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...
Main Authors: | , , , , , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Wiley
2024-01-01
|
Series: | Cancer Medicine |
Subjects: | |
Online Access: | https://doi.org/10.1002/cam4.6864 |
_version_ | 1827329608495661056 |
---|---|
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. |
first_indexed | 2024-03-07T15:43:36Z |
format | Article |
id | doaj.art-674858e58ce5490e8640aebfb1e40398 |
institution | Directory Open Access Journal |
issn | 2045-7634 |
language | English |
last_indexed | 2024-03-07T15:43:36Z |
publishDate | 2024-01-01 |
publisher | Wiley |
record_format | Article |
series | Cancer Medicine |
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 |
work_keys_str_mv | AT jinyuangu immunecellswithintertiarylymphoidstructuresareassociatedwithprogressionfreesurvivalinpatientswithlocoregionalrecurrentbreastcancer AT jiamingwang immunecellswithintertiarylymphoidstructuresareassociatedwithprogressionfreesurvivalinpatientswithlocoregionalrecurrentbreastcancer AT yuesun immunecellswithintertiarylymphoidstructuresareassociatedwithprogressionfreesurvivalinpatientswithlocoregionalrecurrentbreastcancer AT xinruimao immunecellswithintertiarylymphoidstructuresareassociatedwithprogressionfreesurvivalinpatientswithlocoregionalrecurrentbreastcancer AT chaoqian immunecellswithintertiarylymphoidstructuresareassociatedwithprogressionfreesurvivalinpatientswithlocoregionalrecurrentbreastcancer AT xinyutang immunecellswithintertiarylymphoidstructuresareassociatedwithprogressionfreesurvivalinpatientswithlocoregionalrecurrentbreastcancer AT jiwang immunecellswithintertiarylymphoidstructuresareassociatedwithprogressionfreesurvivalinpatientswithlocoregionalrecurrentbreastcancer AT huixie immunecellswithintertiarylymphoidstructuresareassociatedwithprogressionfreesurvivalinpatientswithlocoregionalrecurrentbreastcancer AT lijunling immunecellswithintertiarylymphoidstructuresareassociatedwithprogressionfreesurvivalinpatientswithlocoregionalrecurrentbreastcancer AT yizhao immunecellswithintertiarylymphoidstructuresareassociatedwithprogressionfreesurvivalinpatientswithlocoregionalrecurrentbreastcancer AT xiaoanliu immunecellswithintertiarylymphoidstructuresareassociatedwithprogressionfreesurvivalinpatientswithlocoregionalrecurrentbreastcancer AT kaizhang immunecellswithintertiarylymphoidstructuresareassociatedwithprogressionfreesurvivalinpatientswithlocoregionalrecurrentbreastcancer AT hongpan immunecellswithintertiarylymphoidstructuresareassociatedwithprogressionfreesurvivalinpatientswithlocoregionalrecurrentbreastcancer AT shuiwang immunecellswithintertiarylymphoidstructuresareassociatedwithprogressionfreesurvivalinpatientswithlocoregionalrecurrentbreastcancer AT congwang immunecellswithintertiarylymphoidstructuresareassociatedwithprogressionfreesurvivalinpatientswithlocoregionalrecurrentbreastcancer AT wenbinzhou immunecellswithintertiarylymphoidstructuresareassociatedwithprogressionfreesurvivalinpatientswithlocoregionalrecurrentbreastcancer |