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Published in: Annals of Surgical Oncology 3/2024

02-01-2024 | Neuroendocrine Tumor | Gastrointestinal Oncology

ASO Practice Guidelines Series: Surgical Management of Gastrointestinal (Midgut) Neuroendocrine Neoplasms

Authors: Julie Hallet, MD, MSc, Callisia N. Clarke, MD, MS

Published in: Annals of Surgical Oncology | Issue 3/2024

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Abstract

Gastrointestinal midgut neuroendocrine neoplasms (NENs) are a heterogeneous group of uncommon malignancies. For well-differentiated NENs, known as neuroendocrine tumors (NETs), surgery is a cornerstone of management in localized and metastatic disease. Because of heterogeneous tumor behaviour, association with endocrine syndrome, and prognosis, the management of NETs must be individualized to all these factors in addition to the primary site. With the fast pace of advancement in the field, both for therapies and understanding of tumoral etiology and behaviour, it is important for surgical oncologists to remain updated on guidelines recommendations and suggested treatment pathways. Those guidelines provide important guidance for management of NETs but are largely based on expert opinions and interpretation of retrospective evidence. This article reviews highlights of most recent practice guidelines for midgut (gastric, duodenal, small intestinal, and appendiceal) NETs.
Literature
1.
go back to reference Hallet J, Cukier M, Saskin R, Liu N. Exploring the rising incidence of neuroendocrine tumors: a population-based analysis of epidemiology, metastatic presentation, and outcomes. Cancer. 2015;121(4):589–97.PubMedCrossRef Hallet J, Cukier M, Saskin R, Liu N. Exploring the rising incidence of neuroendocrine tumors: a population-based analysis of epidemiology, metastatic presentation, and outcomes. Cancer. 2015;121(4):589–97.PubMedCrossRef
2.
go back to reference Dasari A, Shen C, Halperin D, et al. Trends in the incidence, prevalence, and survival outcomes in patients with neuroendocrine tumors in the United States. JAMA Oncol. 2017;3(10):1335–8.PubMedPubMedCentralCrossRef Dasari A, Shen C, Halperin D, et al. Trends in the incidence, prevalence, and survival outcomes in patients with neuroendocrine tumors in the United States. JAMA Oncol. 2017;3(10):1335–8.PubMedPubMedCentralCrossRef
3.
go back to reference Modlin IM, Oberg K, Chung DC, et al. Gastroenteropancreatic neuroendocrine tumours. Lancet Oncol. 2008;9(1):61–72.PubMedCrossRef Modlin IM, Oberg K, Chung DC, et al. Gastroenteropancreatic neuroendocrine tumours. Lancet Oncol. 2008;9(1):61–72.PubMedCrossRef
7.
go back to reference Laskaratos F-M, Rombouts K, Caplin M, Toumpanakis C, Thirlwell C, Mandair D. Neuroendocrine tumors and fibrosis: An unsolved mystery? Cancer. 2017;123(24):4770–90.PubMedCrossRef Laskaratos F-M, Rombouts K, Caplin M, Toumpanakis C, Thirlwell C, Mandair D. Neuroendocrine tumors and fibrosis: An unsolved mystery? Cancer. 2017;123(24):4770–90.PubMedCrossRef
8.
go back to reference Laskaratos FM, Diamantopoulos L, Walker M, et al. Prognostic factors for survival among patients with small bowel neuroendocrine tumours associated with mesenteric desmoplasia. Neuroendocrinology. 2018;106(4):366–80.PubMedCrossRef Laskaratos FM, Diamantopoulos L, Walker M, et al. Prognostic factors for survival among patients with small bowel neuroendocrine tumours associated with mesenteric desmoplasia. Neuroendocrinology. 2018;106(4):366–80.PubMedCrossRef
9.
go back to reference Rindi G, Mete O, Uccella S, et al. Overview of the 2022 WHO classification of neuroendocrine neoplasms. Endocr Pathol. 2022;33(1):115–54.PubMedCrossRef Rindi G, Mete O, Uccella S, et al. Overview of the 2022 WHO classification of neuroendocrine neoplasms. Endocr Pathol. 2022;33(1):115–54.PubMedCrossRef
11.
go back to reference Strosberg JR, Halfdanarson TR, Bellizzi AM, et al. The north American neuroendocrine tumor society consensus guidelines for surveillance and medical management of midgut neuroendocrine tumors. Pancreas. 2017;46(6):707–14.PubMedPubMedCentralCrossRef Strosberg JR, Halfdanarson TR, Bellizzi AM, et al. The north American neuroendocrine tumor society consensus guidelines for surveillance and medical management of midgut neuroendocrine tumors. Pancreas. 2017;46(6):707–14.PubMedPubMedCentralCrossRef
12.
go back to reference Howe JR, Cardona K, Fraker DL, et al. The surgical management of small bowel neuroendocrine tumors: Consensus guidelines of the North American Neuroendocrine Tumor Society. Pancreas. 2017;46(6):715–31.PubMedPubMedCentralCrossRef Howe JR, Cardona K, Fraker DL, et al. The surgical management of small bowel neuroendocrine tumors: Consensus guidelines of the North American Neuroendocrine Tumor Society. Pancreas. 2017;46(6):715–31.PubMedPubMedCentralCrossRef
13.
go back to reference Pavel M, Öberg K, Falconi M, et al. Gastroenteropancreatic neuroendocrine neoplasms: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2020;31(7):844–60.PubMedCrossRef Pavel M, Öberg K, Falconi M, et al. Gastroenteropancreatic neuroendocrine neoplasms: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2020;31(7):844–60.PubMedCrossRef
14.
go back to reference Panzuto F, Ramage J, Pritchard DM, et al. European Neuroendocrine Tumor Society (ENETS) 2023 guidance paper for gastroduodenal neuroendocrine tumours (NETs) G1–G3. J Neuroendocrinol. 2023;35(8):e13306.PubMedCrossRef Panzuto F, Ramage J, Pritchard DM, et al. European Neuroendocrine Tumor Society (ENETS) 2023 guidance paper for gastroduodenal neuroendocrine tumours (NETs) G1–G3. J Neuroendocrinol. 2023;35(8):e13306.PubMedCrossRef
15.
go back to reference Rinke A, Ambrosini V, Dromain C, et al. European Neuroendocrine Tumor Society (ENETS) 2023 guidance paper for colorectal neuroendocrine tumours. J Neuroendocrinol. 2023;35(6):e13309.PubMedCrossRef Rinke A, Ambrosini V, Dromain C, et al. European Neuroendocrine Tumor Society (ENETS) 2023 guidance paper for colorectal neuroendocrine tumours. J Neuroendocrinol. 2023;35(6):e13309.PubMedCrossRef
16.
go back to reference Shah MH, Goldner WS, Benson AB, et al. Neuroendocrine and adrenal tumors, version 2.2021, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw. 2021;19(7):839–68. Shah MH, Goldner WS, Benson AB, et al. Neuroendocrine and adrenal tumors, version 2.2021, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw. 2021;19(7):839–68.
17.
go back to reference Singh S, Moody L, Chan DL, et al. Follow-up recommendations for completely resected gastroenteropancreatic neuroendocrine tumors. JAMA Oncol. 2018;4(11):1597–604.PubMedCrossRef Singh S, Moody L, Chan DL, et al. Follow-up recommendations for completely resected gastroenteropancreatic neuroendocrine tumors. JAMA Oncol. 2018;4(11):1597–604.PubMedCrossRef
18.
go back to reference Tsolakis AV, Ragkousi A, Vujasinovic M, Kaltsas G, Daskalakis K. Gastric neuroendocrine neoplasms type 1: a systematic review and meta-analysis. World J Gastroenterol. 2019;25(35):5376–87.PubMedPubMedCentralCrossRef Tsolakis AV, Ragkousi A, Vujasinovic M, Kaltsas G, Daskalakis K. Gastric neuroendocrine neoplasms type 1: a systematic review and meta-analysis. World J Gastroenterol. 2019;25(35):5376–87.PubMedPubMedCentralCrossRef
19.
go back to reference Howe JR, Merchant NB, Conrad C, et al. The North American Neuroendocrine Tumor Society consensus paper on the surgical management of pancreatic neuroendocrine tumors. Pancreas. 2020;49(1):1–33.PubMedPubMedCentralCrossRef Howe JR, Merchant NB, Conrad C, et al. The North American Neuroendocrine Tumor Society consensus paper on the surgical management of pancreatic neuroendocrine tumors. Pancreas. 2020;49(1):1–33.PubMedPubMedCentralCrossRef
20.
go back to reference Oberg K, Couvelard A, Delle Fave G, et al. ENETS consensus guidelines for standard of care in neuroendocrine tumours: Biochemical markers. Neuroendocrinology. 2017;105(3):201–11.PubMedCrossRef Oberg K, Couvelard A, Delle Fave G, et al. ENETS consensus guidelines for standard of care in neuroendocrine tumours: Biochemical markers. Neuroendocrinology. 2017;105(3):201–11.PubMedCrossRef
21.
go back to reference Fossmark R, Jianu CS, Martinsen TC, Qvigstad G, Syversen U, Waldum HL. Serum gastrin and chromogranin A levels in patients with fundic gland polyps caused by long-term proton-pump inhibition. Scand J Gastroenterol. 2008;43(1):20–4.PubMedCrossRef Fossmark R, Jianu CS, Martinsen TC, Qvigstad G, Syversen U, Waldum HL. Serum gastrin and chromogranin A levels in patients with fundic gland polyps caused by long-term proton-pump inhibition. Scand J Gastroenterol. 2008;43(1):20–4.PubMedCrossRef
22.
go back to reference Esposito G, Cazzato M, Rinzivillo M, et al. Management of type-I gastric neuroendocrine neoplasms: A 10-years prospective single centre study. Dig Liver Dis. 2022;54(7):890–5.PubMedCrossRef Esposito G, Cazzato M, Rinzivillo M, et al. Management of type-I gastric neuroendocrine neoplasms: A 10-years prospective single centre study. Dig Liver Dis. 2022;54(7):890–5.PubMedCrossRef
23.
go back to reference Mandair D, Kamieniarz L, Pizanias M, et al. Diagnostic features and management options for duodenal neuroendocrine neoplasms: a retrospective, multi-centre study. Sci Rep. 2022;12(1):15762.ADSPubMedPubMedCentralCrossRef Mandair D, Kamieniarz L, Pizanias M, et al. Diagnostic features and management options for duodenal neuroendocrine neoplasms: a retrospective, multi-centre study. Sci Rep. 2022;12(1):15762.ADSPubMedPubMedCentralCrossRef
24.
go back to reference Exarchou K, Howes N, Pritchard DM. Systematic review: management of localised low-grade upper gastrointestinal neuroendocrine tumours. Aliment Pharmacol Ther. 2020;51(12):1247–67.PubMedCrossRef Exarchou K, Howes N, Pritchard DM. Systematic review: management of localised low-grade upper gastrointestinal neuroendocrine tumours. Aliment Pharmacol Ther. 2020;51(12):1247–67.PubMedCrossRef
25.
go back to reference Niederle B, Pape UF, Costa F, et al. ENETS consensus guidelines update for neuroendocrine neoplasms of the jejunum and ileum. Neuroendocrinology. 2016;103(2):125–38.PubMedCrossRef Niederle B, Pape UF, Costa F, et al. ENETS consensus guidelines update for neuroendocrine neoplasms of the jejunum and ileum. Neuroendocrinology. 2016;103(2):125–38.PubMedCrossRef
27.
go back to reference Partelli S, Bartsch DK, Capdevila J, et al. ENETS consensus guidelines for standard of care in neuroendocrine tumours: surgery for small intestinal and pancreatic neuroendocrine tumours. Neuroendocrinology. 2017;105(3):255–65.PubMedCrossRef Partelli S, Bartsch DK, Capdevila J, et al. ENETS consensus guidelines for standard of care in neuroendocrine tumours: surgery for small intestinal and pancreatic neuroendocrine tumours. Neuroendocrinology. 2017;105(3):255–65.PubMedCrossRef
28.
go back to reference Öhrvall U, Eriksson B, Juhlin C, et al. Method for dissection of mesenteric metastases in mid-gut carcinoid tumors. World J Surg. 2014;24(11):1402–8.CrossRef Öhrvall U, Eriksson B, Juhlin C, et al. Method for dissection of mesenteric metastases in mid-gut carcinoid tumors. World J Surg. 2014;24(11):1402–8.CrossRef
29.
go back to reference Ohrvall U, Eriksson B, Juhlin C, et al. Method for dissection of mesenteric metastases in mid-gut carcinoid tumors. World J Surg. 2000;24(11):1402–8.PubMedCrossRef Ohrvall U, Eriksson B, Juhlin C, et al. Method for dissection of mesenteric metastases in mid-gut carcinoid tumors. World J Surg. 2000;24(11):1402–8.PubMedCrossRef
30.
go back to reference Hallet J, Law C, Commonwealth Neuroendocrine Tumours Research Collaborative (CommNETs) Surgical Section. Extent of lymph node dissection for small bowel neuroendocrine tumors. World J Surg. 2021;45(1):197–202.PubMedCrossRef Hallet J, Law C, Commonwealth Neuroendocrine Tumours Research Collaborative (CommNETs) Surgical Section. Extent of lymph node dissection for small bowel neuroendocrine tumors. World J Surg. 2021;45(1):197–202.PubMedCrossRef
31.
go back to reference Bennett S, Coburn N, Law C, et al. Upfront small bowel resection for small bowel neuroendocrine tumors with synchronous metastases. Ann Surg. 2022;276(5):e450–8.PubMedCrossRef Bennett S, Coburn N, Law C, et al. Upfront small bowel resection for small bowel neuroendocrine tumors with synchronous metastases. Ann Surg. 2022;276(5):e450–8.PubMedCrossRef
32.
go back to reference Hellman P, Lundström T, Öhrvall U, et al. Effect of surgery on the outcome of midgut carcinoid disease with lymph node and liver metastases. World J Surg. 2002;26:991–7.PubMedCrossRef Hellman P, Lundström T, Öhrvall U, et al. Effect of surgery on the outcome of midgut carcinoid disease with lymph node and liver metastases. World J Surg. 2002;26:991–7.PubMedCrossRef
33.
go back to reference Toumpanakis C, Fazio N, Tiensuu Janson E, et al. Unmet needs in appendiceal neuroendocrine neoplasms. Neuroendocrinology. 2019;108(1):37–44.PubMedCrossRef Toumpanakis C, Fazio N, Tiensuu Janson E, et al. Unmet needs in appendiceal neuroendocrine neoplasms. Neuroendocrinology. 2019;108(1):37–44.PubMedCrossRef
34.
go back to reference Ribeiro S, De Maeyer F, De Man M, et al. Lessons learned about appendiceal neuroendocrine neoplasms from data analysis of the Belgian Cancer Registry 2010–2015. Acta Gastroenterol Belg. 2021;84(3):458–66.PubMedCrossRef Ribeiro S, De Maeyer F, De Man M, et al. Lessons learned about appendiceal neuroendocrine neoplasms from data analysis of the Belgian Cancer Registry 2010–2015. Acta Gastroenterol Belg. 2021;84(3):458–66.PubMedCrossRef
35.
go back to reference Holmager P, Willemoe GL, Nielsen K, et al. Neuroendocrine neoplasms of the appendix: characterization of 335 patients referred to the Copenhagen NET Center of Excellence. Eur J Surg Oncol. 2021;47(6):1357–63.PubMedCrossRef Holmager P, Willemoe GL, Nielsen K, et al. Neuroendocrine neoplasms of the appendix: characterization of 335 patients referred to the Copenhagen NET Center of Excellence. Eur J Surg Oncol. 2021;47(6):1357–63.PubMedCrossRef
36.
go back to reference Boudreaux JP, Klimstra DS, Hassan MM, et al. The NANETS consensus guideline for the diagnosis and management of neuroendocrine tumors: well-differentiated neuroendocrine tumors of the jejunum, ileum, appendix, and cecum. Pancreas. 2010;39(6):753–66.PubMedCrossRef Boudreaux JP, Klimstra DS, Hassan MM, et al. The NANETS consensus guideline for the diagnosis and management of neuroendocrine tumors: well-differentiated neuroendocrine tumors of the jejunum, ileum, appendix, and cecum. Pancreas. 2010;39(6):753–66.PubMedCrossRef
37.
go back to reference Brighi N, La Rosa S, Rossi G, et al. Morphological factors related to nodal metastases in neuroendocrine tumors of the appendix. Ann Surg. 2020;271(3):527–33.PubMedCrossRef Brighi N, La Rosa S, Rossi G, et al. Morphological factors related to nodal metastases in neuroendocrine tumors of the appendix. Ann Surg. 2020;271(3):527–33.PubMedCrossRef
38.
go back to reference Daskalakis K, Alexandraki K, Kassi E, et al. The risk of lymph node metastases and their impact on survival in patients with appendiceal neuroendocrine neoplasms: a systematic review and meta-analysis of adult and paediatric patients. Endocrine. 2020;67(1):20–34.PubMedCrossRef Daskalakis K, Alexandraki K, Kassi E, et al. The risk of lymph node metastases and their impact on survival in patients with appendiceal neuroendocrine neoplasms: a systematic review and meta-analysis of adult and paediatric patients. Endocrine. 2020;67(1):20–34.PubMedCrossRef
39.
go back to reference Galanopoulos M, McFadyen R, Drami I, et al. Challenging the current risk factors of appendiceal neuroendocrine neoplasms: Can they accurately predict local lymph nodal invasion? Results from a large case series. Neuroendocrinology. 2019;109(2):179–86.PubMedCrossRef Galanopoulos M, McFadyen R, Drami I, et al. Challenging the current risk factors of appendiceal neuroendocrine neoplasms: Can they accurately predict local lymph nodal invasion? Results from a large case series. Neuroendocrinology. 2019;109(2):179–86.PubMedCrossRef
40.
go back to reference Pavel M, Baudin E, Couvelard A, et al. ENETS Consensus Guidelines for the management of patients with liver and other distant metastases from neuroendocrine neoplasms of foregut, midgut, hindgut, and unknown primary. Neuroendocrinology. 2012;95(2):157–76.PubMedCrossRef Pavel M, Baudin E, Couvelard A, et al. ENETS Consensus Guidelines for the management of patients with liver and other distant metastases from neuroendocrine neoplasms of foregut, midgut, hindgut, and unknown primary. Neuroendocrinology. 2012;95(2):157–76.PubMedCrossRef
41.
go back to reference Fossmark R, Balto TM, Martinsen TC, et al. Hepatic micrometastases outside macrometastases are present in all patients with ileal neuroendocrine primary tumour at the time of liver resection. Scand J Gastroenterol. 2019;54(8):1003–7.PubMedCrossRef Fossmark R, Balto TM, Martinsen TC, et al. Hepatic micrometastases outside macrometastases are present in all patients with ileal neuroendocrine primary tumour at the time of liver resection. Scand J Gastroenterol. 2019;54(8):1003–7.PubMedCrossRef
42.
go back to reference Elias D, Lefèvre JH, Duvillard P, et al. Hepatic metastases from neuroendocrine tumors with a “thin slice” pathological examination. Ann Surg. 2010;251(2):307–10.PubMedCrossRef Elias D, Lefèvre JH, Duvillard P, et al. Hepatic metastases from neuroendocrine tumors with a “thin slice” pathological examination. Ann Surg. 2010;251(2):307–10.PubMedCrossRef
43.
go back to reference Scott AT, Breheny PJ, Keck KJ, et al. Effective cytoreduction can be achieved in patients with numerous neuroendocrine tumor liver metastases (NETLMs). Surgery. 2019;165(1):166–75.PubMedCrossRef Scott AT, Breheny PJ, Keck KJ, et al. Effective cytoreduction can be achieved in patients with numerous neuroendocrine tumor liver metastases (NETLMs). Surgery. 2019;165(1):166–75.PubMedCrossRef
44.
go back to reference Nadler A, Cukier M, Milot L, Singh S, Law C. Hepatic parenchymal preserving technique in the management of diffuse bilateral neuroendocrine tumour liver metastases: a feasible approach. Can J Surg. 2014;57(2):E2-8.PubMedPubMedCentralCrossRef Nadler A, Cukier M, Milot L, Singh S, Law C. Hepatic parenchymal preserving technique in the management of diffuse bilateral neuroendocrine tumour liver metastases: a feasible approach. Can J Surg. 2014;57(2):E2-8.PubMedPubMedCentralCrossRef
45.
go back to reference Norlén O, Stålberg P, Öberg K, et al. Long-term results of surgery for small intestinal neuroendocrine tumors at a tertiary referral center. World J Surg. 2012;36(6):1419–31.PubMedCrossRef Norlén O, Stålberg P, Öberg K, et al. Long-term results of surgery for small intestinal neuroendocrine tumors at a tertiary referral center. World J Surg. 2012;36(6):1419–31.PubMedCrossRef
Metadata
Title
ASO Practice Guidelines Series: Surgical Management of Gastrointestinal (Midgut) Neuroendocrine Neoplasms
Authors
Julie Hallet, MD, MSc
Callisia N. Clarke, MD, MS
Publication date
02-01-2024
Publisher
Springer International Publishing
Published in
Annals of Surgical Oncology / Issue 3/2024
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-023-14802-8

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