Tumor infiltrative growth pattern correlates with the immune microenvironment and is an independent factor for lymph nod
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ORIGINAL ARTICLE
Tumor infiltrative growth pattern correlates with the immune microenvironment and is an independent factor for lymph node metastasis and prognosis in stage T1 esophageal squamous cell carcinoma Yuanyuan Zhao 1,2 & Enwei Xu 2 & Xuanqin Yang 2 & Yong Zhang 3 & Hong Chen 1 & Ying Wang 1 & Mulan Jin 1 Received: 27 January 2020 / Revised: 12 March 2020 / Accepted: 18 March 2020 # Springer-Verlag GmbH Germany, part of Springer Nature 2020
Abstract In this retrospective study, we analyzed the association between the tumor infiltrative growth pattern (INF) and tumor immune environment and its predictive value for lymph node metastasis and overall survival (OS) in stage T1 esophageal squamous cell carcinoma (ESCC). In total, 593 patients with a diagnosis of stage T1 ESCC who underwent esophagectomy and regional lymphadenectomy between 2009 and 2018 were included. The INF type and elements of the tumor immune microenvironment, including tumor infiltrative lymphocytes (TILs) and tertiary lymphoid structures (TLSs), were microscopically evaluated within the tumor invasive margin with hematoxylin and eosin (HE)-stained slices. The infiltrative-type INF (INFc) was associated with low-grade TILs and the absence of TLSs, deep tumor invasion, poorly differentiated phenotype. Multivariate logistic regression identified INFc as one of the independent risk factors for lymph node metastasis. INFc and low-grade TILs were independent inferior predictive factors for OS. A novel histologic risk stratification model was classified as INFa/b and high-grade TILs, INFa/ b and low-grade TILs, INFc and high-grade TILs, and INFc and low-grade TILs. The Kaplan-Meier curves showed that INFa/b and high-grade TILs were associated with the best prognosis, and INFc and low-grade TILs were associated with the worst prognosis, and there was significant difference between groups. In conclusion, INFc is an independent risk factor for lymph node metastasis and an independent inferior prognostic factor for stage T1 ESCC. Furthermore, INFc is associated with immunosuppression, and the combination of the INF and TILs is useful for the risk stratification of prognosis. Keywords Esophageal squamous cell carcinoma . Tumor immune microenvironment . Infiltrative growth pattern . Tumor-infiltrating lymphocytes . Tertiary lymphoid structures . Overall survival
Introduction Esophageal cancer is a kind of malignant tumor that seriously threatens human health, and its incidence and morbidity in China rank first in the world [1]. Esophageal squamous cell This article is part of the Topical Collection on Quality in Pathology * Mulan Jin [email protected] 1
Department of Pathology, Beijing Chaoyang Hospital, Capital Medical University, Beijing, China
2
Department of Pathology, Shanxi Cancer Hospital, Taiyuan, China
3
Department of Gastroenterology, Shanxi Cancer Hospital, Taiyuan, China
cancer (ESCC) accounts for 90% of all esophageal cancer cases in China. In Japan, the infiltrative growth pattern (INF) has been routinely assessed as a pathologi
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