The efficacy of neoadjuvant immunotherapy and lymphocyte subset predictors in locally advanced esophageal squamous cell carcinoma: A retrospective study

Abstract Background Despite the recognized therapeutic potential of programmed cell death protein 1/programmed death‐ligand 1 (PD‐1/PD‐L1) inhibitors in advanced esophageal squamous cell carcinoma (ESCC), their role in neoadjuvant therapy and reliable efficacy biomarkers remain elusive. Materials an...

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Main Authors: Ruotong Wang, Shaodi Wen, Xiaoyue Du, Jingwei Xia, Bowen Hu, Yihan Zhang, Guoren Zhou, Feng Jiang, Xiaomin Lu, Miaolin Zhu, Xinyu Xu, Bo Shen
Format: Article
Language:English
Published: Wiley 2024-09-01
Series:Cancer Medicine
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Online Access:https://doi.org/10.1002/cam4.70228
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author Ruotong Wang
Shaodi Wen
Xiaoyue Du
Jingwei Xia
Bowen Hu
Yihan Zhang
Guoren Zhou
Feng Jiang
Xiaomin Lu
Miaolin Zhu
Xinyu Xu
Bo Shen
author_facet Ruotong Wang
Shaodi Wen
Xiaoyue Du
Jingwei Xia
Bowen Hu
Yihan Zhang
Guoren Zhou
Feng Jiang
Xiaomin Lu
Miaolin Zhu
Xinyu Xu
Bo Shen
author_sort Ruotong Wang
collection DOAJ
description Abstract Background Despite the recognized therapeutic potential of programmed cell death protein 1/programmed death‐ligand 1 (PD‐1/PD‐L1) inhibitors in advanced esophageal squamous cell carcinoma (ESCC), their role in neoadjuvant therapy and reliable efficacy biomarkers remain elusive. Materials and Methods We retrospectively analyzed locally advanced ESCC patients who underwent surgery following a 2‐cycle platinum and paclitaxel‐based treatment, with or without PD‐1 inhibitors (January 2020–March 2023). We assessed peripheral blood indexes and tertiary lymphoid structures (TLS) density to evaluate their impact on pathological response and prognosis, leading to a clinical prediction model for treatment efficacy and survival. Results Of the 157 patients recruited, 106 received immunochemotherapy (ICT) and 51 received chemotherapy (CT) alone. The ICT group demonstrated a superior pathological response rate (PRR) (47.2% vs. 29.4%, p = 0.034) with comparable adverse events and postoperative complications. The ICT group also showed a median disease‐free survival (DFS) of 39.8 months, unattained by the CT group. The 1‐year DFS and overall survival (OS) rates were 73% and 91% for the ICT group, and 68% and 81% for the CT group, respectively. We found higher baseline activated T cells, lower baseline Treg cells, and a decreased posttreatment total lymphocyte and CD4+/CD8+ ratio predicted an enhanced PRR. Reduced posttreatment CD4+/CD8+ ratio and increased NK cells were associated with prolonged survival, while higher TLS density indicated poorer prognosis. Among ICT group, a lower posttreatment CD4+/CD8+ ratio indicated longer DFS and reduced posttreatment B cells indicated longer OS. A nomogram integrating these predictors was developed to forecast treatment efficacy and survival. Conclusion The combination of PD‐1 inhibitors and chemotherapy appears promising for locally advanced ESCC. Evaluating the differentiation status and dynamic changes of peripheral blood immune cells may provide valuable predictive insights into treatment efficacy and prognosis.
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spelling doaj-art-64bab336fbf5471fb8f1066ac0688b522025-02-07T09:08:08ZengWileyCancer Medicine2045-76342024-09-011317n/an/a10.1002/cam4.70228The efficacy of neoadjuvant immunotherapy and lymphocyte subset predictors in locally advanced esophageal squamous cell carcinoma: A retrospective studyRuotong Wang0Shaodi Wen1Xiaoyue Du2Jingwei Xia3Bowen Hu4Yihan Zhang5Guoren Zhou6Feng Jiang7Xiaomin Lu8Miaolin Zhu9Xinyu Xu10Bo Shen11Department of Oncology, The Affiliated Cancer Hospital of Nanjing Medical University, Jiangsu Cancer Hospital Jiangsu Institute of Cancer Research Nanjing ChinaDepartment of Oncology, The Affiliated Cancer Hospital of Nanjing Medical University, Jiangsu Cancer Hospital Jiangsu Institute of Cancer Research Nanjing ChinaDepartment of Oncology, The Affiliated Cancer Hospital of Nanjing Medical University, Jiangsu Cancer Hospital Jiangsu Institute of Cancer Research Nanjing ChinaDepartment of Oncology, The Affiliated Cancer Hospital of Nanjing Medical University, Jiangsu Cancer Hospital Jiangsu Institute of Cancer Research Nanjing ChinaDepartment of Oncology, The Affiliated Cancer Hospital of Nanjing Medical University, Jiangsu Cancer Hospital Jiangsu Institute of Cancer Research Nanjing ChinaDepartment of Oncology, The Affiliated Cancer Hospital of Nanjing Medical University, Jiangsu Cancer Hospital Jiangsu Institute of Cancer Research Nanjing ChinaDepartment of Oncology, The Affiliated Cancer Hospital of Nanjing Medical University, Jiangsu Cancer Hospital Jiangsu Institute of Cancer Research Nanjing ChinaDepartment of Thoracic Surgery, The Affiliated Cancer Hospital of Nanjing Medical University, Jiangsu Cancer Hospital Jiangsu Institute of Cancer Research Nanjing ChinaDepartment of Oncology Affiliated Haian Hospital of Nantong University Haian Nantong ChinaDepartment of Pathology, The Affiliated Cancer Hospital of Nanjing Medical University, Jiangsu Cancer Hospital Jiangsu Institute of Cancer Research Nanjing ChinaDepartment of Pathology, The Affiliated Cancer Hospital of Nanjing Medical University, Jiangsu Cancer Hospital Jiangsu Institute of Cancer Research Nanjing ChinaDepartment of Oncology, The Affiliated Cancer Hospital of Nanjing Medical University, Jiangsu Cancer Hospital Jiangsu Institute of Cancer Research Nanjing ChinaAbstract Background Despite the recognized therapeutic potential of programmed cell death protein 1/programmed death‐ligand 1 (PD‐1/PD‐L1) inhibitors in advanced esophageal squamous cell carcinoma (ESCC), their role in neoadjuvant therapy and reliable efficacy biomarkers remain elusive. Materials and Methods We retrospectively analyzed locally advanced ESCC patients who underwent surgery following a 2‐cycle platinum and paclitaxel‐based treatment, with or without PD‐1 inhibitors (January 2020–March 2023). We assessed peripheral blood indexes and tertiary lymphoid structures (TLS) density to evaluate their impact on pathological response and prognosis, leading to a clinical prediction model for treatment efficacy and survival. Results Of the 157 patients recruited, 106 received immunochemotherapy (ICT) and 51 received chemotherapy (CT) alone. The ICT group demonstrated a superior pathological response rate (PRR) (47.2% vs. 29.4%, p = 0.034) with comparable adverse events and postoperative complications. The ICT group also showed a median disease‐free survival (DFS) of 39.8 months, unattained by the CT group. The 1‐year DFS and overall survival (OS) rates were 73% and 91% for the ICT group, and 68% and 81% for the CT group, respectively. We found higher baseline activated T cells, lower baseline Treg cells, and a decreased posttreatment total lymphocyte and CD4+/CD8+ ratio predicted an enhanced PRR. Reduced posttreatment CD4+/CD8+ ratio and increased NK cells were associated with prolonged survival, while higher TLS density indicated poorer prognosis. Among ICT group, a lower posttreatment CD4+/CD8+ ratio indicated longer DFS and reduced posttreatment B cells indicated longer OS. A nomogram integrating these predictors was developed to forecast treatment efficacy and survival. Conclusion The combination of PD‐1 inhibitors and chemotherapy appears promising for locally advanced ESCC. Evaluating the differentiation status and dynamic changes of peripheral blood immune cells may provide valuable predictive insights into treatment efficacy and prognosis.https://doi.org/10.1002/cam4.70228biomarkersesophageal squamous cellimmunologyneoadjuvant chemotherapynomogramprognostic factor
spellingShingle Ruotong Wang
Shaodi Wen
Xiaoyue Du
Jingwei Xia
Bowen Hu
Yihan Zhang
Guoren Zhou
Feng Jiang
Xiaomin Lu
Miaolin Zhu
Xinyu Xu
Bo Shen
The efficacy of neoadjuvant immunotherapy and lymphocyte subset predictors in locally advanced esophageal squamous cell carcinoma: A retrospective study
Cancer Medicine
biomarkers
esophageal squamous cell
immunology
neoadjuvant chemotherapy
nomogram
prognostic factor
title The efficacy of neoadjuvant immunotherapy and lymphocyte subset predictors in locally advanced esophageal squamous cell carcinoma: A retrospective study
title_full The efficacy of neoadjuvant immunotherapy and lymphocyte subset predictors in locally advanced esophageal squamous cell carcinoma: A retrospective study
title_fullStr The efficacy of neoadjuvant immunotherapy and lymphocyte subset predictors in locally advanced esophageal squamous cell carcinoma: A retrospective study
title_full_unstemmed The efficacy of neoadjuvant immunotherapy and lymphocyte subset predictors in locally advanced esophageal squamous cell carcinoma: A retrospective study
title_short The efficacy of neoadjuvant immunotherapy and lymphocyte subset predictors in locally advanced esophageal squamous cell carcinoma: A retrospective study
title_sort efficacy of neoadjuvant immunotherapy and lymphocyte subset predictors in locally advanced esophageal squamous cell carcinoma a retrospective study
topic biomarkers
esophageal squamous cell
immunology
neoadjuvant chemotherapy
nomogram
prognostic factor
url https://doi.org/10.1002/cam4.70228
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