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Machine learning radiomics of magnetic resonance imaging predicts recurrence-free survival after surgery and correlation of LncRNAs in patients with breast cancer: a multicenter cohort study

BACKGROUND: Several studies have indicated that magnetic resonance imaging radiomics can predict survival in patients with breast cancer, but the potential biological underpinning remains indistinct. Herein, we aim to develop an interpretable deep-learning-based network for classifying recurrence ri...

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Autores principales: Yu, Yunfang, Ren, Wei, He, Zifan, Chen, Yongjian, Tan, Yujie, Mao, Luhui, Ouyang, Wenhao, Lu, Nian, Ouyang, Jie, Chen, Kai, Li, Chenchen, Zhang, Rong, Wu, Zhuo, Su, Fengxi, Wang, Zehua, Hu, Qiugen, Xie, Chuanmiao, Yao, Herui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10619251/
https://www.ncbi.nlm.nih.gov/pubmed/37915093
http://dx.doi.org/10.1186/s13058-023-01688-3
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author Yu, Yunfang
Ren, Wei
He, Zifan
Chen, Yongjian
Tan, Yujie
Mao, Luhui
Ouyang, Wenhao
Lu, Nian
Ouyang, Jie
Chen, Kai
Li, Chenchen
Zhang, Rong
Wu, Zhuo
Su, Fengxi
Wang, Zehua
Hu, Qiugen
Xie, Chuanmiao
Yao, Herui
author_facet Yu, Yunfang
Ren, Wei
He, Zifan
Chen, Yongjian
Tan, Yujie
Mao, Luhui
Ouyang, Wenhao
Lu, Nian
Ouyang, Jie
Chen, Kai
Li, Chenchen
Zhang, Rong
Wu, Zhuo
Su, Fengxi
Wang, Zehua
Hu, Qiugen
Xie, Chuanmiao
Yao, Herui
author_sort Yu, Yunfang
collection PubMed
description BACKGROUND: Several studies have indicated that magnetic resonance imaging radiomics can predict survival in patients with breast cancer, but the potential biological underpinning remains indistinct. Herein, we aim to develop an interpretable deep-learning-based network for classifying recurrence risk and revealing the potential biological mechanisms. METHODS: In this multicenter study, 1113 nonmetastatic invasive breast cancer patients were included, and were divided into the training cohort (n = 698), the validation cohort (n = 171), and the testing cohort (n = 244). The Radiomic DeepSurv Net (RDeepNet) model was constructed using the Cox proportional hazards deep neural network DeepSurv for predicting individual recurrence risk. RNA-sequencing was performed to explore the association between radiomics and tumor microenvironment. Correlation and variance analyses were conducted to examine changes of radiomics among patients with different therapeutic responses and after neoadjuvant chemotherapy. The association and quantitative relation of radiomics and epigenetic molecular characteristics were further analyzed to reveal the mechanisms of radiomics. RESULTS: The RDeepNet model showed a significant association with recurrence-free survival (RFS) (HR 0.03, 95% CI 0.02–0.06, P < 0.001) and achieved AUCs of 0.98, 0.94, and 0.92 for 1-, 2-, and 3-year RFS, respectively. In the validation and testing cohorts, the RDeepNet model could also clarify patients into high- and low-risk groups, and demonstrated AUCs of 0.91 and 0.94 for 3-year RFS, respectively. Radiomic features displayed differential expression between the two risk groups. Furthermore, the generalizability of RDeepNet model was confirmed across different molecular subtypes and patient populations with different therapy regimens (All P < 0.001). The study also identified variations in radiomic features among patients with diverse therapeutic responses and after neoadjuvant chemotherapy. Importantly, a significant correlation between radiomics and long non-coding RNAs (lncRNAs) was discovered. A key lncRNA was found to be noninvasively quantified by a deep learning-based radiomics prediction model with AUCs of 0.79 in the training cohort and 0.77 in the testing cohort. CONCLUSIONS: This study demonstrates that machine learning radiomics of MRI can effectively predict RFS after surgery in patients with breast cancer, and highlights the feasibility of non-invasive quantification of lncRNAs using radiomics, which indicates the potential of radiomics in guiding treatment decisions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13058-023-01688-3.
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spelling pubmed-106192512023-11-02 Machine learning radiomics of magnetic resonance imaging predicts recurrence-free survival after surgery and correlation of LncRNAs in patients with breast cancer: a multicenter cohort study Yu, Yunfang Ren, Wei He, Zifan Chen, Yongjian Tan, Yujie Mao, Luhui Ouyang, Wenhao Lu, Nian Ouyang, Jie Chen, Kai Li, Chenchen Zhang, Rong Wu, Zhuo Su, Fengxi Wang, Zehua Hu, Qiugen Xie, Chuanmiao Yao, Herui Breast Cancer Res Research BACKGROUND: Several studies have indicated that magnetic resonance imaging radiomics can predict survival in patients with breast cancer, but the potential biological underpinning remains indistinct. Herein, we aim to develop an interpretable deep-learning-based network for classifying recurrence risk and revealing the potential biological mechanisms. METHODS: In this multicenter study, 1113 nonmetastatic invasive breast cancer patients were included, and were divided into the training cohort (n = 698), the validation cohort (n = 171), and the testing cohort (n = 244). The Radiomic DeepSurv Net (RDeepNet) model was constructed using the Cox proportional hazards deep neural network DeepSurv for predicting individual recurrence risk. RNA-sequencing was performed to explore the association between radiomics and tumor microenvironment. Correlation and variance analyses were conducted to examine changes of radiomics among patients with different therapeutic responses and after neoadjuvant chemotherapy. The association and quantitative relation of radiomics and epigenetic molecular characteristics were further analyzed to reveal the mechanisms of radiomics. RESULTS: The RDeepNet model showed a significant association with recurrence-free survival (RFS) (HR 0.03, 95% CI 0.02–0.06, P < 0.001) and achieved AUCs of 0.98, 0.94, and 0.92 for 1-, 2-, and 3-year RFS, respectively. In the validation and testing cohorts, the RDeepNet model could also clarify patients into high- and low-risk groups, and demonstrated AUCs of 0.91 and 0.94 for 3-year RFS, respectively. Radiomic features displayed differential expression between the two risk groups. Furthermore, the generalizability of RDeepNet model was confirmed across different molecular subtypes and patient populations with different therapy regimens (All P < 0.001). The study also identified variations in radiomic features among patients with diverse therapeutic responses and after neoadjuvant chemotherapy. Importantly, a significant correlation between radiomics and long non-coding RNAs (lncRNAs) was discovered. A key lncRNA was found to be noninvasively quantified by a deep learning-based radiomics prediction model with AUCs of 0.79 in the training cohort and 0.77 in the testing cohort. CONCLUSIONS: This study demonstrates that machine learning radiomics of MRI can effectively predict RFS after surgery in patients with breast cancer, and highlights the feasibility of non-invasive quantification of lncRNAs using radiomics, which indicates the potential of radiomics in guiding treatment decisions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13058-023-01688-3. BioMed Central 2023-11-01 2023 /pmc/articles/PMC10619251/ /pubmed/37915093 http://dx.doi.org/10.1186/s13058-023-01688-3 Text en © The Author(s) 2023 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/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Yu, Yunfang
Ren, Wei
He, Zifan
Chen, Yongjian
Tan, Yujie
Mao, Luhui
Ouyang, Wenhao
Lu, Nian
Ouyang, Jie
Chen, Kai
Li, Chenchen
Zhang, Rong
Wu, Zhuo
Su, Fengxi
Wang, Zehua
Hu, Qiugen
Xie, Chuanmiao
Yao, Herui
Machine learning radiomics of magnetic resonance imaging predicts recurrence-free survival after surgery and correlation of LncRNAs in patients with breast cancer: a multicenter cohort study
title Machine learning radiomics of magnetic resonance imaging predicts recurrence-free survival after surgery and correlation of LncRNAs in patients with breast cancer: a multicenter cohort study
title_full Machine learning radiomics of magnetic resonance imaging predicts recurrence-free survival after surgery and correlation of LncRNAs in patients with breast cancer: a multicenter cohort study
title_fullStr Machine learning radiomics of magnetic resonance imaging predicts recurrence-free survival after surgery and correlation of LncRNAs in patients with breast cancer: a multicenter cohort study
title_full_unstemmed Machine learning radiomics of magnetic resonance imaging predicts recurrence-free survival after surgery and correlation of LncRNAs in patients with breast cancer: a multicenter cohort study
title_short Machine learning radiomics of magnetic resonance imaging predicts recurrence-free survival after surgery and correlation of LncRNAs in patients with breast cancer: a multicenter cohort study
title_sort machine learning radiomics of magnetic resonance imaging predicts recurrence-free survival after surgery and correlation of lncrnas in patients with breast cancer: a multicenter cohort study
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10619251/
https://www.ncbi.nlm.nih.gov/pubmed/37915093
http://dx.doi.org/10.1186/s13058-023-01688-3
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