Retrospective Study
Copyright ©The Author(s) 2020. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Clin Oncol. Apr 24, 2020; 11(4): 205-216
Published online Apr 24, 2020. doi: 10.5306/wjco.v11.i4.205
Prognostic importance of lymph node yield after curative resection of gastroenteropancreatic neuroendocrine tumours
Jaseela Chiramel, Rose Almond, Astrid Slagter, Adeel Khan, Xin Wang, Kok Haw Jonathan Lim, Melissa Frizziero, Bipasha Chakrabarty, Annamaria Minicozzi, Angela Lamarca, Wasat Mansoor, Richard A Hubner, Juan William Valle, Mairéad Geraldine McNamara
Jaseela Chiramel, Adeel Khan, Kok Haw Jonathan Lim, Melissa Frizziero, Angela Lamarca, Wasat Mansoor, Richard A Hubner, Juan William Valle, Mairéad Geraldine McNamara, Department of Medical Oncology, The Christie NHS Foundation Trust, Manchester M20 4BX, United Kingdom
Jaseela Chiramel, Royal Free London NHS Foundation Trust, London NW3 2QG, United Kingdom
Rose Almond, Xin Wang, Statistics Group, Digital Services, The Christie NHS Foundation Trust, Manchester, M20 4BX, United Kingdom
Astrid Slagter, Antoni van Leeuwenhoek/Netherlands Cancer Institute, Amsterdam 1066 Cx, Netherlands
Bipasha Chakrabarty, Department of Pathology, The Christie NHS Foundation Trust, Manchester M20 4BX, United Kingdom
Annamaria Minicozzi, Department of Surgery, Barts Health NHS Trust, London EC1A 7BE, United Kingdom
Richard A Hubner, Juan William Valle, Mairéad Geraldine McNamara, Division of Cancer Sciences, University of Manchester, Manchester M13 9PL, United Kingdom
Author contributions: Chiramel J wrote the manuscript, drafted conception and designed the study; Almond R and Xin W were in charge of statistical analysis of data; Slagter A, Khan A, and Lim KHJ collected and analysed the data; Frizzero M, Chakrabarty B, Minicozzi A, Lamarca A, Mansoor W, Hubner RA, Valle JW and McNamara MG editing and review the manuscript.
Institutional review board statement: This study was approved by the Quality Improvement and Clinical Audit Committee of The Christie NHS Foundation Trust, Manchester, United Kingdom (reference SE17/2065).
Informed consent statement: Patients were not required to give informed consent to the study. We used anonymous clinical data for the analysis.
Conflict-of-interest statement: The authors report no conflict of interest in this work.
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: http://creativecommons.org/licenses/by-nc/4.0/
Corresponding author: Mairéad Geraldine McNamara, BM BCh, MD, MSc, PhD, Attending Doctor, Senior Lecturer, Senior Researcher, Department of Medical Oncology, The Christie NHS Foundation Trust, 550 Wilmslow Road, Manchester M20 4BX, United Kingdom. mairead.mcnamara@christie.nhs.uk
Received: December 24, 2019
Peer-review started: December 24, 2019
First decision: February 20, 2020
Revised: February 29, 2020
Accepted: April 8, 2020
Article in press: April 8, 2020
Published online: April 24, 2020
Processing time: 119 Days and 17 Hours
Abstract
BACKGROUND

The prognostic significance of lymph nodes (LNs) metastases and the optimum number of LN yield in gastroenteropancreatic neuroendocrine tumours (GEP NETs) undergoing curative resection is still debatable. Many studies have demonstrated that cure rate for patients with GEP NETs can be improved by the resection of the primary tumour and regional lymphadenectomy

AIM

To evaluate the effect of lymph node (LN) status and yield on relapse-free survival (RFS) and overall survival (OS) in patients with resected GEP NETs.

METHODS

Data on patients who underwent curative resection for GEP NETs between January 2002 and March 2017 were analysed retrospectively. Grade 3 tumours (Ki67 > 20%) were excluded. Univariate Cox proportional hazard models were computed for RFS and OS and assessed alongside cut-point analysis to distinguish a suitable binary categorisation of total LNs retrieved associated with RFS.

RESULTS

A total of 217 patients were included in the study. The median age was 59 years (21-97 years) and 51% (n = 111) were male. Primary tumour sites were small bowel (42%), pancreas (25%), appendix (18%), rectum (7%), colon (3%), gastric (2%), others (2%). Median follow up times for all patients were 41 mo (95%CI: 36-51) and 71 mo (95%CI: 63–76) for RFS and OS respectively; 50 relapses and 35 deaths were reported. LNs were retrieved in 151 patients. Eight or more LNs were harvested in 106 patients and LN positivity reported in 114 patients. Three or more positive LNs were detected in 62 cases. The result of univariate analysis suggested perineural invasion (P = 0.0023), LN positivity (P = 0.033), LN retrieval of ≥ 8 (P = 0.047) and localisation (P = 0.0049) have a statistically significant association with shorter RFS, but there was no effect of LN ratio on RFS: P = 0.1 or OS: P = 0.75. Tumour necrosis (P = 0.021) and perineural invasion (P = 0.016) were the only two variables significantly associated with worse OS. In the final multivariable analysis, localisation (pancreas HR = 27.33, P = 0.006, small bowel HR = 32.44, P = 0.005), and retrieval of ≥ 8 LNs (HR = 2.7, P = 0.036) were independent prognostic factors for worse RFS.

CONCLUSION

An outcome-oriented approach to cut-point analysis can suggest a minimum number of adequate LNs to be harvested in patients with GEP NETs undergoing curative surgery. Removal of ≥ 8 LNs is associated with increased risk of relapse, which could be due to high rates of LN positivity at the time of surgery. Given that localisation had a significant association with RFS, a prospective multicentre study is warranted with a clear direction on recommended surgical practice and follow-up guidance for GEP NETs.

Keywords: Well differentiated neuroendocrine tumours, Pancreatic neuroendocrine tumours, Small intestinal neuroendocrine tumours, Ki67, Lymph node ratio, Lymph node retrieval, Lymph node positivity, Relapse-free survival, Overall survival

Core tip: There is no consensus on the optimal number of lymph node (LN) retrieval in patients undergoing resection for gastroenteropancreatic neuroendocrine tumours (GEP NETs). The purpose of this study was to evaluate the LN status and yield on relapse-free survival and overall survival in patients with resected GEP NETs. By using the outcome-oriented approach to cut-point analysis, this study suggested a retrieval of a minimum of eight or more LNs in patients with GEP NETs undergoing curative surgery. The risk of relapse was high in patients who had ≥ 8 LNs retrieved and a high LN yield and LN positivity were seen in small intestinal NETs and pancreatic NETs. The localisation has a significant association with relapse-free survival, necessitating stricter surveillance especially for intestinal NETs and pancreatic NETs.