Free water modeling of peritumoral edema using multi-fiber tractography: application to tracking the arcuate fasciculus for neurosurgical planning
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PURPOSE: Peritumoral edema impedes the full delineation of fiber tracts due to partial volume effects in image voxels that contain a mixture of cerebral parenchyma and extracellular water. The purpose of this study is to investigate the effect of incorporating a free water (FW) model of edema for white matter tractography in the presence of edema. MATERIALS AND METHODS: We retrospectively evaluated 26 consecutive brain tumor patients with diffusion MRI and T2-weighted images acquired presurgically. Tractography of the arcuate fasciculus (AF) was performed using the two-tensor unscented Kalman filter tractography (UKFt) method, the UKFt method with a reduced fiber tracking stopping fractional anisotropy (FA) threshold (UKFt+rFA), and the UKFt method with the addition of a FW compartment (UKFt+FW). An automated white matter fiber tract identification approach was applied to delineate the AF. Quantitative measurements included tract volume, edema volume, and mean FW fraction. Visual comparisons were performed by three experts to evaluate the quality of the detected AF tracts. RESULTS: The AF volume in edematous brain hemispheres was significantly larger using the UKFt+FW method (p<0.0001) compared to UKFt, but not significantly larger (p = 0.0996) in hemispheres without edema. The AF size increase depended on the volume of edema: a significant correlation was found between AF volume affected by (intersecting) edema and AF volume change with the FW model (Pearson r = 0.806, p<0.0001). The mean FW fraction was significantly larger in tracts intersecting edema (p = 0.0271). Compared to the UKFt+rFA method, there was a significant increase of the volume of the AF tract that intersected the edema using the UKFt+FW method, while the whole AF volumes were similar. Expert judgment results, based on the five patients with the smallest AF volumes, indicated that the expert readers generally preferred the AF tract obtained by using the FW model, according to their anatomical knowledge and considering the potential influence of the final results on the surgical route. CONCLUSION: Our results indicate that incorporating biophysical models of edema can increase the sensitivity of tractography in regions of peritumoral edema, allowing better tract visualization in patients with high grade gliomas and metastases.
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Tractography results can be sensitive to parameter choices within a given algorithm, such as seeding and stopping thresholds.
“On the other hand, tractography results can also be sensitive to the choice of parameters (such as seeding and stopping thresholds) within a certain algorithm (Chamberland et al., 2014; Côté et al., 2013; Gong et al., 2018; Moldrich et al., 2010; Xie et al., 2020).”
From Quantitative mapping of the brain’s structural connectivity using diffusion MRI tractography: A review (2022) · cites this paper as Gong et al., 2018
The diffusion or fiber model can be simultaneously estimated when performing tractography so that microstructural measures are directly computed at points along each streamline.
“Instead of using a pre-calculated microstructure image, the diffusion or fiber model can be simultaneously estimated when performing tractography so that the microstructural measures are directly computed at points along each streamline (Girard et al., 2017; Gong et al., 2018; Malcolm et al., 2010; Olszewski et al., 2017; Reddy and Rathi, 2016).”
From Quantitative mapping of the brain’s structural connectivity using diffusion MRI tractography: A review (2022) · cites this paper as Gong et al., 2018
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White-matter free-water diffusion MRI in schizophrenia: A systematic review and meta-analysis
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Self-citationClinical applications of magnetic resonance imaging based functional and structural connectivity
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Self-citationTractography in Neurosurgery: A Systematic Review of Current Applications
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Self-citationCreation of a novel trigeminal tractography atlas for automated trigeminal nerve identification
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Self-citationGeneralized Richardson-Lucy (GRL) for analyzing multi-shell diffusion MRI data
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Enhanced Fiber Tractography Using Edema Correction: Application and Evaluation in High-Grade Gliomas
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Exploring Peritumoral Neural Tracts by Using Neurite Orientation Dispersion and Density Imaging
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Self-citationEffects of Multi-Shell Free Water Correction on Glioma Characterization
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Self-citationA unified global tractography framework for automatic visual pathway reconstruction
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- Authors
- Gong, S., Zhang, F., Norton, I., Essayed, W. I., Unadkat, P., Rigolo, L., Pasternak, O., Rathi, Y., Hou, L., Golby, A. J., & O’Donnell, L. J.
- Affiliations
- Brigham and Women's Hospital (US)
- Shanghai Changzheng Hospital (CN)
- Corresponding author
- Gong, Shun
- Zhang, Fan
- Norton, Isaiah
- Essayed, Walid I.
- Unadkat, Prashin
- Rigolo, Laura
- Pasternak, Ofer
- Hou, Lijun
- Golby, Alexandra J.
- O’Donnell, Lauren J.
- ORCID
- Venue
- PLOS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2018-05-10
- Volume
- 13
- Issue
- 5
- Pages
- e0197056
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC5944935
- OpenAlex
- W2801639927
- Cited by
- 51
- References
- 78
- Citations by year
- 2026: 6 · 2025: 6 · 2024: 4 · 2023: 3 · 2022: 8 · 2021: 10 · 2020: 11 · 2019: 1 · 2018: 2
- FWCI
- 4.15
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- National Institutes of Health (U01 CA199459, R03 NS088301, P41 EB015898, R01 MH074794, P41 EB015902, R25 CA089017, R01 MH097979, R21 CA198740, U01 NS083223; R01 MH108574)
- China Scholarship Council (201503170356)
- National Nature Science Foundation of China (81371382)
- Shanghai Outstanding Academic Leader Fund (XBR2013075)
- National "12th Five-Year" key issues (BWS12J025)
- Topics
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Physical Sciences › Computer Science › Computer Vision and Pattern Recognition › Medical Image Segmentation Techniques
- Keywords
- arcuate fasciculus, peritumoral edema, partial volume effect, white matter fiber tracking, high-grade glioma, brain metastases, neurosurgical planning, diffusion MRI
- MeSH terms
- Adult, Aged, Brain Edema, Brain Neoplasms, Female, Glioma, Humans, Male, Middle Aged, Models, Neurological, Retrospective Studies, Diffusion Tensor Imaging
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