Prognostic value of tumor necrosis based on the evaluation of frequency in invasive breast cancer

Abstract Background Tumor necrosis (TN) was associated with poor prognosis. However, the traditional classification of TN ignored spatial intratumor heterogeneity, which may be associated with important prognosis. The purpose of this study was to propose a new method to reveal the hidden prognostic...

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Main Authors: Jianhua Chen, Zhijun Li, Zhonghua Han, Deyong Kang, Jianli Ma, Yu Yi, Fangmeng Fu, Wenhui Guo, Liqin Zheng, Gangqin Xi, Jiajia He, Lida Qiu, Lianhuang Li, Qingyuan Zhang, Chuan Wang, Jianxin Chen
Format: Article
Language:English
Published: BMC 2023-06-01
Series:BMC Cancer
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Online Access:https://doi.org/10.1186/s12885-023-10943-x
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author Jianhua Chen
Zhijun Li
Zhonghua Han
Deyong Kang
Jianli Ma
Yu Yi
Fangmeng Fu
Wenhui Guo
Liqin Zheng
Gangqin Xi
Jiajia He
Lida Qiu
Lianhuang Li
Qingyuan Zhang
Chuan Wang
Jianxin Chen
author_facet Jianhua Chen
Zhijun Li
Zhonghua Han
Deyong Kang
Jianli Ma
Yu Yi
Fangmeng Fu
Wenhui Guo
Liqin Zheng
Gangqin Xi
Jiajia He
Lida Qiu
Lianhuang Li
Qingyuan Zhang
Chuan Wang
Jianxin Chen
author_sort Jianhua Chen
collection DOAJ
description Abstract Background Tumor necrosis (TN) was associated with poor prognosis. However, the traditional classification of TN ignored spatial intratumor heterogeneity, which may be associated with important prognosis. The purpose of this study was to propose a new method to reveal the hidden prognostic value of spatial heterogeneity of TN in invasive breast cancer (IBC). Methods Multiphoton microscopy (MPM) was used to obtain multiphoton images from 471 patients. According to the relative spatial positions of TN, tumor cells, collagen fibers and myoepithelium, four spatial heterogeneities of TN (TN1-4) were defined. Based on the frequency of individual TN, TN-score was obtained to investigate the prognostic value of TN. Results Patients with high-risk TN had worse 5-year disease-free survival (DFS) than patients with no necrosis (32.5% vs. 64.7%; P < 0.0001 in training set; 45.8% vs. 70.8%; P = 0.017 in validation set), while patients with low-risk TN had a 5-year DFS comparable to patients with no necrosis (60.0% vs. 64.7%; P = 0.497 in training set; 59.8% vs. 70.8%; P = 0.121 in validation set). Furthermore, high-risk TN “up-staged” the patients with IBC. Patients with high-risk TN and stage I tumors had a 5-year DFS comparable to patients with stage II tumors (55.6% vs. 62.0%; P = 0.565 in training set; 62.5% vs. 66.3%; P = 0.856 in validation set), as well as patients with high-risk TN and stage II tumors had a 5-year DFS comparable to patients with stage III tumors (33.3% vs. 24.6%; P = 0.271 in training set; 44.4% vs. 39.3%; P = 0.519 in validation set). Conclusions TN-score was an independent prognostic factor for 5-year DFS. Only high-risk TN was associated with poor prognosis. High-risk TN “up-staged” the patients with IBC. Incorporating TN-score into staging category could improve its performance to stratify patients.
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spelling doaj.art-ebf15282658341ff8a273b4a5a7180942023-06-11T11:16:42ZengBMCBMC Cancer1471-24072023-06-0123111410.1186/s12885-023-10943-xPrognostic value of tumor necrosis based on the evaluation of frequency in invasive breast cancerJianhua Chen0Zhijun Li1Zhonghua Han2Deyong Kang3Jianli Ma4Yu Yi5Fangmeng Fu6Wenhui Guo7Liqin Zheng8Gangqin Xi9Jiajia He10Lida Qiu11Lianhuang Li12Qingyuan Zhang13Chuan Wang14Jianxin Chen15Key Laboratory of OptoElectronic Science and Technology for Medicine of Ministry of Education, Fujian Provincial Key Laboratory of Photonics Technology, College of Photonic and Electronic Engineering, Fujian Normal UniversityKey Laboratory of OptoElectronic Science and Technology for Medicine of Ministry of Education, Fujian Provincial Key Laboratory of Photonics Technology, College of Photonic and Electronic Engineering, Fujian Normal UniversityDepartment of Breast Surgery, Fujian Medical University Union HospitalDepartment of Pathology, Fujian Medical University Union HospitalDepartment of Radiation Oncology, Harbin Medical University Cancer HospitalKey Laboratory of OptoElectronic Science and Technology for Medicine of Ministry of Education, Fujian Provincial Key Laboratory of Photonics Technology, College of Photonic and Electronic Engineering, Fujian Normal UniversityDepartment of Breast Surgery, Fujian Medical University Union HospitalDepartment of Breast Surgery, Fujian Medical University Union HospitalKey Laboratory of OptoElectronic Science and Technology for Medicine of Ministry of Education, Fujian Provincial Key Laboratory of Photonics Technology, College of Photonic and Electronic Engineering, Fujian Normal UniversityKey Laboratory of OptoElectronic Science and Technology for Medicine of Ministry of Education, Fujian Provincial Key Laboratory of Photonics Technology, College of Photonic and Electronic Engineering, Fujian Normal UniversityKey Laboratory of OptoElectronic Science and Technology for Medicine of Ministry of Education, Fujian Provincial Key Laboratory of Photonics Technology, College of Photonic and Electronic Engineering, Fujian Normal UniversityKey Laboratory of OptoElectronic Science and Technology for Medicine of Ministry of Education, Fujian Provincial Key Laboratory of Photonics Technology, College of Photonic and Electronic Engineering, Fujian Normal UniversityKey Laboratory of OptoElectronic Science and Technology for Medicine of Ministry of Education, Fujian Provincial Key Laboratory of Photonics Technology, College of Photonic and Electronic Engineering, Fujian Normal UniversityDepartment of Medical Oncology, Harbin Medical University Cancer HospitalDepartment of Breast Surgery, Fujian Medical University Union HospitalKey Laboratory of OptoElectronic Science and Technology for Medicine of Ministry of Education, Fujian Provincial Key Laboratory of Photonics Technology, College of Photonic and Electronic Engineering, Fujian Normal UniversityAbstract Background Tumor necrosis (TN) was associated with poor prognosis. However, the traditional classification of TN ignored spatial intratumor heterogeneity, which may be associated with important prognosis. The purpose of this study was to propose a new method to reveal the hidden prognostic value of spatial heterogeneity of TN in invasive breast cancer (IBC). Methods Multiphoton microscopy (MPM) was used to obtain multiphoton images from 471 patients. According to the relative spatial positions of TN, tumor cells, collagen fibers and myoepithelium, four spatial heterogeneities of TN (TN1-4) were defined. Based on the frequency of individual TN, TN-score was obtained to investigate the prognostic value of TN. Results Patients with high-risk TN had worse 5-year disease-free survival (DFS) than patients with no necrosis (32.5% vs. 64.7%; P < 0.0001 in training set; 45.8% vs. 70.8%; P = 0.017 in validation set), while patients with low-risk TN had a 5-year DFS comparable to patients with no necrosis (60.0% vs. 64.7%; P = 0.497 in training set; 59.8% vs. 70.8%; P = 0.121 in validation set). Furthermore, high-risk TN “up-staged” the patients with IBC. Patients with high-risk TN and stage I tumors had a 5-year DFS comparable to patients with stage II tumors (55.6% vs. 62.0%; P = 0.565 in training set; 62.5% vs. 66.3%; P = 0.856 in validation set), as well as patients with high-risk TN and stage II tumors had a 5-year DFS comparable to patients with stage III tumors (33.3% vs. 24.6%; P = 0.271 in training set; 44.4% vs. 39.3%; P = 0.519 in validation set). Conclusions TN-score was an independent prognostic factor for 5-year DFS. Only high-risk TN was associated with poor prognosis. High-risk TN “up-staged” the patients with IBC. Incorporating TN-score into staging category could improve its performance to stratify patients.https://doi.org/10.1186/s12885-023-10943-xFrequencyInvasive breast cancerMultiphoton imagingTumor necrosisSpatial heterogeneityPrognosis
spellingShingle Jianhua Chen
Zhijun Li
Zhonghua Han
Deyong Kang
Jianli Ma
Yu Yi
Fangmeng Fu
Wenhui Guo
Liqin Zheng
Gangqin Xi
Jiajia He
Lida Qiu
Lianhuang Li
Qingyuan Zhang
Chuan Wang
Jianxin Chen
Prognostic value of tumor necrosis based on the evaluation of frequency in invasive breast cancer
BMC Cancer
Frequency
Invasive breast cancer
Multiphoton imaging
Tumor necrosis
Spatial heterogeneity
Prognosis
title Prognostic value of tumor necrosis based on the evaluation of frequency in invasive breast cancer
title_full Prognostic value of tumor necrosis based on the evaluation of frequency in invasive breast cancer
title_fullStr Prognostic value of tumor necrosis based on the evaluation of frequency in invasive breast cancer
title_full_unstemmed Prognostic value of tumor necrosis based on the evaluation of frequency in invasive breast cancer
title_short Prognostic value of tumor necrosis based on the evaluation of frequency in invasive breast cancer
title_sort prognostic value of tumor necrosis based on the evaluation of frequency in invasive breast cancer
topic Frequency
Invasive breast cancer
Multiphoton imaging
Tumor necrosis
Spatial heterogeneity
Prognosis
url https://doi.org/10.1186/s12885-023-10943-x
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