The link between gliomas infiltration and white matter architecture investigated with electron microscopy and diffusion tensor imaging

Latini, Francesco; Fahlström, Markus; Beháňová, Andrea; Sintorn, Ida‐Maria; Hodik, Monika; Staxäng, Karin; Ryttlefors, Mats

doi:10.1016/j.nicl.2021.102735

Cited by 18 publications

(12 citation statements)

References 80 publications

(131 reference statements)

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“…Studies on PTZ patterns of WM displacement and/or invasion may be important for understanding how much functional brain tissue is compromised, because invasion of the WM tract connectivity prior to surgery represents a main limitation of neuroplasticity [35]. Latini et al (2021), when trying to understand whether specific features of the different WM pathways could reflect the differences in observed glioma infiltration, built a theory that a smaller fiber diameter, decreased fiber density and increased extracellular space may represent pathways of least resistance for glioma cell dissemination [36]. In the same spirit, a recent review on DLGG interaction with WM tracts suggested that myelin may constitute a protection against glioma cell migration; therefore, its nonexistence or destruction could result in fragility sites facilitating tumor invasiveness [37].…”

Section: Dlgg Heterogeneity and Relation With The Surrounding Brain: ...mentioning

confidence: 99%

The Concept of «Peritumoral Zone» in Diffuse Low-Grade Gliomas: Oncological and Functional Implications for a Connectome-Guided Therapeutic Attitude

2022

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Diffuse low-grade gliomas (DLGGs) are heterogeneous and poorly circumscribed neoplasms with isolated tumor cells that extend beyond the margins of the lesion depicted on MRI. Efforts to demarcate the glioma core from the surrounding healthy brain led us to define an intermediate region, the so-called peritumoral zone (PTZ). Although most studies about PTZ have been conducted on high-grade gliomas, the purpose here is to review the cellular, metabolic, and radiological characteristics of PTZ in the specific context of DLGG. A better delineation of PTZ, in which glioma cells and neural tissue strongly interact, may open new therapeutic avenues to optimize both functional and oncological results. First, a connectome-based “supratotal” surgical resection (i.e., with the removal of PTZ in addition to the tumor core) resulted in prolonged survival by limiting the risk of malignant transformation, while improving the quality of life, thanks to a better control of seizures. Second, the timing and order of (neo)adjuvant medical treatments can be modulated according to the pattern of peritumoral infiltration. Third, the development of new drugs specifically targeting the PTZ could be considered from an oncological (such as immunotherapy) and epileptological perspective. Further multimodal investigations of PTZ are needed to maximize long-term outcomes in DLGG patients.

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Section: Dlgg Heterogeneity and Relation With The Surrounding Brain: ...mentioning

confidence: 99%

The Concept of «Peritumoral Zone» in Diffuse Low-Grade Gliomas: Oncological and Functional Implications for a Connectome-Guided Therapeutic Attitude

2022

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“…In recent years, this field has gradually shifted from exploring the relationship between macroscopic, whole-brain diffusion tensor changes and tumor progression, to exploring the relationship between local, www.nature.com/scientificreports/ microscopic fiber bundle changes and local tumor invasion. Previous work has revealed that voxels with higher RD and lower FA are associated with glioma cell infiltration 15 . Among the existing studies, only one has focused on insular glioma.…”

Section: Discussionmentioning

confidence: 99%

“…Due to the unique anatomical location of the insular lobe, the relationship of insular glioma to surrounding fiber bundles is more complicated than that of general intracranial tumors. Using traditional imaging data, previous studies have focused on qualitative analyses of the fiber bundles that may be involved in insular tumors [13][14][15] . These studies could only assess changes in the surrounding fibers due to invasion or edema, which could not be remodeled to preserve local function; such plastic changes in white matter typically occur distal to the tumor.…”

Section: Discussionmentioning

confidence: 99%

Microstructural changes of white matter fiber tracts induced by insular glioma revealed by tract-based spatial statistics and automatic fiber quantification

Wang

Zhou

Wang

et al. 2022

Sci Rep

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Gliomas typically grow along white matter fiber tracts, yet their invasion patterns remain unclear. This study assessed the effect of insular glioma on large white matter fiber tracts and the microstructural subcortical changes associated with clinical outcomes in patients with insular glioma. Twenty-five patients with insular glioma were enrolled and divided into left and right groups according to tumor lateralization. The control group comprised 14 healthy volunteers. Subjects in both the glioma and control groups underwent diffusion tensor magnetic resonance imaging at 3.0 T. The characteristics of white matter fiber bundles were analyzed using tract-based spatial statistics and automatic fiber quantification. Both Automatic Fiber Quantification and Tract-Based Spatial Statistics revealed that patients with insular glioma had significantly lower fractional anisotropy (FA) values in the inferior frontal-occipital fasciculus and uncinate fasciculus ipsilateral to the tumor, than the controls. Fractional anisotropy associated with mean diffusivity values several large fiber tracts showed potential on tumor-grade distinguishing. Diffusion metrics can sensitively detect microstructural changes in tumor progression. Insular glioma significantly affects the microstructure of white matter fibers proximal to the tumor. The range of white matter fiber bundles affected differs according to the grade of the glioma. These changes are mainly associated with early-stage tumor invasion.

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“…In a study of 1097 cases, a tumor located in a nonfrontal area was an independent factor of poor prognosis [ 10 ]. With its invasive profile, glioma has a high propension to migrate along the subcortical fibers, as shown radiologically [ 41 , 42 ] as well as pathologically: biopsy samples evidenced that the tumor cells followed the white matter tracts and were slightly more concentrated in the peripheral parts of those tracts [ 43 ]. It seems that the myelin status could play a pivotal role not only in LGG invasion in adults but also possibly in its origin in teenagers [ 44 ].…”

Section: Predicting Oncological Interindividual Variability and Its C...mentioning

confidence: 99%

A Personalized Longitudinal Strategy in Low-Grade Glioma Patients: Predicting Oncological and Neural Interindividual Variability and Its Changes over Years to Think One Step Ahead

Duffau

2022

JPM

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Diffuse low-grade glioma (LGG) is a rare cerebral cancer, mostly involving young adults with an active life at diagnosis. If left untreated, LGG widely invades the brain and becomes malignant, generating neurological worsening and ultimately death. Early and repeat treatments for this incurable tumor, including maximal connectome-based surgical resection(s) in awake patients, enable postponement of malignant transformation while preserving quality of life owing to constant neural network reconfiguration. Due to considerable interindividual variability in terms of LGG course and consecutive cerebral reorganization, a multistage longitudinal strategy should be tailored accordingly in each patient. It is crucial to predict how the glioma will progress (changes in growth rate and pattern of migration, genetic mutation, etc.) and how the brain will adapt (changes in patterns of spatiotemporal redistribution, possible functional consequences such as epilepsy or cognitive decline, etc.). The goal is to anticipate therapeutic management, remaining one step ahead in order to select the optimal (re-)treatment(s) (some of them possibly kept in reserve), at the appropriate time(s) in the evolution of this chronic disease, before malignization and clinical worsening. Here, predictive tumoral and non-tumoral factors, and their ever-changing interactions, are reviewed to guide individual decisions in advance based on patient-specific markers, for the treatment of LGG.

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The link between gliomas infiltration and white matter architecture investigated with electron microscopy and diffusion tensor imaging

Cited by 18 publications

References 80 publications

The Concept of «Peritumoral Zone» in Diffuse Low-Grade Gliomas: Oncological and Functional Implications for a Connectome-Guided Therapeutic Attitude

The Concept of «Peritumoral Zone» in Diffuse Low-Grade Gliomas: Oncological and Functional Implications for a Connectome-Guided Therapeutic Attitude

Microstructural changes of white matter fiber tracts induced by insular glioma revealed by tract-based spatial statistics and automatic fiber quantification

A Personalized Longitudinal Strategy in Low-Grade Glioma Patients: Predicting Oncological and Neural Interindividual Variability and Its Changes over Years to Think One Step Ahead

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