Retrospective Study
Copyright ©The Author(s) 2022. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Sep 14, 2022; 28(34): 5047-5057
Published online Sep 14, 2022. doi: 10.3748/wjg.v28.i34.5047
Analysis of invasiveness and tumor-associated macrophages infiltration in solid pseudopapillary tumors of pancreas
Jie Yang, Chun-Lu Tan, Dan Long, Yan Liang, Li Zhou, Xu-Bao Liu, Yong-Hua Chen
Jie Yang, Chun-Lu Tan, Xu-Bao Liu, Yong-Hua Chen, Department of Pancreatic Surgery, West China Hospital, Sichuan University, Chengdu 610041, Sichuan Province, China
Dan Long, Key Laboratory of Transplant Engineering and Immunology of the Ministry of Health, West China Hospital, Sichuan University, Chengdu 610041, Sichuan Province, China
Yan Liang, Li Zhou, Core Facilities, West China Hospital, Sichuan University, Chengdu 610041, Sichuan Province, China
Author contributions: Yang J, Tan CL, Long D, Liang Y, Zhou Li, Liu XB, and Chen YH designed the research study; Yang J, Tan CL, Liu XB, and Chen YH performed the research; Yang J, Long D, Liang Y, Zhou Li, and Chen YH analyzed the data and wrote the manuscript; all authors have read and approved the final manuscript.
Supported by Natural Science Foundation of China, No. 82071746; Key Research and Development Projects in Sichuan Province, No. 2019YFS0043; and 1·3·5 Project for Disciplines of Excellence–Clinical Research Incubation Project, West China Hospital, Sichuan University, No. ZY2017302.
Institutional review board statement: The study was reviewed and approved by the Medical Ethics Committee of West China Hospital at Sichuan University (2014 Trial No. 37).
Informed consent statement: All study participants or their legal guardians provided informed written consent about personal and medical data collection prior to study enrollment.
Conflict-of-interest statement: All authors report no relevant conflict of interest for this article.
Data sharing statement: No additional data are available.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Yong-Hua Chen, MD, Professor, Department of Pancreatic Surgery, West China Hospital, Sichuan University, No. 37 Guoxue Alley, Wuhou District, Chengdu 610041, Sichuan Province, China. chenyonghua2007@163.com
Received: May 17, 2022
Peer-review started: May 17, 2022
First decision: August 1, 2022
Revised: August 5, 2022
Accepted: August 25, 2022
Article in press: August 25, 2022
Published online: September 14, 2022
Processing time: 113 Days and 6.4 Hours
Abstract
BACKGROUND

Solid pseudopapillary tumor (SPT) is a rare pancreatic tumor. Considering its malignant behaviors, SPT has been classified as a low-grade malignant tumor. Indeed, only 9.2% of all SPT patients are initially diagnosed as malignant with invasion or metastasis. Thus, one of the challenges in managing SPT patients is predicting malignant behavior.

AIM

To investigate the malignant behavior and tumor-associated macrophage (TAM) infiltration between different histopathologic features of SPT patients.

METHODS

Twenty-five formalin-fixed paraffin-embedded tissue samples from 22 patients pathologically diagnosed with an SPT between 2009 and 2019 at West China Hospital were included in this retrospective study. Integrity of the capsule and growth pattern of the tumor cells was assessed microscopically in hematoxylin-eosin (HE)-stained sections. Based on the histopathological features, the SPT patients were divided into two groups: capsule or invasion. Clinical features, malignant behavior, and TAM infiltration were compared between the two groups.

RESULTS

Among the 22 SPT patients, 11 were identified for each group, having either a capsule or invasion histopathologic feature. Malignant behavior was more frequent in the invasion group, including 2 patients who had peripheral organ invasion, 3 with liver metastasis, and 1 with both lymph node and spleen metastases (P= 0.045). Ki-67 index of more than 3% was also more frequent in the invasion group (P = 0.045). Immunohistochemical analysis showed that the invasion group had a significant increase of CD68-positive TAMs in intratumor and peritumor sites in comparison with the capsule group (all P < 0.0001). Similarly, CD163-positive M2-like macrophages were also markedly increased in the intratumor and peritumor sites in the invasion group (all P < 0.0001). At the liver metastasis site, both intratumor and peritumor tissues showed relatively high-level CD68-positive TAMs and CD163-positive M2-like macrophages infiltration. However, the differences between the intratumor, peritumor and normal hepatic tissues did not reach statistical significance (all P > 0.05).

CONCLUSION

SPT patients with invasion evident under microscope were more likely to exhibit malignant behavior and TAM infiltration, especially M2-like macrophages. This finding can help in future investigations of the underlying mechanism of TAM-mediated SPT malignant behavior.

Keywords: Pancreatic neoplasms; Solid pseudopapillary tumors; Malignancy; Tumor-associated macrophages; Histological labeling; Immunohistochemistry

Core Tip: In the present study, we reviewed 22 solid pseudopapillary tumor (SPT) patients to investigate the malignant behavior and tumor-associated macrophage (TAM) infiltration between different histopathologic features. The results showed that invasion detected under microscope was associated with the malignant behavior and TAM infiltration. The phenomenon of increased infiltration of TAMs, especially M2-like macrophages in the invasion feature, might help us to investigate the underlying mechanism of TAM-mediated SPT malignant behavior, as well as to potentially treat recurrent and metastatic SPT by targeting TAMs.