Assessment of structural disconnections in gliomas: comparison of indirect and direct approaches

Abstract

Gliomas are amongst the most common primary brain tumours in adults and are often associated with poor prognosis. Understanding the extent of white matter (WM) which is affected outside the tumoral lesion may be of paramount importance to explain cognitive deficits and the clinical progression of the disease. To this end, we explored both direct (i.e., tractography based) and indirect (i.e., atlas-based) approaches to quantifying WM structural disconnections in a cohort of 44 high- and low-grade glioma patients. While these methodologies have recently gained popularity in the context of stroke and other pathologies, to our knowledge, this is the first time they are applied in patients with brain tumours. More specifically, in this work, we present a quantitative comparison of the disconnection maps provided by the two methodologies by applying well-known metrics of spatial similarity, extension, and correlation. Given the important role the oedematous tissue plays in the physiopathology of tumours, we performed these analyses both by including and excluding it in the definition of the tumoral lesion. This was done to investigate possible differences determined by this choice. We found that direct and indirect approaches offer two distinct pictures of structural disconnections in patients affected by brain gliomas, presenting key differences in several regions of the brain. Following the outcomes of our analysis, we eventually discuss the strengths and pitfalls of these two approaches when applied in this critical field.

Longitudinal prediction of motor dysfunction after stroke: a disconnectome study

“…When comparing those methods, the disconnection analysis often explains more variance in data than lesion load analysis (Corbetta et al 2015 ; Hope et al 2016 ). The disconnection analysis (Conrad et al 2022 ; Hajhajate et al 2022 ; Forkel et al 2022 ; Souter et al 2022 ; Silvestri et al 2022 ; Sperber et al 2022 ) is different from the lesion network symptom mapping methods that estimate from a normative dataset the functional connectivity impaired by a lesion (Boes et al 2015 ; Bowren et al 2022 ; Cotovio et al 2022 ). Thus, prediction studies may benefit from the redirection of the focus in clinical research from lesion localisation analysis to the analysis of the disconnections where remote alterations of a focal damage to distant regions can also be considered as a contributor to a network of structures and functions.…”

White Matter Tract Density Index Prediction Model of Overall Survival in Glioblastoma

“…The availability of large MRI databases has allowed for the indirect estimation of disconnection following brain lesions using novel methods in which lesions are embedded into normative connectome atlases . These approaches have been extensively used in the study of stroke but only preliminarily in tumors …”

“…[32][33][34] These approaches have been extensively used in the study of stroke 25,[35][36][37][38] but only preliminarily in tumors. 39 On the basis of these premises, we have developed a hypothesis that the prognosis of GBM may be linked to the organization of WM affected by a specific GBM lesion. Our hypothesis suggests that tumors localizing in WM regions with a high density of tracts may have a worse outcome.…”

Longitudinal prediction of motor dysfunction after stroke: a disconnectome study

“…When comparing those methods, the disconnection analysis often explains more variance in data than lesion load analysis (Corbetta et al 2015; Hope et al 2016). The disconnection analysis (Conrad et al, 2022; Hajhajate et al, 2022; Forkel et al 2022); Souter et al, 2022; Silvestri et al, 2022; Sperber et al, 2022) is different from the lesion network symptom mapping methods that estimate from a normative dataset the functional connectivity impaired by a lesion (Boes et al 2015; Bowren et al, 2022; Cototvio et al, 2022). Thus, prediction studies may benefit from the redirection of the focus in clinical research from lesion localisation analysis to the analysis of the disconnections where remote alterations of a focal damage to distant regions can also be considered as a contributor to a network of structures and functions.…”