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Directionally encoded color track density imaging in brain tumor patients: A potential application to neuro-oncology surgical planning

BACKGROUND: Diffusion magnetic resonance imaging white matter tractography, an increasingly popular preoperative planning modality used for pre-surgical planning in brain tumor patients, is employed with the goal of maximizing tumor resection while sparing postoperative neurological function. Clinic...

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Autores principales: Sullivan, Jared J., Zekelman, Leo R., Zhang, Fan, Juvekar, Parikshit, Torio, Erickson F., Bunevicius, Adomas, Essayed, Walid I., Bastos, Dhiego, He, Jianzhong, Rigolo, Laura, Golby, Alexandra J., O'Donnell, Lauren J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10165166/
https://www.ncbi.nlm.nih.gov/pubmed/37116355
http://dx.doi.org/10.1016/j.nicl.2023.103412
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author Sullivan, Jared J.
Zekelman, Leo R.
Zhang, Fan
Juvekar, Parikshit
Torio, Erickson F.
Bunevicius, Adomas
Essayed, Walid I.
Bastos, Dhiego
He, Jianzhong
Rigolo, Laura
Golby, Alexandra J.
O'Donnell, Lauren J.
author_facet Sullivan, Jared J.
Zekelman, Leo R.
Zhang, Fan
Juvekar, Parikshit
Torio, Erickson F.
Bunevicius, Adomas
Essayed, Walid I.
Bastos, Dhiego
He, Jianzhong
Rigolo, Laura
Golby, Alexandra J.
O'Donnell, Lauren J.
author_sort Sullivan, Jared J.
collection PubMed
description BACKGROUND: Diffusion magnetic resonance imaging white matter tractography, an increasingly popular preoperative planning modality used for pre-surgical planning in brain tumor patients, is employed with the goal of maximizing tumor resection while sparing postoperative neurological function. Clinical translation of white matter tractography has been limited by several shortcomings of standard diffusion tensor imaging (DTI), including poor modeling of fibers crossing through regions of peritumoral edema and low spatial resolution for typical clinical diffusion MRI (dMRI) sequences. Track density imaging (TDI) is a post-tractography technique that uses the number of tractography streamlines and their long-range continuity to map the white matter connections of the brain with enhanced image resolution relative to the acquired dMRI data, potentially offering improved white matter visualization in patients with brain tumors. The aim of this study was to assess the utility of TDI-based white matter maps in a neurosurgical planning context compared to the current clinical standard of DTI-based white matter maps. METHODS: Fourteen consecutive brain tumor patients from a single institution were retrospectively selected for the study. Each patient underwent 3-Tesla dMRI scanning with 30 gradient directions and a b-value of 1000 s/mm(2). For each patient, two directionally encoded color (DEC) maps were produced as follows. DTI-based DEC-fractional anisotropy maps (DEC-FA) were generated on the scanner, while DEC-track density images (DEC-TDI) were generated using constrained spherical deconvolution based tractography. The potential clinical utility of each map was assessed by five practicing neurosurgeons, who rated the maps according to four clinical utility statements regarding different clinical aspects of pre-surgical planning. The neurosurgeons rated each map according to their agreement with four clinical utility statements regarding if the map 1 identified clinically relevant tracts, (2) helped establish a goal resection margin, (3) influenced a planned surgical route, and (4) was useful overall. Cumulative link mixed effect modeling and analysis of variance were performed to test the primary effect of map type (DEC-TDI vs. DEC-FA) on rater score. Pairwise comparisons using estimated marginal means were then calculated to determine the magnitude and directionality of differences in rater scores by map type. RESULTS: A majority of rater responses agreed with the four clinical utility statements, indicating that neurosurgeons found both DEC maps to be useful. Across all four investigated clinical utility statements, the DEC map type significantly influenced rater score. Rater scores were significantly higher for DEC-TDI maps compared to DEC-FA maps. The largest effect size in rater scores in favor of DEC-TDI maps was observed for clinical utility statement 2, which assessed establishing a goal resection margin. CONCLUSION: We observed a significant neurosurgeon preference for DEC-TDI maps, indicating their potential utility for neurosurgical planning.
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spelling pubmed-101651662023-05-09 Directionally encoded color track density imaging in brain tumor patients: A potential application to neuro-oncology surgical planning Sullivan, Jared J. Zekelman, Leo R. Zhang, Fan Juvekar, Parikshit Torio, Erickson F. Bunevicius, Adomas Essayed, Walid I. Bastos, Dhiego He, Jianzhong Rigolo, Laura Golby, Alexandra J. O'Donnell, Lauren J. Neuroimage Clin Regular Article BACKGROUND: Diffusion magnetic resonance imaging white matter tractography, an increasingly popular preoperative planning modality used for pre-surgical planning in brain tumor patients, is employed with the goal of maximizing tumor resection while sparing postoperative neurological function. Clinical translation of white matter tractography has been limited by several shortcomings of standard diffusion tensor imaging (DTI), including poor modeling of fibers crossing through regions of peritumoral edema and low spatial resolution for typical clinical diffusion MRI (dMRI) sequences. Track density imaging (TDI) is a post-tractography technique that uses the number of tractography streamlines and their long-range continuity to map the white matter connections of the brain with enhanced image resolution relative to the acquired dMRI data, potentially offering improved white matter visualization in patients with brain tumors. The aim of this study was to assess the utility of TDI-based white matter maps in a neurosurgical planning context compared to the current clinical standard of DTI-based white matter maps. METHODS: Fourteen consecutive brain tumor patients from a single institution were retrospectively selected for the study. Each patient underwent 3-Tesla dMRI scanning with 30 gradient directions and a b-value of 1000 s/mm(2). For each patient, two directionally encoded color (DEC) maps were produced as follows. DTI-based DEC-fractional anisotropy maps (DEC-FA) were generated on the scanner, while DEC-track density images (DEC-TDI) were generated using constrained spherical deconvolution based tractography. The potential clinical utility of each map was assessed by five practicing neurosurgeons, who rated the maps according to four clinical utility statements regarding different clinical aspects of pre-surgical planning. The neurosurgeons rated each map according to their agreement with four clinical utility statements regarding if the map 1 identified clinically relevant tracts, (2) helped establish a goal resection margin, (3) influenced a planned surgical route, and (4) was useful overall. Cumulative link mixed effect modeling and analysis of variance were performed to test the primary effect of map type (DEC-TDI vs. DEC-FA) on rater score. Pairwise comparisons using estimated marginal means were then calculated to determine the magnitude and directionality of differences in rater scores by map type. RESULTS: A majority of rater responses agreed with the four clinical utility statements, indicating that neurosurgeons found both DEC maps to be useful. Across all four investigated clinical utility statements, the DEC map type significantly influenced rater score. Rater scores were significantly higher for DEC-TDI maps compared to DEC-FA maps. The largest effect size in rater scores in favor of DEC-TDI maps was observed for clinical utility statement 2, which assessed establishing a goal resection margin. CONCLUSION: We observed a significant neurosurgeon preference for DEC-TDI maps, indicating their potential utility for neurosurgical planning. Elsevier 2023-04-20 /pmc/articles/PMC10165166/ /pubmed/37116355 http://dx.doi.org/10.1016/j.nicl.2023.103412 Text en © 2023 The Authors https://creativecommons.org/licenses/by/4.0/This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Regular Article
Sullivan, Jared J.
Zekelman, Leo R.
Zhang, Fan
Juvekar, Parikshit
Torio, Erickson F.
Bunevicius, Adomas
Essayed, Walid I.
Bastos, Dhiego
He, Jianzhong
Rigolo, Laura
Golby, Alexandra J.
O'Donnell, Lauren J.
Directionally encoded color track density imaging in brain tumor patients: A potential application to neuro-oncology surgical planning
title Directionally encoded color track density imaging in brain tumor patients: A potential application to neuro-oncology surgical planning
title_full Directionally encoded color track density imaging in brain tumor patients: A potential application to neuro-oncology surgical planning
title_fullStr Directionally encoded color track density imaging in brain tumor patients: A potential application to neuro-oncology surgical planning
title_full_unstemmed Directionally encoded color track density imaging in brain tumor patients: A potential application to neuro-oncology surgical planning
title_short Directionally encoded color track density imaging in brain tumor patients: A potential application to neuro-oncology surgical planning
title_sort directionally encoded color track density imaging in brain tumor patients: a potential application to neuro-oncology surgical planning
topic Regular Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10165166/
https://www.ncbi.nlm.nih.gov/pubmed/37116355
http://dx.doi.org/10.1016/j.nicl.2023.103412
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