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European Radiology
Published in: European Radiology 3/2024

02-09-2023 | Breast Cancer | Breast

MRI-based radiomic models to predict surgical margin status and infer tumor immune microenvironment in breast cancer patients with breast-conserving surgery: a multicenter validation study

Authors: Jiafan Ma, Kai Chen, Shunrong Li, Liling Zhu, Yunfang Yu, Jingwu Li, Jie Ma, Jie Ouyang, Zhuo Wu, Yujie Tan, Zifan He, Haiqing Liu, Zhilong Pan, Haojiang Li, Qiang Liu, Erwei Song

Published in: European Radiology | Issue 3/2024

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Abstract

Objectives

Accurate preoperative estimation of the risk of breast-conserving surgery (BCS) resection margin positivity would be beneficial to surgical planning. In this multicenter validation study, we developed an MRI-based radiomic model to predict the surgical margin status.

Methods

We retrospectively collected preoperative breast MRI of patients undergoing BCS from three hospitals (SYMH, n = 296; SYSUCC, n = 131; TSPH, n = 143). Radiomic-based model for risk prediction of the margin positivity was trained on the SYMH patients (7:3 ratio split for the training and testing cohorts), and externally validated in the SYSUCC and TSPH cohorts. The model was able to stratify patients into different subgroups with varied risk of margin positivity. Moreover, we used the immune-radiomic models and epithelial-mesenchymal transition (EMT) signature to infer the distribution patterns of immune cells and tumor cell EMT status under different marginal status.

Results

The AUCs of the radiomic-based model were 0.78 (0.66–0.90), 0.88 (0.79–0.96), and 0.76 (0.68–0.84) in the testing cohort and two external validation cohorts, respectively. The actual margin positivity rates ranged between 0–10% and 27.3–87.2% in low-risk and high-risk subgroups, respectively. Positive surgical margin was associated with higher levels of EMT and B cell infiltration in the tumor area, as well as the enrichment of B cells, immature dendritic cells, and neutrophil infiltration in the peritumoral area.

Conclusions

This MRI-based predictive model can be used as a reliable tool to predict the risk of margin positivity of BCS. Tumor immune-microenvironment alteration was associated with surgical margin status.

Clinical relevance statement

This study can assist the pre-operative planning of BCS. Further research on the tumor immune microenvironment of different resection margin states is expected to develop new margin evaluation indicators and decipher the internal mechanism.

Key Points

• The MRI-based radiomic prediction model (CSS model) incorporating features extracted from multiple sequences and segments could estimate the margin positivity risk of breast-conserving surgery.
• The radiomic score of the CSS model allows risk stratification of patients undergoing breast-conserving surgery, which could assist in surgical planning.
• With the help of MRI-based radiomics to estimate the components of the immune microenvironment, for the first time, it is found that the margin status of breast-conserving surgery is associated with the infiltration of immune cells in the microenvironment and the EMT status of breast tumor cells.
Appendix
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Metadata
Title
MRI-based radiomic models to predict surgical margin status and infer tumor immune microenvironment in breast cancer patients with breast-conserving surgery: a multicenter validation study
Authors
Jiafan Ma
Kai Chen
Shunrong Li
Liling Zhu
Yunfang Yu
Jingwu Li
Jie Ma
Jie Ouyang
Zhuo Wu
Yujie Tan
Zifan He
Haiqing Liu
Zhilong Pan
Haojiang Li
Qiang Liu
Erwei Song
Publication date
02-09-2023
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 3/2024
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-023-10144-x

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