Role of Preoperative Assessment in Predicting Tumor-Induced Plasticity in Patients with Diffuse Gliomas

Abstract

When diffuse gliomas (DG) affect the brain’s potential to reorganize functional networks, patients can exhibit seizures and/or language/cognitive impairment. The tumor–brain interaction and the individual connectomic organization cannot be predicted preoperatively. We aimed to, first, investigate the relationship between preoperative assessment and intraoperative findings of eloquent tumors in 36 DG operated with awake surgery. Second, we also studied possible mechanisms of tumor-induced brain reorganization in these patients. FLAIR-MRI sequences were used for tumor volume segmentation and the Brain-Grid system (BG) was used as an overlay for infiltration analysis. Neuropsychological (NPS) and/or language assessments were performed in all patients. The distance between eloquent spots and tumor margins was measured. All variables were used for correlation and logistic regression analyses. Eloquent tumors were detected in 75% of the patients with no single variable able to predict this finding. Impaired NPS functions correlated with invasive tumors, crucial location (A4C2S2/A3C2S2-voxels, left opercular-insular/sub-insular region) and higher risk of eloquent tumors. Epilepsy was correlated with larger tumor volumes and infiltrated A4C2S2/A3C2S2 voxels. Language impairment was correlated with infiltrated A3C2S2 voxel. Peritumoral cortical eloquent spots reflected an early compensative mechanism with age as possible influencing factor. Preoperative NPS impairment is linked with high risk of eloquent tumors. A systematic integration of extensive cognitive assessment and advanced neuroimaging can improve our comprehension of the connectomic brain organization at the individual scale and lead to a better oncological/functional balance.

Influences on cognitive outcomes in adult patients with gliomas: A systematic review

“…On balance, the evidence is overall more against a role of tumor volume on cognition, with most studies concluding this being prospective in design and including a randomized trial (n=187); two of the three studies supporting a tumor volume were retrospective in design ( 54 , 60 ), although one of these had a large study population (n=780) ( 54 ). Invasiveness of a tumor determined using MRI has also been shown to be associated with neurocognitive functioning ( 34 ).…”

Dynamics in cognition and health-related quality of life in grade 2 and 3 gliomas after surgery

“…As described in previous studies by our group [ 13 , 39 ], the intent of the tumor surgery was maximal and safe resection. The surgical procedure included craniotomy and microsurgical technique, guided by neuronavigation and intraoperative ultrasound.…”

“…For tumors located in or near motor cortex/pathways, intraoperative neurophysiological monitoring of motor function was performed. For tumors close to eloquent areas related to language function or other cognitive domains, awake surgery was done to monitor those functions, as previously described [ 13 ]. Further follow-up and eventual adjunct oncological treatments (radio- and/or chemotherapy) were discussed and decided on at multidisciplinary conferences after the histomolecular diagnosis had been determined, in accordance with the European Association of Neuro-Oncology (EANO) guidelines [ 43 ].…”

“…T2 turbo spin echo or T2-FLAIR images in Vue picture archiving and communication system (PACS) software (version 11.1.0, Carestream Health Inc., Rochester, NY) were used to segment the lesions both pre- and postoperatively with the aid of a semiautomatic method (Livewire Algorithm) [ 14 ]. Tumor location and eloquence was analyzed by means of diffusion tensor imaging (DTI) reconstructions, as described in detail in a previous study by our group [ 13 ]. The tumors were considered eloquent if they exhibited infiltration of the white matter pathways in the inferior fronto-occipital fascicle (IFOF), arcuate fasciculus (AF), corticospinal tract (CST), and optic radiation (OR), i.e., the “minimal common brain” [ 35 ].…”

Editorial: Investigating the gliomas/white matter interplay and its implications for multidisciplinary treatment: State of art and future perspectives

“…Gliomas are heterogeneous and challenging tumors, they tend to preferentially infiltrate “secondary” functional areas (immediately near the so-called primary eloquent regions), or the so-called “minimal common brain” (Duffau and Capelle, 2004 ; Ius et al, 2011 ; Latini et al, 2020 ). It is clear that the tumor tends to interfere with normal brain function by disrupting the functional connectivity of brain networks within peritumoral and distant brain areas, thereby inducing neuropsychological impairment or seizure activity (Szalisznyo et al, 2013 ; Smits et al, 2015 ; Smits and Jakola, 2019 ; Aabedi et al, 2021 ; Latini et al, 2021a ). The mechanisms of cortical-subcortical plasticity at the individual level are not fully understood with important anatomical-functional variability (Herbet et al, 2016 ; Sarubbo et al, 2020 ).…”