Copyright
©The Author(s) 2025. Published by Baishideng Publishing Group Inc. All rights reserved.
Beyond the tumor region: Peritumoral radiomics enhances prognostic accuracy in locally advanced rectal cancer
Zhi-Ying Liang, Mao-Li Yu, Hui Yang, Hao-Jiang Li, Hui Xie, Chun-Yan Cui, Wei-Jing Zhang, Chao Luo, Pei-Qiang Cai, Xiao-Feng Lin, Kun-Feng Liu, Lang Xiong, Li-Zhi Liu, Bi-Yun Chen
Zhi-Ying Liang, Hui Yang, Hao-Jiang Li, Hui Xie, Chun-Yan Cui, Wei-Jing Zhang, Chao Luo, Pei-Qiang Cai, Xiao-Feng Lin, Kun-Feng Liu, Li-Zhi Liu, Bi-Yun Chen, Department of Radiology, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center, Guangzhou 510060, Guangdong Province, China
Mao-Li Yu, Department of Radiology, West China Hospital, Sichuan University, Chengdu 610041, Sichuan Province, China
Mao-Li Yu, West China School of Medicine, Sichuan University, Chengdu 610041, Sichuan Province, China
Lang Xiong, Department of Medical Imaging, First Affiliated Hospital of Gannan Medical University, Ganzhou 341000, Jiangxi Province, China
Co-first authors: Zhi-Ying Liang and Mao-Li Yu.
Co-corresponding authors: Li-Zhi Liu and Bi-Yun Chen.
Author contributions: Chen BY, Li HJ and Liang ZY contributed to conceptualization; Li HJ, Xie H contributed to methodology; Yang H, Yu ML, Xie H, Cui CY, Zhang WJ, Luo C, Cai PQ, Lin XF, Liu KF, Xiong L and Chen BY contributed to data curation and investigation; Li HJ, Liang ZY contributed to formal analysis and software; Chen BY, Liang ZY contributed to writing original draft preparation; Liu LZ contributed to resources and supervision; All authors contributed to writing, review, editing, critically reviewed and provided final approval of the manuscript, were responsible for the decision to submit the manuscript for publication.
Institutional review board statement: This investigation was approved by the Institutional Ethics Committee of the Sun Yat-sen University Cancer Center, approval No. B2021-157-Y03.
Informed consent statement: The requirement for informed consent was waived due to the study’s retrospective nature.
Conflict-of-interest statement: The authors declare that they have no conflict of interest.
Data sharing statement: The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Open Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See:
https://creativecommons.org/Licenses/by-nc/4.0/ Corresponding author: Bi-Yun Chen, PhD, Doctor, Department of Radiology, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center, No. 651 Dongfeng Dong Road, Guangzhou 510060, Guangdong Province, China.
chenby2@sysucc.org.cn
Received: July 12, 2024
Revised: October 9, 2024
Accepted: November 5, 2024
Published online: February 28, 2025
Processing time: 195 Days and 0.3 Hours
BACKGROUND
The peritumoral region possesses attributes that promote cancer growth and progression. However, the potential prognostic biomarkers in this region remain relatively underexplored in radiomics.
AIM
To investigate the prognostic value and importance of peritumoral radiomics in locally advanced rectal cancer (LARC).
METHODS
This retrospective study included 409 patients with biopsy-confirmed LARC treated with neoadjuvant chemoradiotherapy and surgically. Patients were divided into training (n = 273) and validation (n = 136) sets. Based on intratumoral and peritumoral radiomic features extracted from pretreatment axial high-resolution small-field-of-view T2-weighted images, multivariate Cox models for progression-free survival (PFS) prediction were developed with or without clinicoradiological features and evaluated with Harrell’s concordance index (C-index), calibration curve, and decision curve analyses. Risk stratification, Kaplan-Meier analysis, and permutation feature importance analysis were performed.
RESULTS
The comprehensive integrated clinical-radiological-omics model (ModelICRO) integrating seven peritumoral, three intratumoral, and four clinicoradiological features achieved the highest C-indices (0.836 and 0.801 in the training and validation sets, respectively). This model showed robust calibration and better clinical net benefits, effectively distinguished high-risk from low-risk patients (PFS: 97.2% vs 67.6% and 95.4% vs 64.8% in the training and validation sets, respectively; both P < 0.001). Three most influential predictors in the comprehensive ModelICRO were, in order, a peritumoral, an intratumoral, and a clinicoradiological feature. Notably, the peritumoral model outperformed the intratumoral model (C-index: 0.754 vs 0.670; P = 0.015); peritumoral features significantly enhanced the performance of models based on clinicoradiological or intratumoral features or their combinations.
CONCLUSION
Peritumoral radiomics holds greater prognostic value than intratumoral radiomics for predicting PFS in LARC. The comprehensive model may serve as a reliable tool for better stratification and management postoperatively.
Core Tip: This study highlights the superior prognostic value of peritumoral radiomics over intratumoral radiomics in predicting progression-free survival in patients with locally advanced rectal cancer. By integrating peritumoral, intratumoral, and clinicopathological features, our comprehensive model achieved high predictive accuracy, significantly improving risk stratification for disease progression. Notably, peritumoral features emerged as the most influential predictors of progression-free survival among the features analyzed. These findings underscore the importance of focusing on peritumoral radiomic characteristics in prognostic assessments. Additionally, we developed a nomogram incorporating these features to facilitate personalized treatment strategies and clinical decision-making in locally advanced rectal cancer.
