From Neurosurgical Planning to Histopathological Brain Tumor Characterization: Potentialities of Arcuate Fasciculus Along-Tract Diffusion Tensor Imaging Tractography Measures

Background: Tractography has been widely adopted to improve brain gliomas' surgical planning and guide their resection. This study aimed to evaluate state-of-the-art of arcuate fasciculus (AF) tractography for surgical planning and explore the role of along-tract analyses in vivo for characteri...

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Main Authors: Matteo Zoli, Lia Talozzi, Matteo Martinoni, David N. Manners, Filippo Badaloni, Claudia Testa, Sofia Asioli, Micaela Mitolo, Fiorina Bartiromo, Magali Jane Rochat, Viscardo Paolo Fabbri, Carmelo Sturiale, Alfredo Conti, Raffaele Lodi, Diego Mazzatenta, Caterina Tonon
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-02-01
Series:Frontiers in Neurology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fneur.2021.633209/full
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author Matteo Zoli
Matteo Zoli
Lia Talozzi
Matteo Martinoni
David N. Manners
Filippo Badaloni
Claudia Testa
Sofia Asioli
Sofia Asioli
Micaela Mitolo
Fiorina Bartiromo
Magali Jane Rochat
Viscardo Paolo Fabbri
Carmelo Sturiale
Alfredo Conti
Alfredo Conti
Raffaele Lodi
Raffaele Lodi
Diego Mazzatenta
Diego Mazzatenta
Caterina Tonon
Caterina Tonon
author_facet Matteo Zoli
Matteo Zoli
Lia Talozzi
Matteo Martinoni
David N. Manners
Filippo Badaloni
Claudia Testa
Sofia Asioli
Sofia Asioli
Micaela Mitolo
Fiorina Bartiromo
Magali Jane Rochat
Viscardo Paolo Fabbri
Carmelo Sturiale
Alfredo Conti
Alfredo Conti
Raffaele Lodi
Raffaele Lodi
Diego Mazzatenta
Diego Mazzatenta
Caterina Tonon
Caterina Tonon
author_sort Matteo Zoli
collection DOAJ
description Background: Tractography has been widely adopted to improve brain gliomas' surgical planning and guide their resection. This study aimed to evaluate state-of-the-art of arcuate fasciculus (AF) tractography for surgical planning and explore the role of along-tract analyses in vivo for characterizing tumor histopathology.Methods: High angular resolution diffusion imaging (HARDI) images were acquired for nine patients with tumors located in or near language areas (age: 41 ± 14 years, mean ± standard deviation; five males) and 32 healthy volunteers (age: 39 ± 16 years; 16 males). Phonemic fluency task fMRI was acquired preoperatively for patients. AF tractography was performed using constrained spherical deconvolution diffusivity modeling and probabilistic fiber tracking. Along-tract analyses were performed, dividing the AF into 15 segments along the length of the tract defined using the Laplacian operator. For each AF segment, diffusion tensor imaging (DTI) measures were compared with those obtained in healthy controls (HCs). The hemispheric laterality index (LI) was calculated from language task fMRI activations in the frontal, parietal, and temporal lobe parcellations. Tumors were grouped into low/high grade (LG/HG).Results: Four tumors were LG gliomas (one dysembryoplastic neuroepithelial tumor and three glioma grade II) and five HG gliomas (two grade III and three grade IV). For LG tumors, gross total removal was achieved in all but one case, for HG in two patients. Tractography identified the AF trajectory in all cases. Four along-tract DTI measures potentially discriminated LG and HG tumor patients (false discovery rate < 0.1): the number of abnormal MD and RD segments, median AD, and MD measures. Both a higher number of abnormal AF segments and a higher AD and MD measures were associated with HG tumor patients. Moreover, correlations (unadjusted p < 0.05) were found between the parietal lobe LI and the DTI measures, which discriminated between LG and HG tumor patients. In particular, a more rightward parietal lobe activation (LI < 0) correlated with a higher number of abnormal MD segments (R = −0.732) and RD segments (R = −0.724).Conclusions: AF tractography allows to detect the course of the tract, favoring the safer-as-possible tumor resection. Our preliminary study shows that along-tract DTI metrics can provide useful information for differentiating LG and HG tumors during pre-surgical tumor characterization.
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spelling doaj.art-e86f3175757a477da3f80c047fa2df8d2022-12-21T20:24:42ZengFrontiers Media S.A.Frontiers in Neurology1664-22952021-02-011210.3389/fneur.2021.633209633209From Neurosurgical Planning to Histopathological Brain Tumor Characterization: Potentialities of Arcuate Fasciculus Along-Tract Diffusion Tensor Imaging Tractography MeasuresMatteo Zoli0Matteo Zoli1Lia Talozzi2Matteo Martinoni3David N. Manners4Filippo Badaloni5Claudia Testa6Sofia Asioli7Sofia Asioli8Micaela Mitolo9Fiorina Bartiromo10Magali Jane Rochat11Viscardo Paolo Fabbri12Carmelo Sturiale13Alfredo Conti14Alfredo Conti15Raffaele Lodi16Raffaele Lodi17Diego Mazzatenta18Diego Mazzatenta19Caterina Tonon20Caterina Tonon21Pituitary Unit, IRCCS Istituto delle Scienze Neurologiche di Bologna, Bologna, ItalyDepartment of Biomedical and Neuromotor Sciences, University of Bologna, Bologna, ItalyDepartment of Biomedical and Neuromotor Sciences, University of Bologna, Bologna, ItalyNeurosurgery Unit, IRCCS Istituto delle Scienze Neurologiche di Bologna, Bologna, ItalyDepartment of Biomedical and Neuromotor Sciences, University of Bologna, Bologna, ItalyNeurosurgery Unit, IRCCS Istituto delle Scienze Neurologiche di Bologna, Bologna, ItalyDepartment of Physics and Astronomy, University of Bologna, Bologna, ItalyDepartment of Biomedical and Neuromotor Sciences, University of Bologna, Bologna, ItalyAnatomic Pathology Unit, Azienda USL di Bologna, Bologna, ItalyFunctional and Molecular Neuroimaging Unit, IRCCS Istituto delle Scienze Neurologiche di Bologna, Bologna, ItalyFunctional and Molecular Neuroimaging Unit, IRCCS Istituto delle Scienze Neurologiche di Bologna, Bologna, ItalyFunctional and Molecular Neuroimaging Unit, IRCCS Istituto delle Scienze Neurologiche di Bologna, Bologna, ItalyDepartment of Biomedical and Neuromotor Sciences, University of Bologna, Bologna, ItalyNeurosurgery Unit, IRCCS Istituto delle Scienze Neurologiche di Bologna, Bologna, ItalyDepartment of Biomedical and Neuromotor Sciences, University of Bologna, Bologna, ItalyNeurosurgery Unit, IRCCS Istituto delle Scienze Neurologiche di Bologna, Bologna, ItalyDepartment of Biomedical and Neuromotor Sciences, University of Bologna, Bologna, ItalyFunctional and Molecular Neuroimaging Unit, IRCCS Istituto delle Scienze Neurologiche di Bologna, Bologna, ItalyPituitary Unit, IRCCS Istituto delle Scienze Neurologiche di Bologna, Bologna, ItalyDepartment of Biomedical and Neuromotor Sciences, University of Bologna, Bologna, ItalyDepartment of Biomedical and Neuromotor Sciences, University of Bologna, Bologna, ItalyFunctional and Molecular Neuroimaging Unit, IRCCS Istituto delle Scienze Neurologiche di Bologna, Bologna, ItalyBackground: Tractography has been widely adopted to improve brain gliomas' surgical planning and guide their resection. This study aimed to evaluate state-of-the-art of arcuate fasciculus (AF) tractography for surgical planning and explore the role of along-tract analyses in vivo for characterizing tumor histopathology.Methods: High angular resolution diffusion imaging (HARDI) images were acquired for nine patients with tumors located in or near language areas (age: 41 ± 14 years, mean ± standard deviation; five males) and 32 healthy volunteers (age: 39 ± 16 years; 16 males). Phonemic fluency task fMRI was acquired preoperatively for patients. AF tractography was performed using constrained spherical deconvolution diffusivity modeling and probabilistic fiber tracking. Along-tract analyses were performed, dividing the AF into 15 segments along the length of the tract defined using the Laplacian operator. For each AF segment, diffusion tensor imaging (DTI) measures were compared with those obtained in healthy controls (HCs). The hemispheric laterality index (LI) was calculated from language task fMRI activations in the frontal, parietal, and temporal lobe parcellations. Tumors were grouped into low/high grade (LG/HG).Results: Four tumors were LG gliomas (one dysembryoplastic neuroepithelial tumor and three glioma grade II) and five HG gliomas (two grade III and three grade IV). For LG tumors, gross total removal was achieved in all but one case, for HG in two patients. Tractography identified the AF trajectory in all cases. Four along-tract DTI measures potentially discriminated LG and HG tumor patients (false discovery rate < 0.1): the number of abnormal MD and RD segments, median AD, and MD measures. Both a higher number of abnormal AF segments and a higher AD and MD measures were associated with HG tumor patients. Moreover, correlations (unadjusted p < 0.05) were found between the parietal lobe LI and the DTI measures, which discriminated between LG and HG tumor patients. In particular, a more rightward parietal lobe activation (LI < 0) correlated with a higher number of abnormal MD segments (R = −0.732) and RD segments (R = −0.724).Conclusions: AF tractography allows to detect the course of the tract, favoring the safer-as-possible tumor resection. Our preliminary study shows that along-tract DTI metrics can provide useful information for differentiating LG and HG tumors during pre-surgical tumor characterization.https://www.frontiersin.org/articles/10.3389/fneur.2021.633209/fullneurosurgerytractographyarcuate fasciculusalong-tractgliomas gradinglanguage network
spellingShingle Matteo Zoli
Matteo Zoli
Lia Talozzi
Matteo Martinoni
David N. Manners
Filippo Badaloni
Claudia Testa
Sofia Asioli
Sofia Asioli
Micaela Mitolo
Fiorina Bartiromo
Magali Jane Rochat
Viscardo Paolo Fabbri
Carmelo Sturiale
Alfredo Conti
Alfredo Conti
Raffaele Lodi
Raffaele Lodi
Diego Mazzatenta
Diego Mazzatenta
Caterina Tonon
Caterina Tonon
From Neurosurgical Planning to Histopathological Brain Tumor Characterization: Potentialities of Arcuate Fasciculus Along-Tract Diffusion Tensor Imaging Tractography Measures
Frontiers in Neurology
neurosurgery
tractography
arcuate fasciculus
along-tract
gliomas grading
language network
title From Neurosurgical Planning to Histopathological Brain Tumor Characterization: Potentialities of Arcuate Fasciculus Along-Tract Diffusion Tensor Imaging Tractography Measures
title_full From Neurosurgical Planning to Histopathological Brain Tumor Characterization: Potentialities of Arcuate Fasciculus Along-Tract Diffusion Tensor Imaging Tractography Measures
title_fullStr From Neurosurgical Planning to Histopathological Brain Tumor Characterization: Potentialities of Arcuate Fasciculus Along-Tract Diffusion Tensor Imaging Tractography Measures
title_full_unstemmed From Neurosurgical Planning to Histopathological Brain Tumor Characterization: Potentialities of Arcuate Fasciculus Along-Tract Diffusion Tensor Imaging Tractography Measures
title_short From Neurosurgical Planning to Histopathological Brain Tumor Characterization: Potentialities of Arcuate Fasciculus Along-Tract Diffusion Tensor Imaging Tractography Measures
title_sort from neurosurgical planning to histopathological brain tumor characterization potentialities of arcuate fasciculus along tract diffusion tensor imaging tractography measures
topic neurosurgery
tractography
arcuate fasciculus
along-tract
gliomas grading
language network
url https://www.frontiersin.org/articles/10.3389/fneur.2021.633209/full
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