Immune cells within tertiary lymphoid structures are associated with progression‐free survival in patients with locoregional recurrent breast cancer

Abstract Introduction Locoregional recurrent breast cancers have a poor prognosis. Little is known about the prognostic impact of immune microenvironment, and tertiary lymphoid structures (TLSs) in particular have not been reported. Thus, we aimed to characterize the immune microenvironment in locor...

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Main Authors: Jinyuan Gu, Jiaming Wang, Yue Sun, Xinrui Mao, Chao Qian, Xinyu Tang, Ji Wang, Hui Xie, Lijun Ling, Yi Zhao, Xiaoan Liu, Kai Zhang, Hong Pan, Shui Wang, Cong Wang, Wenbin Zhou
Format: Article
Language:English
Published: Wiley 2024-01-01
Series:Cancer Medicine
Subjects:
Online Access:https://doi.org/10.1002/cam4.6864
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author Jinyuan Gu
Jiaming Wang
Yue Sun
Xinrui Mao
Chao Qian
Xinyu Tang
Ji Wang
Hui Xie
Lijun Ling
Yi Zhao
Xiaoan Liu
Kai Zhang
Hong Pan
Shui Wang
Cong Wang
Wenbin Zhou
author_facet Jinyuan Gu
Jiaming Wang
Yue Sun
Xinrui Mao
Chao Qian
Xinyu Tang
Ji Wang
Hui Xie
Lijun Ling
Yi Zhao
Xiaoan Liu
Kai Zhang
Hong Pan
Shui Wang
Cong Wang
Wenbin Zhou
author_sort Jinyuan Gu
collection DOAJ
description Abstract Introduction Locoregional recurrent breast cancers have a poor prognosis. Little is known about the prognostic impact of immune microenvironment, and tertiary lymphoid structures (TLSs) in particular have not been reported. Thus, we aimed to characterize the immune microenvironment in locoregional recurrent breast tumors and to investigate its relationship with prognosis. Methods We retrospectively included 112 patients with locoregional recurrent breast cancer, and hematoxylin–eosin staining and immunohistochemical staining (CD3, CD4, CD8, CD19, CD38, and CD68) were performed on locoregional recurrent tumor samples. The association of immune cells and TLSs with progression‐free survival (PFS) were analyzed by survival analysis. Results We found more immune cells in the peritumor than stroma. After grouping according to estrogen receptor (ER) status, a low level of peritumoral CD3+ cells in ER+ subgroup (p = 0.015) and a low level of stromal CD68+ cells in ER− subgroup (p = 0.047) were both associated with longer PFS. TLSs were present in 68% of recurrent tumors, and CD68+ cells within TLSs were significantly associated with PFS as an independent prognostic factor (p = 0.035). TLSs and immune cells (CD3, CD38, and CD68) within TLSs were associated with longer PFS in ER− recurrent tumors (p = 0.044, p = 0.012, p = 0.050, p < 0.001, respectively), whereas CD38+ cells within TLSs were associated with shorter PFS in ER+ recurrent tumors (p = 0.037). Conclusion Our study proposes potential predictors for the clinical prognosis of patients with locoregional recurrent breast cancer, emphasizing the prognostic value of immune cells within TLSs, especially CD68+ cells.
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spelling doaj.art-674858e58ce5490e8640aebfb1e403982024-03-05T06:22:52ZengWileyCancer Medicine2045-76342024-01-01131n/an/a10.1002/cam4.6864Immune cells within tertiary lymphoid structures are associated with progression‐free survival in patients with locoregional recurrent breast cancerJinyuan Gu0Jiaming Wang1Yue Sun2Xinrui Mao3Chao Qian4Xinyu Tang5Ji Wang6Hui Xie7Lijun Ling8Yi Zhao9Xiaoan Liu10Kai Zhang11Hong Pan12Shui Wang13Cong Wang14Wenbin Zhou15Department of Breast Surgery The First Affiliated Hospital with Nanjing Medical University Nanjing ChinaDepartment of Breast Surgery The First Affiliated Hospital with Nanjing Medical University Nanjing ChinaDepartment of Oncology The First Affiliated Hospital with Nanjing Medical University Nanjing ChinaDepartment of Breast Surgery The First Affiliated Hospital with Nanjing Medical University Nanjing ChinaDepartment of General Surgery Sir Run Run Hospital Nanjing Medical University Nanjing ChinaDepartment of Breast Surgery The First Affiliated Hospital with Nanjing Medical University Nanjing ChinaDepartment of Breast Surgery The First Affiliated Hospital with Nanjing Medical University Nanjing ChinaDepartment of Breast Surgery The First Affiliated Hospital with Nanjing Medical University Nanjing ChinaDepartment of Breast Surgery The First Affiliated Hospital with Nanjing Medical University Nanjing ChinaDepartment of Breast Surgery The First Affiliated Hospital with Nanjing Medical University Nanjing ChinaDepartment of Breast Surgery The First Affiliated Hospital with Nanjing Medical University Nanjing ChinaPancreas Center & Department of General Surgery The First Affiliated Hospital with Nanjing Medical University Nanjing Jiangsu ChinaDepartment of Breast Surgery The First Affiliated Hospital with Nanjing Medical University Nanjing ChinaDepartment of Breast Surgery The First Affiliated Hospital with Nanjing Medical University Nanjing ChinaDepartment of Pathology The First Affiliated Hospital with Nanjing Medical University Nanjing ChinaDepartment of Breast Surgery The First Affiliated Hospital with Nanjing Medical University Nanjing ChinaAbstract Introduction Locoregional recurrent breast cancers have a poor prognosis. Little is known about the prognostic impact of immune microenvironment, and tertiary lymphoid structures (TLSs) in particular have not been reported. Thus, we aimed to characterize the immune microenvironment in locoregional recurrent breast tumors and to investigate its relationship with prognosis. Methods We retrospectively included 112 patients with locoregional recurrent breast cancer, and hematoxylin–eosin staining and immunohistochemical staining (CD3, CD4, CD8, CD19, CD38, and CD68) were performed on locoregional recurrent tumor samples. The association of immune cells and TLSs with progression‐free survival (PFS) were analyzed by survival analysis. Results We found more immune cells in the peritumor than stroma. After grouping according to estrogen receptor (ER) status, a low level of peritumoral CD3+ cells in ER+ subgroup (p = 0.015) and a low level of stromal CD68+ cells in ER− subgroup (p = 0.047) were both associated with longer PFS. TLSs were present in 68% of recurrent tumors, and CD68+ cells within TLSs were significantly associated with PFS as an independent prognostic factor (p = 0.035). TLSs and immune cells (CD3, CD38, and CD68) within TLSs were associated with longer PFS in ER− recurrent tumors (p = 0.044, p = 0.012, p = 0.050, p < 0.001, respectively), whereas CD38+ cells within TLSs were associated with shorter PFS in ER+ recurrent tumors (p = 0.037). Conclusion Our study proposes potential predictors for the clinical prognosis of patients with locoregional recurrent breast cancer, emphasizing the prognostic value of immune cells within TLSs, especially CD68+ cells.https://doi.org/10.1002/cam4.6864immune cellslocoregional recurrent breast cancerprognostic predictorprogression‐free survivaltertiary lymphoid structures
spellingShingle Jinyuan Gu
Jiaming Wang
Yue Sun
Xinrui Mao
Chao Qian
Xinyu Tang
Ji Wang
Hui Xie
Lijun Ling
Yi Zhao
Xiaoan Liu
Kai Zhang
Hong Pan
Shui Wang
Cong Wang
Wenbin Zhou
Immune cells within tertiary lymphoid structures are associated with progression‐free survival in patients with locoregional recurrent breast cancer
Cancer Medicine
immune cells
locoregional recurrent breast cancer
prognostic predictor
progression‐free survival
tertiary lymphoid structures
title Immune cells within tertiary lymphoid structures are associated with progression‐free survival in patients with locoregional recurrent breast cancer
title_full Immune cells within tertiary lymphoid structures are associated with progression‐free survival in patients with locoregional recurrent breast cancer
title_fullStr Immune cells within tertiary lymphoid structures are associated with progression‐free survival in patients with locoregional recurrent breast cancer
title_full_unstemmed Immune cells within tertiary lymphoid structures are associated with progression‐free survival in patients with locoregional recurrent breast cancer
title_short Immune cells within tertiary lymphoid structures are associated with progression‐free survival in patients with locoregional recurrent breast cancer
title_sort immune cells within tertiary lymphoid structures are associated with progression free survival in patients with locoregional recurrent breast cancer
topic immune cells
locoregional recurrent breast cancer
prognostic predictor
progression‐free survival
tertiary lymphoid structures
url https://doi.org/10.1002/cam4.6864
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