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Analysis of the Clinicopathological Characteristics, Prognosis, and Lymphocyte Infiltration of Esophageal Neuroendocrine Neoplasms: A Surgery-Based Cohort and Propensity-Score Matching Study

SIMPLE SUMMARY: Esophageal neuroendocrine neoplasms (E-NENs) are a rare malignancy in esophageal carcinoma; their clinical and oncologic characteristics are poorly reported. Additionally, the effect of surgery on E-NENs remains unclear and controversial. In this study, we retrospectively analyzed th...

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Autores principales: Zhang, Long, Yu, Boyao, Liu, Zhichao, Wei, Jinzhi, Pan, Jie, Jiang, Chao, Li, Zhigang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10046526/
https://www.ncbi.nlm.nih.gov/pubmed/36980618
http://dx.doi.org/10.3390/cancers15061732
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author Zhang, Long
Yu, Boyao
Liu, Zhichao
Wei, Jinzhi
Pan, Jie
Jiang, Chao
Li, Zhigang
author_facet Zhang, Long
Yu, Boyao
Liu, Zhichao
Wei, Jinzhi
Pan, Jie
Jiang, Chao
Li, Zhigang
author_sort Zhang, Long
collection PubMed
description SIMPLE SUMMARY: Esophageal neuroendocrine neoplasms (E-NENs) are a rare malignancy in esophageal carcinoma; their clinical and oncologic characteristics are poorly reported. Additionally, the effect of surgery on E-NENs remains unclear and controversial. In this study, we retrospectively analyzed the clinicopathological characteristics, prognosis, and immune cell infiltration in E-NENs and compared them with those of esophageal squamous cell carcinoma (ESCC) to determine whether surgery has the same therapeutic efficacy for E-NENs as for ESCC based on a cohort who received surgical treatment. According to our results, first, the target population for surgery may be limited to stage I E-NENs patients. Secondly, E-NENs and especially pure NENs were correlated with the cold tumor phenotype because of the less infiltration of immune cells compared with ESCC. The findings suggest that strategies for immune activation should be developed and applied when immunotherapy is considered for E-NENs in the future. ABSTRACT: Background: Esophageal neuroendocrine neoplasms (E-NENs) are a rare and poorly reported subtype of esophageal carcinoma. We analyzed the differences in clinicopathological features, prognosis, and tumor-infiltrating lymphocytes (TILs) between E-NENs and esophageal squamous cell carcinoma (ESCC). Methods: A total of 3620 patients who underwent esophagectomy were enrolled retrospectively. The study cohort was divided into two groups (E-NENs and ESCC) through propensity-score matching, and the prognosis and TILs were compared between the two groups. The TILs were assessed using tumor specimens (including six cases of ESCC, six cases of neuroendocrine carcinomas [NECs], and six cases of mixed neuroendocrine–non-neuroendocrine neoplasms [MiNENs]). Results: E-NENs accounted for 3.0% (107/3620) of cases, among which there were just 3 neuroendocrine tumor cases, 51 NEC cases, and 53 MiNENs cases. After matching, esophageal neuroendocrine carcinomas (E-NECs) showed both poorer 5-year overall survival (OS; 35.4% vs. 54.8%, p = 0.0019) and recurrence-free survival (RFS; 29.3% vs. 48.9%, p < 0.001) compared with ESCC. However, the differences were not prominent in the subgroup with stage I. No significant survival benefit was observed for E-NECs with multimodal therapy. Multivariate analysis demonstrated that E-NECs are an independent risk factor for OS and RFS. In the exploratory analysis, E-NECs were associated with less infiltration of immune cells compared with ESCC. Conclusion: E-NECs are significantly associated with a poorer prognosis than ESCC except for early-stage disease. The fewer TILs within the tumor microenvironment of E-NECs compared with ESCC results in weaker anti-tumor immunity and may lead to a poorer prognosis.
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spelling pubmed-100465262023-03-29 Analysis of the Clinicopathological Characteristics, Prognosis, and Lymphocyte Infiltration of Esophageal Neuroendocrine Neoplasms: A Surgery-Based Cohort and Propensity-Score Matching Study Zhang, Long Yu, Boyao Liu, Zhichao Wei, Jinzhi Pan, Jie Jiang, Chao Li, Zhigang Cancers (Basel) Article SIMPLE SUMMARY: Esophageal neuroendocrine neoplasms (E-NENs) are a rare malignancy in esophageal carcinoma; their clinical and oncologic characteristics are poorly reported. Additionally, the effect of surgery on E-NENs remains unclear and controversial. In this study, we retrospectively analyzed the clinicopathological characteristics, prognosis, and immune cell infiltration in E-NENs and compared them with those of esophageal squamous cell carcinoma (ESCC) to determine whether surgery has the same therapeutic efficacy for E-NENs as for ESCC based on a cohort who received surgical treatment. According to our results, first, the target population for surgery may be limited to stage I E-NENs patients. Secondly, E-NENs and especially pure NENs were correlated with the cold tumor phenotype because of the less infiltration of immune cells compared with ESCC. The findings suggest that strategies for immune activation should be developed and applied when immunotherapy is considered for E-NENs in the future. ABSTRACT: Background: Esophageal neuroendocrine neoplasms (E-NENs) are a rare and poorly reported subtype of esophageal carcinoma. We analyzed the differences in clinicopathological features, prognosis, and tumor-infiltrating lymphocytes (TILs) between E-NENs and esophageal squamous cell carcinoma (ESCC). Methods: A total of 3620 patients who underwent esophagectomy were enrolled retrospectively. The study cohort was divided into two groups (E-NENs and ESCC) through propensity-score matching, and the prognosis and TILs were compared between the two groups. The TILs were assessed using tumor specimens (including six cases of ESCC, six cases of neuroendocrine carcinomas [NECs], and six cases of mixed neuroendocrine–non-neuroendocrine neoplasms [MiNENs]). Results: E-NENs accounted for 3.0% (107/3620) of cases, among which there were just 3 neuroendocrine tumor cases, 51 NEC cases, and 53 MiNENs cases. After matching, esophageal neuroendocrine carcinomas (E-NECs) showed both poorer 5-year overall survival (OS; 35.4% vs. 54.8%, p = 0.0019) and recurrence-free survival (RFS; 29.3% vs. 48.9%, p < 0.001) compared with ESCC. However, the differences were not prominent in the subgroup with stage I. No significant survival benefit was observed for E-NECs with multimodal therapy. Multivariate analysis demonstrated that E-NECs are an independent risk factor for OS and RFS. In the exploratory analysis, E-NECs were associated with less infiltration of immune cells compared with ESCC. Conclusion: E-NECs are significantly associated with a poorer prognosis than ESCC except for early-stage disease. The fewer TILs within the tumor microenvironment of E-NECs compared with ESCC results in weaker anti-tumor immunity and may lead to a poorer prognosis. MDPI 2023-03-13 /pmc/articles/PMC10046526/ /pubmed/36980618 http://dx.doi.org/10.3390/cancers15061732 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Zhang, Long
Yu, Boyao
Liu, Zhichao
Wei, Jinzhi
Pan, Jie
Jiang, Chao
Li, Zhigang
Analysis of the Clinicopathological Characteristics, Prognosis, and Lymphocyte Infiltration of Esophageal Neuroendocrine Neoplasms: A Surgery-Based Cohort and Propensity-Score Matching Study
title Analysis of the Clinicopathological Characteristics, Prognosis, and Lymphocyte Infiltration of Esophageal Neuroendocrine Neoplasms: A Surgery-Based Cohort and Propensity-Score Matching Study
title_full Analysis of the Clinicopathological Characteristics, Prognosis, and Lymphocyte Infiltration of Esophageal Neuroendocrine Neoplasms: A Surgery-Based Cohort and Propensity-Score Matching Study
title_fullStr Analysis of the Clinicopathological Characteristics, Prognosis, and Lymphocyte Infiltration of Esophageal Neuroendocrine Neoplasms: A Surgery-Based Cohort and Propensity-Score Matching Study
title_full_unstemmed Analysis of the Clinicopathological Characteristics, Prognosis, and Lymphocyte Infiltration of Esophageal Neuroendocrine Neoplasms: A Surgery-Based Cohort and Propensity-Score Matching Study
title_short Analysis of the Clinicopathological Characteristics, Prognosis, and Lymphocyte Infiltration of Esophageal Neuroendocrine Neoplasms: A Surgery-Based Cohort and Propensity-Score Matching Study
title_sort analysis of the clinicopathological characteristics, prognosis, and lymphocyte infiltration of esophageal neuroendocrine neoplasms: a surgery-based cohort and propensity-score matching study
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10046526/
https://www.ncbi.nlm.nih.gov/pubmed/36980618
http://dx.doi.org/10.3390/cancers15061732
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