Brain connectomics applied to oncological neuroscience: from a traditional surgical strategy focusing on glioma topography to a meta-network approach

Duffau, Hugues

doi:10.1007/s00701-021-04752-z

Cited by 45 publications

(36 citation statements)

References 118 publications

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“…These findings confirming the low plastic capacity of the WM fibers play a critical role in the surgical strategy, not only regarding the principle of connectome-based resection relying on the mapping of cortico-subcortical networks critical for brain functions (with special emphasis on the preservation of WM connections) (94), but also concerning the indications of potential reoperation(s) (95). Indeed, the degree of additional functional reorganization occurring after the first surgery and making (or not) possible subsequent resection(s) is constrained by the prominent LGG relapse within the subcortical connectivity (96).…”

Section: Towards More Consideration Of Wm Tracts For An Adapted Manag...supporting

confidence: 59%

White Matter Tracts and Diffuse Lower-Grade Gliomas: The Pivotal Role of Myelin Plasticity in the Tumor Pathogenesis, Infiltration Patterns, Functional Consequences and Therapeutic Management

Duffau

2022

Front. Oncol.

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For many decades, interactions between diffuse lower-grade glioma (LGG) and brain connectome were neglected. However, the neoplasm progression is intimately linked to its environment, especially the white matter (WM) tracts and their myelin status. First, while the etiopathogenesis of LGG is unclear, this tumor seems to appear during the adolescence, and it is mostly located within anterior and associative cerebral areas. Because these structures correspond to those which were myelinated later in the brain maturation process, WM myelination could play a role in the development of LGG. Second, WM fibers and the myelin characteristics also participate in LGG diffusion, since glioma cells migrate along the subcortical pathways, especially when exhibiting a demyelinated phenotype, which may result in a large invasion of the parenchyma. Third, such a migratory pattern can induce functional (neurological, cognitive and behavioral) disturbances, because myelinated WM tracts represent the main limitation of neuroplastic potential. These parameters are critical for tailoring an individualized therapeutic strategy, both (i) regarding the timing of active treatment(s) which must be proposed earlier, before a too wide glioma infiltration along the WM bundles, (ii) and regarding the anatomic extent of surgical resection and irradiation, which should take account of the subcortical connectivity. Therefore, the new science of connectomics must be integrated in LGG management, based upon an improved understanding of the interplay across glioma dissemination within WM and reactional neural networks reconfiguration, in order to optimize long-term oncological and functional outcomes. To this end, mechanisms of activity-dependent myelin plasticity should be better investigated.

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Section: Towards More Consideration Of Wm Tracts For An Adapted Manag...supporting

confidence: 59%

White Matter Tracts and Diffuse Lower-Grade Gliomas: The Pivotal Role of Myelin Plasticity in the Tumor Pathogenesis, Infiltration Patterns, Functional Consequences and Therapeutic Management

Duffau

2022

Front. Oncol.

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“…The goal was to identify and preserve the arcuate fasciculus (AF) (which generates phonological disorders during DES), the inferior fronto-occipital fasciculus (IFOF) (which induces semantics disturbances during DES), the somatosensory thalamocortical pathway (TCP) (which elicits dysesthesia or pain during DES), the pyramidal pathway (PT) (which evokes involuntary movement during DES), and/or the optic radiation (OR) (which causes visual disorders during DES). Resections were thus pursued until critical neural networks were encountered around the whole surgical cavity, with no margin around eloquent structures, to optimize the extent of resection (EOR) ( 14 ).…”

Section: Methodsmentioning

confidence: 99%

Awake Surgery for Left Posterior Insular Low-Grade Glioma Through the Parietorolandic Operculum: The Need to Preserve the Functional Connectivity. A Case Series

Duffau

2022

Front. Surg.

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Objective: Surgical approach to low-grade glioma (LGG) involving the posterior insula is challenging, especially in the left hemisphere, with a high risk of sensorimotor, language, or visual deterioration. In this study, a case series of 5 right-handed patients harboring a left posterior insular LGG is reported, by detailing a transcorticosubcortical approach.Method: The five surgeries were achieved in awake patients using cortical and axonal electrostimulation mapping. The glioma was removed through the left rolandic and/or parietal opercula, with preservation of the subcortical connectivity.Results: The cortical mapping was positive in the five patients, enabling the selection of an optimal transcortical approach, via the anterolateral supramarginal gyrus in four patients and/or via the lateral retrocentral gyrus in three cases (plus through the left superior temporal gyrus in one case). Moreover, the white matter tracts were identified in all cases, i.e., the lateral part of the superior longitudinal fasciculus (five cases), the arcuate fasciculus (four cases), the thalamocortical somatosensory pathways (four cases), the motor pathway (one case), the semantic pathway (three cases), and the optic tract (one case). Complete resection of the LGG was achieved in two patients and near-total resection in three patients. There were no postoperative permanent sensorimotor, language, or visual deficits.Conclusion: A transcortical approach through the parietorolandic operculum in awake patients represents safe and effective access to the left posterior insular LGG. Detection and preservation of the functional connectivity using direct electrostimulation of the white matter bundles are needed in this cross-road brain region to prevent otherwise predictable postsurgical impairments.

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“…Tumor growth patterns could be further assessed with large-scale data using normative structural connectomics. Two recently published reviews also suggest the application of brain connectomics for glioma surgery [50,51]. Similarly, understanding tumor behaviors and associated symptoms might require a whole-brain approach [52].…”

Section: Neuro-oncology Applicationsmentioning

confidence: 99%

Untapped Neuroimaging Tools for Neuro-Oncology: Connectomics and Spatial Transcriptomics

Germann

Zadeh

Mansouri

et al. 2022

Cancers

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Neuro-oncology research is broad and includes several branches, one of which is neuroimaging. Magnetic resonance imaging (MRI) is instrumental for the diagnosis and treatment monitoring of patients with brain tumors. Most commonly, structural and perfusion MRI sequences are acquired to characterize tumors and understand their behaviors. Thanks to technological advances, structural brain MRI can now be transformed into a so-called average brain accounting for individual morphological differences, which enables retrospective group analysis. These normative analyses are uncommonly used in neuro-oncology research. Once the data have been normalized, voxel-wise analyses and spatial mapping can be performed. Additionally, investigations of underlying connectomics can be performed using functional and structural templates. Additionally, a recently available template of spatial transcriptomics has enabled the assessment of associated gene expression. The few published normative analyses have shown relationships between tumor characteristics and spatial localization, as well as insights into the circuitry associated with epileptogenic tumors and depression after cingulate tumor resection. The wide breadth of possibilities with normative analyses remain largely unexplored, specifically in terms of connectomics and imaging transcriptomics. We provide a framework for performing normative analyses in oncology while also highlighting their limitations. Normative analyses are an opportunity to address neuro-oncology questions from a different perspective.

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Brain connectomics applied to oncological neuroscience: from a traditional surgical strategy focusing on glioma topography to a meta-network approach

Cited by 45 publications

References 118 publications

White Matter Tracts and Diffuse Lower-Grade Gliomas: The Pivotal Role of Myelin Plasticity in the Tumor Pathogenesis, Infiltration Patterns, Functional Consequences and Therapeutic Management

White Matter Tracts and Diffuse Lower-Grade Gliomas: The Pivotal Role of Myelin Plasticity in the Tumor Pathogenesis, Infiltration Patterns, Functional Consequences and Therapeutic Management

Awake Surgery for Left Posterior Insular Low-Grade Glioma Through the Parietorolandic Operculum: The Need to Preserve the Functional Connectivity. A Case Series

Untapped Neuroimaging Tools for Neuro-Oncology: Connectomics and Spatial Transcriptomics

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