta-networking theory of cerebral functions. Physiol Rev 100(3):1181–1228. https://doi.org/10.1152/physrev.00033.2019

    Article  PubMed  Google Scholar 

  57. Kawauchi D, Ohno M, Honda-Kitahara M et al (2022) The clinical characteristics and outcomes of incidentally discovered glioblastoma. J Neurooncol 156(3):551–557. https://doi.org/10.1007/s11060-021-03931-3

    Article  PubMed  Google Scholar 

  58. Roux FE, Dufor O, Lauwers-Cances V et al (2011) Electrostimulation mapping of spatial neglect. Neurosurgery 69(6):1218–1231 (https://journals.lww.com/neurosurgery/fulltext/2011/12000/electrostimulation_mapping_of_spatial_neglect.16.aspx). Accessed 7 Nov 2023

  59. Herbet G, Yordanova YN, Duffau H (2017) Left spatial neglect evoked by electrostimulation of the right inferior fronto-occipital fasciculus. Brain Topogr 30(6):747–756. https://doi.org/10.1007/s10548-017-0574-y

    Article  PubMed  Google Scholar 

  60. Rech F, Herbet G, Gaudeau Y et al (2019) A probabilistic map of negative motor areas of the upper limb and face: a brain stimulation study. Brain 142(4):952–965. https://doi.org/10.1093/brain/awz021

    Article  PubMed  PubMed Central  Google Scholar 

  61. Mashour GA, Woodrum DT, Avidan MS (2015) Neurological complications of surgery and anaesthesia. Br J Anaesth 114(2):194–203. https://doi.org/10.1093/bja/aeu296

    Article  CAS  PubMed  Google Scholar 

  62. Moiyadi A, Shetty P (2012) Perioperative outcomes following surgery for brain tumors: Objective assessment and risk factor evaluation. J Neurosci Rural Pract 3(1):28–35. https://doi.org/10.4103/0976-3147.91927

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

I would like to express my gratitude to Professor James W. Dalling, PhD and Carlos F. Duran M.D., for reviewing the grammar and statistical analysis.

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Authors and Affiliations

  1. School of Medicine, Universidad del Rosario, Bogotá, Colombia

    Esteban Ramírez-Ferrer

  2. Department of Neurosurgery, Hospital Universitario La Samaritana, Bogotá, Colombia

    Esteban Ramírez-Ferrer

  3. Department of Neurosurgery, Hospital Universitario Mayor de Méderi, Bogotá, Colombia

    Esteban Ramírez-Ferrer

  4. Center of Research and Training in Neurosurgery (CIEN), Bogotá, Colombia

    Esteban Ramírez-Ferrer & Maria Paula Aguilera-Pena

  5. Cedars Sinai Medical Center, Los Angeles, CA, USA

    Maria Paula Aguilera-Pena

  6. Department of Neurosurgery, Gui De Chauliac Hospital, Montpellier University Medical Center, Montpellier, France

    Hugues Duffau

  7. U1191 Laboratory, Team “Brain Plasticity, Stem Cells and Glial Tumors”, Institute of Functional Genomics of Montpellier, National Institute for Health and Medical Research (INSERM), University of Montpellier, Montpellier, France

    Hugues Duffau

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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by E.R.F and M.P.A. The first draft of the manuscript was written by E.R.F and H.D. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Ramírez-Ferrer, E., Aguilera-Pena, M.P. & Duffau, H. Functional and oncological outcomes after right hemisphere glioma resection in awake versus asleep patients: a systematic review and meta-analysis. Neurosurg Rev 47, 160 (2024). https://doi.org/10.1007/s10143-024-02370-8

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