Neurocognition in adults with intracranial tumors: does location really matter?


Journal

Journal of neuro-oncology
ISSN: 1573-7373
Titre abrégé: J Neurooncol
Pays: United States
ID NLM: 8309335

Informations de publication

Date de publication:
Dec 2022
Historique:
received: 22 09 2022
accepted: 22 10 2022
pubmed: 9 11 2022
medline: 21 12 2022
entrez: 8 11 2022
Statut: ppublish

Résumé

As preservation of cognitive functioning increasingly becomes important in the light of ameliorated survival after intracranial tumor treatments, identification of eloquent brain areas would enable optimization of these treatments. This cohort study enrolled adult intracranial tumor patients who received neuropsychological assessments pre-irradiation, estimating processing speed, verbal fluency and memory. Anatomical magnetic resonance imaging scans were used for multivariate voxel-wise lesion-symptom predictions of the test scores (corrected for age, gender, educational level, histological subtype, surgery, and tumor volume). Potential effects of histological and molecular subtype and corresponding WHO grades on the risk of cognitive impairment were investigated using Chi square tests. P-values were adjusted for multiple comparisons (p < .001 and p < .05 for voxel- and cluster-level, resp.). A cohort of 179 intracranial tumor patients was included [aged 19-85 years, median age (SD) = 58.46 (14.62), 50% females]. In this cohort, test-specific impairment was detected in 20-30% of patients. Higher WHO grade was associated with lower processing speed, cognitive flexibility and delayed memory in gliomas, while no acute surgery-effects were found. No grading, nor surgery effects were found in meningiomas. The voxel-wise analyses showed that tumor locations in left temporal areas and right temporo-parietal areas were related to verbal memory and processing speed, respectively. Patients with intracranial tumors affecting the left temporal areas and right temporo-parietal areas might specifically be vulnerable for lower verbal memory and processing speed. These specific patients at-risk might benefit from early-stage interventions. Furthermore, based on future validation studies, imaging-informed surgical and radiotherapy planning could further be improved.

Identifiants

pubmed: 36346497
doi: 10.1007/s11060-022-04181-7
pii: 10.1007/s11060-022-04181-7
pmc: PMC9758085
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

619-629

Informations de copyright

© 2022. The Author(s).

Références

Ghiaseddin A, Minh LBH, Janiszewska M et al (2021) Adult precision medicine: learning from the past to enhance the future. Neurooncol Adv. https://doi.org/10.1093/noajnl/vdaa145
doi: 10.1093/noajnl/vdaa145
Simonelli M, Persico P, Perrino M et al (2018) Checkpoint inhibitors as treatment for malignant gliomas: “a long way to the top.” Cancer Treat Rev. https://doi.org/10.1016/j.ctrv.2018.06.016
doi: 10.1016/j.ctrv.2018.06.016
Frances SM, Velikova G, Klein M et al (2022) Long-term impact of adult WHO grade II or III gliomas on health-related quality of life: a systematic review. Neurooncol Pract. https://doi.org/10.1093/nop/npab062
doi: 10.1093/nop/npab062
Jacob J, Durand T, Feuvret L et al (2018) Cognitive impairment and morphological changes after radiation therapy in brain tumors: a review. Radiother Oncol. https://doi.org/10.1016/j.radonc.2018.05.027
doi: 10.1016/j.radonc.2018.05.027
Keng A, Stewart DE, Sheehan KA (2020) Examining the neuropsychiatric sequelae postsurgical resection of adult brain tumors through a scoping review. Psychosomatics. https://doi.org/10.1016/j.psym.2019.12.008
doi: 10.1016/j.psym.2019.12.008
Duffau H (2021) New philosophy, clinical pearls, and methods for intraoperative cognition mapping and monitoring “à la carte” in brain tumor patients. Neurosurgery. https://doi.org/10.1093/neuros/nyaa363
doi: 10.1093/neuros/nyaa363
Nicol C, Ownsworth T, Cubis L et al (2019) Subjective cognitive functioning and associations with psychological distress in adult brain tumour survivors. J Cancer Surviv. https://doi.org/10.1007/s11764-019-00784-8
doi: 10.1007/s11764-019-00784-8
Campanella F, Arcara G, Crescentini C et al (2021) Cognitive reserve protects language functions in patients with brain tumours. Neuropsychologia. https://doi.org/10.1016/j.neuropsychologia.2021.107769
doi: 10.1016/j.neuropsychologia.2021.107769
Correa DD, Satagopan J, Martin A et al (2019) Genetic variants and cognitive functions in patients with brain tumors. Neuro Oncol. https://doi.org/10.1093/neuonc/noz094
doi: 10.1093/neuonc/noz094
Bunevicius A, Miller J, Parsons M (2020) Isocitrate dehydrogenase, patient-reported outcomes, and cognitive functioning of glioma patients: a systematic review. Curr Oncol Rep. https://doi.org/10.1007/s11912-020-00978-9
doi: 10.1007/s11912-020-00978-9
Schagen SB, Tsvetkov AS, Compter A, Wefel JS (2022) Cognitive adverse effects of chemotherapy and immunotherapy: are interventions within reach? Nat Rev Neurol. https://doi.org/10.1038/s41582-021-00617-2
doi: 10.1038/s41582-021-00617-2
Parker AF, Ohlhauser L, Scarapicchia V et al (2022) A systematic review of neuroimaging studies comparing individuals with subjective cognitive decline to healthy controls. J Alzheimer’s Dis. https://doi.org/10.3233/jad-215249
doi: 10.3233/jad-215249
Dartora CM, Borelli WV, Koole M, Marques da Silva AM (2021) Cognitive decline assessment: a review from medical imaging perspective. Front Aging Neurosci. https://doi.org/10.3389/fnagi.2021.704661
doi: 10.3389/fnagi.2021.704661
Voon NS, Manan HA, Yahya N (2021) Cognitive decline following radiotherapy of head and neck cancer: systematic review and meta-analysis of MRI correlates. Cancers (Basel). https://doi.org/10.3390/cancers13246191
doi: 10.3390/cancers13246191
Tohidinezhad F, di Perri D, Zegers CML et al (2022) Prediction models for radiation-induced neurocognitive decline in adult patients with primary or secondary brain tumors: a systematic review. Front Psychol. https://doi.org/10.3389/fpsyg.2022.853472
doi: 10.3389/fpsyg.2022.853472
Karnath HO, Sperber C, Rorden C (2018) Mapping human brain lesions and their functional consequences. Neuroimage. https://doi.org/10.1016/j.neuroimage.2017.10.028
doi: 10.1016/j.neuroimage.2017.10.028
Broca P (1861) Remarques sur le siège de la faculté du langage articulé suivies d’une observation d’aphemie. Bull Soc Anthropol. https://doi.org/10.3406/bmsap.1865.9495
doi: 10.3406/bmsap.1865.9495
Duffau H (2018) The error of Broca: From the traditional localizationist concept to a connectomal anatomy of human brain. J Chem Neuroanat. https://doi.org/10.1016/j.jchemneu.2017.04.003
doi: 10.1016/j.jchemneu.2017.04.003
Sperber C, Karnath HO (2018) On the validity of lesion-behaviour mapping methods. Neuropsychologia. https://doi.org/10.1016/j.neuropsychologia.2017.07.035
doi: 10.1016/j.neuropsychologia.2017.07.035
Mirman D, Landrigan JF, Kokolis S et al (2018) Corrections for multiple comparisons in voxel-based lesion-symptom mapping. Neuropsychologia. https://doi.org/10.1016/j.neuropsychologia.2017.08.025
doi: 10.1016/j.neuropsychologia.2017.08.025
Habets EJJ, Hendriks EJ, Taphoorn MJB et al (2019) Association between tumor location and neurocognitive functioning using tumor localization maps. J Neurooncol. https://doi.org/10.1007/s11060-019-03259-z
doi: 10.1007/s11060-019-03259-z
Hendriks EJ, Habets EJJ, Taphoorn MJB et al (2018) Linking late cognitive outcome with glioma surgery location using resection cavity maps. Hum Brain Mapp. https://doi.org/10.1002/hbm.23986
doi: 10.1002/hbm.23986
Banerjee P, Leu K, Harris RJ et al (2015) Association between lesion location and language function in adult glioma using voxel-based lesion-symptom mapping. Neuroimage Clin. https://doi.org/10.1016/j.nicl.2015.10.010
doi: 10.1016/j.nicl.2015.10.010
Pisoni A, Mattavelli G, Casarotti A et al (2019) The neural correlates of auditory-verbal short-term memory: a voxel-based lesion-symptom mapping study on 103 patients after glioma removal. Brain Struct Funct. https://doi.org/10.1007/s00429-019-01902-z
doi: 10.1007/s00429-019-01902-z
Guarracino I, Ius T, Baiano C et al (2021) Pre-surgery cognitive performance and voxel-based lesion-symptom mapping in patients with left high-grade glioma. Cancers (Basel). https://doi.org/10.3390/cancers13061467
doi: 10.3390/cancers13061467
Faulkner JW, Wilshire CE (2020) Mapping eloquent cortex: a voxel-based lesion-symptom mapping study of core speech production capacities in brain tumour patients. Brain Lang. https://doi.org/10.1016/j.bandl.2019.104710
doi: 10.1016/j.bandl.2019.104710
Niki C, Kumada T, Maruyama T et al (2020) Primary cognitive factors impaired after glioma surgery and associated brain regions. Behav Neurol. https://doi.org/10.1155/2020/7941689
doi: 10.1155/2020/7941689
Pisoni A, Mattavelli G, Casarotti A et al (2018) Object-action dissociation: a voxel-based lesion-symptom mapping study on 102 patients after glioma removal. Neuroimage Clin. https://doi.org/10.1016/j.nicl.2018.03.022
doi: 10.1016/j.nicl.2018.03.022
de Roeck L, van der Weide HL, Eekers DBP et al (2022) The European Particle Therapy Network (EPTN) consensus on the follow-up of adult patients with brain and skull base tumours treated with photon or proton irradiation. Radiother Oncol. https://doi.org/10.1016/j.radonc.2022.01.018
doi: 10.1016/j.radonc.2022.01.018
Ruff RM, Light RH, Parker SB, Levin HS (1996) Benton controlled oral word association test: reliability and updated norms. Arch Clin Neuropsychol. https://doi.org/10.1016/0887-6177(95)00033-X
doi: 10.1016/0887-6177(95)00033-X
Benedict RHB, Schretlen D, Groninger L, Brandt J (1998) Hopkins verbal learning test–revised: normative data and analysis of inter-form and test-retest reliability. Clin Neuropsychol. https://doi.org/10.1076/clin.12.1.43.1726
doi: 10.1076/clin.12.1.43.1726
Siciliano M, Chiorri C, Battini V et al (2019) Regression-based normative data and equivalent scores for Trail Making Test (TMT): an updated Italian normative study. Neurol Sci. https://doi.org/10.1007/s10072-018-3673-y
doi: 10.1007/s10072-018-3673-y
Verhage F (1964) Intelligentie en leeftijd: onderzoek bij Nederlanders van twaalf tot zevenzeventig jaar [Intelligence and Age: study with Dutch people aged 12 to 77]. Assen: Van Gorcum
EekersIn‘t Ven DBL, Roelofs E et al (2018) The EPTN consensus-based atlas for CT- and MR-based contouring in neuro-oncology. Radiother Oncol. https://doi.org/10.1016/j.radonc.2017.12.013
doi: 10.1016/j.radonc.2017.12.013
Weller M, van den Bent M, Tonn JC et al (2017) European Association for Neuro-Oncology (EANO) guideline on the diagnosis and treatment of adult astrocytic and oligodendroglial gliomas. Lancet Oncol. https://doi.org/10.1016/S1470-2045(17)30194-8
doi: 10.1016/S1470-2045(17)30194-8
Avants BB, Tustison N, Song G (2011) Advanced normalization tools. Insight J 2:1–35
Wefel JS, Vardy J, Ahles T, Schagen SB (2011) International Cognition and Cancer Task Force recommendations to harmonise studies of cognitive function in patients with cancer. Lancet Oncol 12:703–708. https://doi.org/10.1016/S1470-2045(10)70294-1
doi: 10.1016/S1470-2045(10)70294-1
DeMarco AT, Turkeltaub PE (2018) A multivariate lesion symptom mapping toolbox and examination of lesion-volume biases and correction methods in lesion-symptom mapping. Hum Brain Mapp. https://doi.org/10.1002/hbm.24289
doi: 10.1002/hbm.24289
Johnson SC, Saykin AJ, Flashman LA et al (2001) Brain activation on fMRI and verbal memory ability: functional neuroanatomic correlates of CVLT performance. J Int Neuropsychol Soc. https://doi.org/10.1017/S135561770171106X
doi: 10.1017/S135561770171106X
Moll J, de Oliveira-Souza R, Moll FT et al (2002) The cerebral correlates of set-shifting: An fMRI study of the trail making test. Arq Neuropsiquiatr. https://doi.org/10.1590/S0004-282X2002000600002
doi: 10.1590/S0004-282X2002000600002
Varjacic A, Mantini D, Demeyere N, Gillebert CR (2018) Neural signatures of trail making test performance: evidence from lesion-mapping and neuroimaging studies. Neuropsychologia. https://doi.org/10.1016/j.neuropsychologia.2018.03.031
doi: 10.1016/j.neuropsychologia.2018.03.031
Noll KR, Sullaway C, Ziu M et al (2015) Relationships between tumor grade and neurocognitive functioning in patients with glioma of the left temporal lobe prior to surgical resection. Neuro Oncol 17:580–587. https://doi.org/10.1093/neuonc/nou233
doi: 10.1093/neuonc/nou233
van Kessel E, Emons MAC, Wajer IH et al (2019) Tumor-related neurocognitive dysfunction in patients with diffuse glioma: a retrospective cohort study prior to antitumor treatment. Neurooncol Pract. https://doi.org/10.1093/nop/npz008
doi: 10.1093/nop/npz008
Zhang G, Zhang X, Huang H et al (2022) Probing individual-level structural atrophy in frontal glioma patients. Neurosurg Rev. https://doi.org/10.1007/s10143-022-01800-9
doi: 10.1007/s10143-022-01800-9
van Kessel E, Berendsen S, Baumfalk AE et al (2022) Tumor-related molecular determinants of neurocognitive deficits in patients with diffuse glioma. Neuro Oncol. https://doi.org/10.1093/neuonc/noac036
doi: 10.1093/neuonc/noac036
Wefel JS, Zhou R, Sulman EP et al (2022) Genetic modulation of longitudinal change in neurocognitive function among adult glioma patients. J Neurooncol. https://doi.org/10.1007/s11060-021-03905-5
doi: 10.1007/s11060-021-03905-5
Kirkman MA, Hunn BHM, Thomas MSC, Tolmie AK (2022) Influences on cognitive outcomes in adult patients with gliomas: a systematic review. Front Oncol. https://doi.org/10.3389/fonc.2022.943600
doi: 10.3389/fonc.2022.943600
Douw L, van Dellen E, de Groot M et al (2010) Epilepsy is related to theta band brain connectivity and network topology in brain tumor patients. BMC Neurosci. https://doi.org/10.1186/1471-2202-11-103
doi: 10.1186/1471-2202-11-103
Coomans MB, van der Linden SD, Gehring K, Taphoorn MJB (2019) Treatment of cognitive deficits in brain tumour patients: current status and future directions. Curr Opin Oncol. https://doi.org/10.1097/cco.0000000000000581
doi: 10.1097/cco.0000000000000581
Einstein EH, Dadario NB, Khilji H et al (2022) Transcranial magnetic stimulation for post-operative neurorehabilitation in neuro-oncology: a review of the literature and future directions. J Neurooncol. https://doi.org/10.1007/s11060-022-03987-9
doi: 10.1007/s11060-022-03987-9
Miladi N, Dossa R, Dogba MJ et al (2019) Psychostimulants for cancer-related cognitive impairment in adult cancer survivors: a systematic review and meta-analysis. Suppor Care Cancer. https://doi.org/10.1007/s00520-019-04907-w
doi: 10.1007/s00520-019-04907-w
Gerstenecker A, Gammon M, Marotta D et al (2020) Using cognition to predict the ability to understand medical treatment in brain and metastatic cancer. Psychooncology. https://doi.org/10.1002/pon.5277
doi: 10.1002/pon.5277
Meyers CA, Hess KR, Yung WK, Levin VA (2000) Cognitive function as a predictor of survival in patients with recurrent malignant glioma. J Clin Oncol 18:646–650. https://doi.org/10.1200/JCO.2000.18.3.646
doi: 10.1200/JCO.2000.18.3.646
de Baene W, Rijnen SJM, Gehring K et al (2019) Lesion symptom mapping at the regional level in patients with a meningioma. Neuropsychology. https://doi.org/10.1037/neu0000490
doi: 10.1037/neu0000490

Auteurs

Charlotte Sleurs (C)

Department of Cognitive Neuropsychology, Tilburg University, Tilburg, The Netherlands. c.sleurs@tilburguniversity.edu.
Department of Oncology, KU Leuven, Leuven, Belgium. c.sleurs@tilburguniversity.edu.

Catharina M L Zegers (CML)

Department of Radiation Oncology (Maastro), GROW School for Oncology and Reproduction, Maastricht University Medical Center+, Maastricht, The Netherlands.

Inge Compter (I)

Department of Radiation Oncology (Maastro), GROW School for Oncology and Reproduction, Maastricht University Medical Center+, Maastricht, The Netherlands.

Jeanette Dijkstra (J)

Department of Medical Psychology, Maastricht University Medical Center+, MHeNs School for Mental Health and Neuroscience, Maastricht, The Netherlands.

Monique H M E Anten (MHME)

Department of Neurology, Maastricht University Medical Center+, Maastricht, The Netherlands.

Alida A Postma (AA)

Department of Radiology & Nuclear Medicine, Maastricht University Medical Center+, MHeNs School for Mental Health and Neuroscience, Maastricht, The Netherlands.

Olaf E M G Schijns (OEMG)

Department of Neurosurgery, Maastricht University Medical Center+, MHeNs School for Mental Health and Neuroscience, Maastricht, The Netherlands.

Ann Hoeben (A)

Division of Medical Oncology, Department of Internal Medicine, GROW-School of Oncology and Developmental Biology, Maastricht University Medical Center, Maastricht, the Netherlands.

Margriet M Sitskoorn (MM)

Department of Cognitive Neuropsychology, Tilburg University, Tilburg, The Netherlands.

Wouter De Baene (W)

Department of Cognitive Neuropsychology, Tilburg University, Tilburg, The Netherlands.

Laurien De Roeck (L)

Department of Oncology, KU Leuven, Leuven, Belgium.

Stefan Sunaert (S)

Department of Imaging and Pathology, KU Leuven, Leuven, Belgium.

Wouter Van Elmpt (W)

Department of Radiation Oncology (Maastro), GROW School for Oncology and Reproduction, Maastricht University Medical Center+, Maastricht, The Netherlands.

Maarten Lambrecht (M)

Department of Oncology, KU Leuven, Leuven, Belgium.

Daniëlle B P Eekers (DBP)

Department of Radiation Oncology (Maastro), GROW School for Oncology and Reproduction, Maastricht University Medical Center+, Maastricht, The Netherlands.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH