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Distinct tumor signatures using deep learning-based characterization of the peritumoral microenvironment in glioblastomas and brain metastases

Tumor types are classically distinguished based on biopsies of the tumor itself, as well as a radiological interpretation using diverse MRI modalities. In the current study, the overarching goal is to demonstrate that primary (glioblastomas) and secondary (brain metastases) malignancies can be diffe...

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Autores principales: Samani, Zahra Riahi, Parker, Drew, Wolf, Ronald, Hodges, Wes, Brem, Steven, Verma, Ragini
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8280204/
https://www.ncbi.nlm.nih.gov/pubmed/34262079
http://dx.doi.org/10.1038/s41598-021-93804-6
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author Samani, Zahra Riahi
Parker, Drew
Wolf, Ronald
Hodges, Wes
Brem, Steven
Verma, Ragini
author_facet Samani, Zahra Riahi
Parker, Drew
Wolf, Ronald
Hodges, Wes
Brem, Steven
Verma, Ragini
author_sort Samani, Zahra Riahi
collection PubMed
description Tumor types are classically distinguished based on biopsies of the tumor itself, as well as a radiological interpretation using diverse MRI modalities. In the current study, the overarching goal is to demonstrate that primary (glioblastomas) and secondary (brain metastases) malignancies can be differentiated based on the microstructure of the peritumoral region. This is achieved by exploiting the extracellular water differences between vasogenic edema and infiltrative tissue and training a convolutional neural network (CNN) on the Diffusion Tensor Imaging (DTI)-derived free water volume fraction. We obtained 85% accuracy in discriminating extracellular water differences between local patches in the peritumoral area of 66 glioblastomas and 40 metastatic patients in a cross-validation setting. On an independent test cohort consisting of 20 glioblastomas and 10 metastases, we got 93% accuracy in discriminating metastases from glioblastomas using majority voting on patches. This level of accuracy surpasses CNNs trained on other conventional DTI-based measures such as fractional anisotropy (FA) and mean diffusivity (MD), that have been used in other studies. Additionally, the CNN captures the peritumoral heterogeneity better than conventional texture features, including Gabor and radiomic features. Our results demonstrate that the extracellular water content of the peritumoral tissue, as captured by the free water volume fraction, is best able to characterize the differences between infiltrative and vasogenic peritumoral regions, paving the way for its use in classifying and benchmarking peritumoral tissue with varying degrees of infiltration.
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spelling pubmed-82802042021-07-15 Distinct tumor signatures using deep learning-based characterization of the peritumoral microenvironment in glioblastomas and brain metastases Samani, Zahra Riahi Parker, Drew Wolf, Ronald Hodges, Wes Brem, Steven Verma, Ragini Sci Rep Article Tumor types are classically distinguished based on biopsies of the tumor itself, as well as a radiological interpretation using diverse MRI modalities. In the current study, the overarching goal is to demonstrate that primary (glioblastomas) and secondary (brain metastases) malignancies can be differentiated based on the microstructure of the peritumoral region. This is achieved by exploiting the extracellular water differences between vasogenic edema and infiltrative tissue and training a convolutional neural network (CNN) on the Diffusion Tensor Imaging (DTI)-derived free water volume fraction. We obtained 85% accuracy in discriminating extracellular water differences between local patches in the peritumoral area of 66 glioblastomas and 40 metastatic patients in a cross-validation setting. On an independent test cohort consisting of 20 glioblastomas and 10 metastases, we got 93% accuracy in discriminating metastases from glioblastomas using majority voting on patches. This level of accuracy surpasses CNNs trained on other conventional DTI-based measures such as fractional anisotropy (FA) and mean diffusivity (MD), that have been used in other studies. Additionally, the CNN captures the peritumoral heterogeneity better than conventional texture features, including Gabor and radiomic features. Our results demonstrate that the extracellular water content of the peritumoral tissue, as captured by the free water volume fraction, is best able to characterize the differences between infiltrative and vasogenic peritumoral regions, paving the way for its use in classifying and benchmarking peritumoral tissue with varying degrees of infiltration. Nature Publishing Group UK 2021-07-14 /pmc/articles/PMC8280204/ /pubmed/34262079 http://dx.doi.org/10.1038/s41598-021-93804-6 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Samani, Zahra Riahi
Parker, Drew
Wolf, Ronald
Hodges, Wes
Brem, Steven
Verma, Ragini
Distinct tumor signatures using deep learning-based characterization of the peritumoral microenvironment in glioblastomas and brain metastases
title Distinct tumor signatures using deep learning-based characterization of the peritumoral microenvironment in glioblastomas and brain metastases
title_full Distinct tumor signatures using deep learning-based characterization of the peritumoral microenvironment in glioblastomas and brain metastases
title_fullStr Distinct tumor signatures using deep learning-based characterization of the peritumoral microenvironment in glioblastomas and brain metastases
title_full_unstemmed Distinct tumor signatures using deep learning-based characterization of the peritumoral microenvironment in glioblastomas and brain metastases
title_short Distinct tumor signatures using deep learning-based characterization of the peritumoral microenvironment in glioblastomas and brain metastases
title_sort distinct tumor signatures using deep learning-based characterization of the peritumoral microenvironment in glioblastomas and brain metastases
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8280204/
https://www.ncbi.nlm.nih.gov/pubmed/34262079
http://dx.doi.org/10.1038/s41598-021-93804-6
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