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

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). Met...

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Main Authors: Long Zhang, Boyao Yu, Zhichao Liu, Jinzhi Wei, Jie Pan, Chao Jiang, Zhigang Li
Format: Article
Language:English
Published: MDPI AG 2023-03-01
Series:Cancers
Subjects:
Online Access:https://www.mdpi.com/2072-6694/15/6/1732
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author Long Zhang
Boyao Yu
Zhichao Liu
Jinzhi Wei
Jie Pan
Chao Jiang
Zhigang Li
author_facet Long Zhang
Boyao Yu
Zhichao Liu
Jinzhi Wei
Jie Pan
Chao Jiang
Zhigang Li
author_sort Long Zhang
collection DOAJ
description 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%, <i>p</i> = 0.0019) and recurrence-free survival (RFS; 29.3% vs. 48.9%, <i>p</i> < 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 doaj.art-901759681e3d4562b8cd4e666b81d92a2023-11-17T10:06:26ZengMDPI AGCancers2072-66942023-03-01156173210.3390/cancers15061732Analysis of the Clinicopathological Characteristics, Prognosis, and Lymphocyte Infiltration of Esophageal Neuroendocrine Neoplasms: A Surgery-Based Cohort and Propensity-Score Matching StudyLong Zhang0Boyao Yu1Zhichao Liu2Jinzhi Wei3Jie Pan4Chao Jiang5Zhigang Li6Department of Thoracic Surgery, Section of Esophageal Surgery, Shanghai Chest Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200030, ChinaDepartment of Thoracic Surgery, Section of Esophageal Surgery, Shanghai Chest Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200030, ChinaDepartment of Thoracic Surgery, Section of Esophageal Surgery, Shanghai Chest Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200030, ChinaDepartment of Pathology, Shanghai Chest Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200030, ChinaDepartment of Thoracic Surgery, Section of Esophageal Surgery, Shanghai Chest Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200030, ChinaDepartment of Thoracic Surgery, Section of Esophageal Surgery, Shanghai Chest Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200030, ChinaDepartment of Thoracic Surgery, Section of Esophageal Surgery, Shanghai Chest Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200030, ChinaBackground: 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%, <i>p</i> = 0.0019) and recurrence-free survival (RFS; 29.3% vs. 48.9%, <i>p</i> < 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.https://www.mdpi.com/2072-6694/15/6/1732neuroendocrine neoplasmsesophageal carcinomatumor-infiltrating lymphocytesclinicopathological featuresprognosisimmunotherapy
spellingShingle Long Zhang
Boyao Yu
Zhichao Liu
Jinzhi Wei
Jie Pan
Chao Jiang
Zhigang Li
Analysis of the Clinicopathological Characteristics, Prognosis, and Lymphocyte Infiltration of Esophageal Neuroendocrine Neoplasms: A Surgery-Based Cohort and Propensity-Score Matching Study
Cancers
neuroendocrine neoplasms
esophageal carcinoma
tumor-infiltrating lymphocytes
clinicopathological features
prognosis
immunotherapy
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 neuroendocrine neoplasms
esophageal carcinoma
tumor-infiltrating lymphocytes
clinicopathological features
prognosis
immunotherapy
url https://www.mdpi.com/2072-6694/15/6/1732
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