Abstract
Purpose
Neuroplasticity is an ability to maintain neural circuit function when facing damages. It is one of the reasons that making brain tumors notorious. Therefore, we evaluated the characteristics of patients with primary brain tumors, compared neuropsychological deficits between patients who had awake craniotomy with left- or right-sided tumors, and analyzed the association between white matter tracts and neuropsychological deficits in patients with right-sided tumors.
Methods
Using the registration dataset of Chang Gung Memory Hospital between 2014 and 2020, this study included a total of 698 adult patients who received craniotomy for primary brain tumors (538 of conventional craniotomy; 160 of awake craniotomy). Neuropsychological assessments were arranged in patients as preoperative evaluation for awake craniotomies.
Results
A lower proportion of right-sided tumors was noted in patient who had awake craniotomy than those who had conventional craniotomy (33.8% and 51.5%, p < 0.001). In awake craniotomy, 88.7% of patients with left-sided tumors and 77.8% of patients with right-sided tumors had neuropsychological impairment. Patients with left-sided tumors had worse preoperative performance compared to those with right-sided tumors in global function (36.2% and 8.0%, p < 0.001), language domain (57.6% and 22.2%, p < 0.001), and attention (36.0% and 18.5%, p = 0.02). Furthermore, in those with right-sided low-grade gliomas, patients involving pathway of superior longitudinal fasciculus (SLF) I had a higher risk of deficits than those without involvement in verbal memory (p = 0.001, Odd ratio = 11.2, 95% CI = 1.8 ~ 71.4) and visual memory (p = 0.048, Odd ratio = 10.5, 95% CI = 1.0 ~ 111).
Conclusion
In awake craniotomy, patients with left-sided brain tumors had worse cognitive function than those with right-sided tumors in terms of global function, language, and attention. 77% of patients with right-sided tumors had neuropsychological impairment. Therefore, a comprehensive neuropsychological evaluation and awake craniotomy are necessary for patients with brain tumors.
Similar content being viewed by others
References
Lv K, Cao X, Wang R, Du P, Fu J, Geng D, Zhang J (2022) Neuroplasticity of Glioma Patients: Brain structure and Topological Network. Front Neurol 13. https://doi.org/10.3389/fneur.2022.871613
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
Belien AT, Paganetti PA, Schwab ME (1999) Membrane-type 1 matrix metalloprotease (MT1-MMP) enables invasive migration of glioma cells in central nervous system white matter. J Cell Biol 144:373–384. https://doi.org/10.1083/jcb.144.2.373
DeAngelis LM (2001) Brain tumors. N Engl J Med 344:114–123. https://doi.org/10.1056/NEJM200101113440207
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
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
Ostrom QT, Patil N, Cioffi G, Waite K, Kruchko C, Barnholtz-Sloan JS (2020) CBTRUS Statistical Report: primary brain and other Central Nervous System Tumors diagnosed in the United States in 2013–2017. Neuro Oncol 22:iv1–iv96. https://doi.org/10.1093/neuonc/noaa200
Obara T, Blonski M, Brzenczek C, Mezieres S, Gaudeau Y, Pouget C, Gauchotte G, Verger A, Vogin G, Moureaux JM, Duffau H, Rech F, Taillandier L (2020) Adult diffuse Low-Grade Gliomas: 35-Year experience at the Nancy France Neurooncology Unit. Front Oncol 10:574679. https://doi.org/10.3389/fonc.2020.574679
Dwan TM, Ownsworth T, Chambers S, Walker DG, Shum DH (2015) Neuropsychological assessment of individuals with brain tumor: comparison of approaches used in the classification of impairment. Front Oncol 5:56. https://doi.org/10.3389/fonc.2015.00056
Finger S (2010) Chap. 10: the birth of localization theory. Handb Clin Neurol 95:117–128. https://doi.org/10.1016/S0072-9752(08)02110-6
Folstein MF, Folstein SE, McHugh PR (1975) Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198. https://doi.org/10.1016/0022-3956(75)90026-6
Lin K-N, Wang P-N, Liu H-C, Teng EL (2012) Cognitive abilities screening instrument, chinese version 2.0 (CASI C-2.0): administration and clinical application. Acta Neurol Taiwan 21:180–189
Lezak MD, Howieson DB, Loring DW, Fischer JS (2004) Neuropsychological assessment. Oxford University Press, USA
Hua MS, Chang SH, Chen ST (1997) Factor structure and age effects with an aphasia test battery in normal taiwanese adults. Neuropsychology 11:156–162. https://doi.org/10.1037//0894-4105.11.1.156
Chang HT, Chen TF, Cheng TW, Lai YM, Hua MS (2018) Arbitrary and semantic associations in subjective memory impairment and amnestic mild cognitive impairment among taiwanese individuals: a cross-sectional study. J Formos Med Assoc 117:427–433. https://doi.org/10.1016/j.jfma.2017.05.014
Kd H, Roberts R (1983) Word sequence learning test. Department of Neurology, University of Wisconsin Medical School, Milwaukee
Benton AL (1963) The revised visual retention test: clinical and experimental applications. Psychological Corporation
Benton AL (1994) Contributions to neuropsychological assessment: a clinical manual. Oxford University Press, USA
Grant DA, Berg EA (1993) Wisconsin Card sorting test (WCST). PAR.
Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J (1961) An inventory for measuring depression. Arch Gen Psychiatry 4:561–571. https://doi.org/10.1001/archpsyc.1961.01710120031004
Beck AT, Epstein N, Brown G, Steer RA (1988) An inventory for measuring clinical anxiety: psychometric properties. J Consult Clin Psychol 56:893–897. https://doi.org/10.1037//0022-006x.56.6.893
Macdonald DR, Cascino TL, Schold SC Jr, Cairncross JG (1990) Response criteria for phase II studies of supratentorial malignant glioma. J Clin Oncol 8:1277–1280. https://doi.org/10.1200/JCO.1990.8.7.1277
Chang WH, Wei KC, Chen PY, Chen YC, Wu YY, Tsai HC, Chen MH, Chao YP, Chen KT (2023) The impact of patient factors and tumor characteristics on language neuroplasticity in left hemispheric diffuse gliomas prior to surgical resection. J Neurooncol 163:95–104. https://doi.org/10.1007/s11060-023-04311-9
van Kessel E, Baumfalk AE, van Zandvoort MJE, Robe PA, Snijders TJ (2017) Tumor-related neurocognitive dysfunction in patients with diffuse glioma: a systematic review of neurocognitive functioning prior to anti-tumor treatment. J Neurooncol 134:9–18. https://doi.org/10.1007/s11060-017-2503-z
Tan AC, Ashley DM, Lopez GY, Malinzak M, Friedman HS, Khasraw M (2020) Management of glioblastoma: state of the art and future directions. CA Cancer J Clin 70:299–312. https://doi.org/10.3322/caac.21613
Taphoorn MJ, Klein M (2004) Cognitive deficits in adult patients with brain tumours. Lancet Neurol 3:159–168. https://doi.org/10.1016/S1474-4422(04)00680-5
Noll KR, Weinberg JS, Ziu M, Benveniste RJ, Suki D, Wefel JS (2015) Neurocognitive changes Associated with Surgical Resection of Left and right temporal lobe glioma. Neurosurgery 77:777–785. https://doi.org/10.1227/NEU.0000000000000987
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
Kamali A, Flanders AE, Brody J, Hunter JV, Hasan KM (2014) Tracing superior longitudinal fasciculus connectivity in the human brain using high resolution diffusion tensor tractography. Brain Struct Funct 219:269–281. https://doi.org/10.1007/s00429-012-0498-y
Janelle F, Iorio-Morin C, D’Amour S, Fortin D (2022) Superior Longitudinal Fasciculus: a review of the anatomical descriptions with functional correlates. Front Neurol 13:794618. https://doi.org/10.3389/fneur.2022.794618
Herbet G, Maheu M, Costi E, Lafargue G, Duffau H (2016) Mapping neuroplastic potential in brain-damaged patients. Brain 139:829–844. https://doi.org/10.1093/brain/awv394
Acknowledgements
This study is based in part on data from the Chang Gung Research Database provided by Chang Gung Memorial Hospital. The interpretation and conclusions contained herein do not represent the position of Chang Gung Memorial Hospital.
Funding
This study was supported by the Chang Gung Medical Foundation, Taiwan (grant numbers CMRPG3L1341), as well as by the Ministry of Science and Technology, Executive Yuan, Taiwan (grant numbers 109-2629-B-182 A-001, 110-2314-B-182 A-070, 111-2314-B-182 A-134-MY2). All authors report no conflicts of interest.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation and data collection were performed by Y-CC, C-CY, W-CC, K-CW, and W-HC. Analysis was performed by Y-YW, Y-CC, K-TC, and Y-PC. The first draft of the manuscript was written by Y-YW and Y-CC, and all authors commented on previous versions of the manuscript. All authors reviewed and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
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.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Wu, YY., Chen, KT., Chu, YC. et al. Neuropsychological impairment in primary malignant brain tumor patients with awake craniotomy: a hospital-based registration study. J Neurooncol 164, 483–491 (2023). https://doi.org/10.1007/s11060-023-04431-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11060-023-04431-2