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Published in: Annals of Surgical Oncology 2/2024

Open Access 25-11-2023 | Neuroendocrine Tumor | Endocrine Tumors

Surgery as a Principle and Technical Consideration for Primary Tumor Resection of Small Bowel Neuroendocrine Tumors

Authors: Kjetil Søreide, MD, PhD, FRCS (Edin), FACS, FEBS (Hon), Stefan Stättner, MD, Priv.Doz., FRCS (Eng), FEBS (HPB, Hon Surg Onc), Julie Hallet, MD, MSc, FRCSC, FSSO

Published in: Annals of Surgical Oncology | Issue 2/2024

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Abstract

Small bowel neuroendocrine tumors (SB-NETs) are increasingly identified and have become the most frequent entity among small bowel tumors. An increasing incidence, a high prevalence, and a prolonged survival with optimal modern multidisciplinary management makes SB-NETs a unique set of tumors to consider for surgical oncologists. The major goals of surgical treatment in the setting of SB-NET include control of tumor volume, control of endocrine secretion, and prevention of locoregional complications. Key considerations include assessment of multifocality and resection of mesenteric nodal masses with the use of mesenteric-sparing approaches and acceptance of R1 margins if necessary to clear disease while avoiding short bowel syndrome. A description through eight steps for consideration is presented to allow for systematic surgical planning and execution of resection. Moreover, some controversies and evolving considerations to the surgical principles and technical procedures remain. The role of primary tumor resection in the presence of (unresectable) liver metastasis is still unclear. Reports of feasibility of minimally invasive surgery are emerging, with undetermined selection criteria for appropriateness or long-term outcomes. Resection of SB-NETs should be considered in all patients fit for surgery and should follow principles to achieve surgical oncological control that is appropriate for the stage and tumor burden, considering the age and comorbidity of the individual patient.
Literature
1.
go back to reference Lubarsch O. Ueber den primären Krebs des Ileum nebst bemerkungen über das gleichzeitige Vorkommen von Krebs und tuberculose. Virchows Arch Pathol Anat. 1888;111:280–317. Lubarsch O. Ueber den primären Krebs des Ileum nebst bemerkungen über das gleichzeitige Vorkommen von Krebs und tuberculose. Virchows Arch Pathol Anat. 1888;111:280–317.
2.
go back to reference Oberndorfer S. Karzinoide Tumoren des Duenndarms. Frankf Z Pathol. 1907;1:426–9. Oberndorfer S. Karzinoide Tumoren des Duenndarms. Frankf Z Pathol. 1907;1:426–9.
3.
go back to reference Fernandes CJ, Leung G, Eads JR, Katona BW. Gastroenteropancreatic neuroendocrine tumors. Gastroenterol Clin North Am. 2022;51(3):625–47.PubMed Fernandes CJ, Leung G, Eads JR, Katona BW. Gastroenteropancreatic neuroendocrine tumors. Gastroenterol Clin North Am. 2022;51(3):625–47.PubMed
4.
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.PubMed 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.PubMed
5.
go back to reference Board WCoTE, ed WHO classification of tumours. Digestive system Tumours. 5th ed. International Agency for Research Ion Cancer (IARC): WHO Press; 2019. Board WCoTE, ed WHO classification of tumours. Digestive system Tumours. 5th ed. International Agency for Research Ion Cancer (IARC): WHO Press; 2019.
6.
go back to reference Fraenkel M, Kim M, Faggiano A, de Herder WW, Valk GD. Incidence of gastroenteropancreatic neuroendocrine tumours: a systematic review of the literature. Endocr Relat Cancer. 2014;21(3):R153-163.PubMed Fraenkel M, Kim M, Faggiano A, de Herder WW, Valk GD. Incidence of gastroenteropancreatic neuroendocrine tumours: a systematic review of the literature. Endocr Relat Cancer. 2014;21(3):R153-163.PubMed
7.
go back to reference Sandvik OM, Søreide K, Gudlaugsson E, Kvaløy JT, Søreide JA. Epidemiology and classification of gastroenteropancreatic neuroendocrine neoplasms using current coding criteria. Br J Surg. 2016;103(3):226–32.PubMed Sandvik OM, Søreide K, Gudlaugsson E, Kvaløy JT, Søreide JA. Epidemiology and classification of gastroenteropancreatic neuroendocrine neoplasms using current coding criteria. Br J Surg. 2016;103(3):226–32.PubMed
8.
go back to reference White BE, Rous B, Chandrakumaran K, et al. Incidence and survival of neuroendocrine neoplasia in England 1995–2018: a retrospective, population-based study. Lancet Reg Health Eur. 2022;23:100510.PubMedPubMedCentral White BE, Rous B, Chandrakumaran K, et al. Incidence and survival of neuroendocrine neoplasia in England 1995–2018: a retrospective, population-based study. Lancet Reg Health Eur. 2022;23:100510.PubMedPubMedCentral
9.
go back to reference Hallet J, Law CH, Cukier M, Saskin R, Liu N, Singh S. Exploring the rising incidence of neuroendocrine tumors: a population-based analysis of epidemiology, metastatic presentation, and outcomes. Cancer. 2015;121(4):589–97.PubMed Hallet J, Law CH, Cukier M, Saskin R, Liu N, Singh S. Exploring the rising incidence of neuroendocrine tumors: a population-based analysis of epidemiology, metastatic presentation, and outcomes. Cancer. 2015;121(4):589–97.PubMed
10.
go back to reference Søreide K, Hallet J, Jamieson NB, Stättner S. Optimal surgical approach for digestive neuroendocrine neoplasia primaries: oncological benefits versus short and long-term complications. Best Pract Res Clin Endocrinol Metab. 2023;37:101786.PubMed Søreide K, Hallet J, Jamieson NB, Stättner S. Optimal surgical approach for digestive neuroendocrine neoplasia primaries: oncological benefits versus short and long-term complications. Best Pract Res Clin Endocrinol Metab. 2023;37:101786.PubMed
11.
go back to reference Cives M, Strosberg JR. Gastroenteropancreatic neuroendocrine tumors. CA Cancer J Clin. 2018;68(6):471–87.PubMed Cives M, Strosberg JR. Gastroenteropancreatic neuroendocrine tumors. CA Cancer J Clin. 2018;68(6):471–87.PubMed
12.
go back to reference Modlin IM, Champaneria MC, Chan AK, Kidd M. A three-decade analysis of 3911 small intestinal neuroendocrine tumors: the rapid pace of no progress. Am J Gastroenterol. 2007;102(7):1464–73.PubMed Modlin IM, Champaneria MC, Chan AK, Kidd M. A three-decade analysis of 3911 small intestinal neuroendocrine tumors: the rapid pace of no progress. Am J Gastroenterol. 2007;102(7):1464–73.PubMed
13.
go back to reference Kaçmaz E, Sarasqueta AF, van Eeden S, et al. Update on incidence, prevalence, treatment and survival of patients with small bowel neuroendocrine neoplasms in the Netherlands. World J Surg. 2021;45(8):2482–91.PubMedPubMedCentral Kaçmaz E, Sarasqueta AF, van Eeden S, et al. Update on incidence, prevalence, treatment and survival of patients with small bowel neuroendocrine neoplasms in the Netherlands. World J Surg. 2021;45(8):2482–91.PubMedPubMedCentral
14.
go back to reference Snorradottir S, Asgeirsdottir A, Rögnvaldsson S, Jonasson JG, Björnsson ES. Incidence and prognosis of patients with small intestinal neuroendocrine tumors in a population based nationwide study. Cancer Epidemiol. 2022;79:102197.PubMed Snorradottir S, Asgeirsdottir A, Rögnvaldsson S, Jonasson JG, Björnsson ES. Incidence and prognosis of patients with small intestinal neuroendocrine tumors in a population based nationwide study. Cancer Epidemiol. 2022;79:102197.PubMed
15.
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.PubMed 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.PubMed
16.
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.PubMed 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.PubMed
17.
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.PubMedPubMedCentral 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.PubMedPubMedCentral
18.
go back to reference Gangi A, Anaya DA. Surgical principles in the management of small bowel neuroendocrine tumors. Curr Treat Opt Oncol. 2020;21(11):88. Gangi A, Anaya DA. Surgical principles in the management of small bowel neuroendocrine tumors. Curr Treat Opt Oncol. 2020;21(11):88.
19.
go back to reference Hallet J, Law C, Hallet J, et al. Role of primary tumor resection for metastatic small bowel neuroendocrine tumors. World J Surg. 2021;45(1):213–8.PubMed Hallet J, Law C, Hallet J, et al. Role of primary tumor resection for metastatic small bowel neuroendocrine tumors. World J Surg. 2021;45(1):213–8.PubMed
20.
go back to reference Pasquer A, Walter T, Milot L, Hervieu V, Poncet G. Principles of surgical management of small intestinal NET. Cancers (Basel). 2021;13(21):5473.PubMed Pasquer A, Walter T, Milot L, Hervieu V, Poncet G. Principles of surgical management of small intestinal NET. Cancers (Basel). 2021;13(21):5473.PubMed
21.
go back to reference Tran CG, Sherman SK, Howe JR. The landmark series: management of small bowel neuroendocrine tumors. Ann Surg Oncol. 2021;28(5):2741–51.PubMedPubMedCentral Tran CG, Sherman SK, Howe JR. The landmark series: management of small bowel neuroendocrine tumors. Ann Surg Oncol. 2021;28(5):2741–51.PubMedPubMedCentral
22.
go back to reference Bartsch DK, Windel S, Kanngießer V, et al. Vessel-sparing lymphadenectomy should be performed in small intestine neuroendocrine neoplasms. Cancers (Basel). 2022;14(15):3610.PubMed Bartsch DK, Windel S, Kanngießer V, et al. Vessel-sparing lymphadenectomy should be performed in small intestine neuroendocrine neoplasms. Cancers (Basel). 2022;14(15):3610.PubMed
23.
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):1335–42.PubMedPubMedCentral 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):1335–42.PubMedPubMedCentral
24.
go back to reference Blažević A, Hofland J, Hofland LJ, Feelders RA, de Herder WW. Small intestinal neuroendocrine tumours and fibrosis: an entangled conundrum. Endocr Relat Cancer. 2018;25(3):R115-r130.PubMed Blažević A, Hofland J, Hofland LJ, Feelders RA, de Herder WW. Small intestinal neuroendocrine tumours and fibrosis: an entangled conundrum. Endocr Relat Cancer. 2018;25(3):R115-r130.PubMed
25.
go back to reference Daskalakis K, Karakatsanis A, Stålberg P, Norlén O, Hellman P. Clinical signs of fibrosis in small intestinal neuroendocrine tumours. Br J Surg. 2017;104(1):69–75.PubMed Daskalakis K, Karakatsanis A, Stålberg P, Norlén O, Hellman P. Clinical signs of fibrosis in small intestinal neuroendocrine tumours. Br J Surg. 2017;104(1):69–75.PubMed
26.
go back to reference Laskaratos FM, Rombouts K, Caplin M, Toumpanakis C, Thirlwell C, Mandair D. Neuroendocrine tumors and fibrosis: an unsolved mystery? Cancer. 2017;123(24):4770–90.PubMed Laskaratos FM, Rombouts K, Caplin M, Toumpanakis C, Thirlwell C, Mandair D. Neuroendocrine tumors and fibrosis: an unsolved mystery? Cancer. 2017;123(24):4770–90.PubMed
27.
go back to reference Rajaretnam NS, Meyer-Rochow GY. Surgical management of primary small bowel NET presenting acutely with obstruction or perforation. World J Surg. 2021;45(1):203–7.PubMed Rajaretnam NS, Meyer-Rochow GY. Surgical management of primary small bowel NET presenting acutely with obstruction or perforation. World J Surg. 2021;45(1):203–7.PubMed
28.
go back to reference Laskaratos FM, Walker M, Wilkins D, et al. Evaluation of clinical prognostic factors and further delineation of the effect of mesenteric fibrosis on survival in advanced midgut neuroendocrine tumours. Neuroendocrinology. 2018;107(3):292–304.PubMed Laskaratos FM, Walker M, Wilkins D, et al. Evaluation of clinical prognostic factors and further delineation of the effect of mesenteric fibrosis on survival in advanced midgut neuroendocrine tumours. Neuroendocrinology. 2018;107(3):292–304.PubMed
29.
go back to reference Hellman P, Lundström T, Ohrvall U, et al. Effect of surgery on the outcome of midgut carcinoid disease with lymph node and liver metastases. World J Surg. 2002;26(8):991–7.PubMed Hellman P, Lundström T, Ohrvall U, et al. Effect of surgery on the outcome of midgut carcinoid disease with lymph node and liver metastases. World J Surg. 2002;26(8):991–7.PubMed
30.
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.PubMed 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.PubMed
31.
go back to reference Grozinsky-Glasberg S, Davar J, Hofland J, et al. European neuroendocrine tumor society (ENETS) 2022 guidance paper for carcinoid syndrome and carcinoid heart disease. J Neuroendocrinol. 2022;34(7):e13146.PubMedPubMedCentral Grozinsky-Glasberg S, Davar J, Hofland J, et al. European neuroendocrine tumor society (ENETS) 2022 guidance paper for carcinoid syndrome and carcinoid heart disease. J Neuroendocrinol. 2022;34(7):e13146.PubMedPubMedCentral
32.
go back to reference Halperin DM, Shen C, Dasari A, et al. Frequency of carcinoid syndrome at neuroendocrine tumour diagnosis: a population-based study. Lancet Oncol. 2017;18(4):525–34.PubMedPubMedCentral Halperin DM, Shen C, Dasari A, et al. Frequency of carcinoid syndrome at neuroendocrine tumour diagnosis: a population-based study. Lancet Oncol. 2017;18(4):525–34.PubMedPubMedCentral
33.
go back to reference Plöckinger U, Gustafsson B, Ivan D, Szpak W, Davar J. ENETS consensus guidelines for the standards of care in neuroendocrine tumors: echocardiography. Neuroendocrinology. 2009;90(2):190–3.PubMed Plöckinger U, Gustafsson B, Ivan D, Szpak W, Davar J. ENETS consensus guidelines for the standards of care in neuroendocrine tumors: echocardiography. Neuroendocrinology. 2009;90(2):190–3.PubMed
34.
go back to reference Navin PJ, Ehman EC, Liu JB, et al. Imaging of small-bowel neuroendocrine neoplasms: AJR expert panel narrative review. AJR Am J Roentgenol. 2023;221(3):289–301.PubMed Navin PJ, Ehman EC, Liu JB, et al. Imaging of small-bowel neuroendocrine neoplasms: AJR expert panel narrative review. AJR Am J Roentgenol. 2023;221(3):289–301.PubMed
35.
go back to reference Malla S, Kumar P, Madhusudhan KS. Radiology of the neuroendocrine neoplasms of the gastrointestinal tract: a comprehensive review. Abdom Radiol (NY). 2021;46(3):919–35.PubMed Malla S, Kumar P, Madhusudhan KS. Radiology of the neuroendocrine neoplasms of the gastrointestinal tract: a comprehensive review. Abdom Radiol (NY). 2021;46(3):919–35.PubMed
36.
go back to reference Danti G, Flammia F, Matteuzzi B, et al. Gastrointestinal neuroendocrine neoplasms (GI-NENs): hot topics in morphological, functional, and prognostic imaging. Radiol Med. 2021;126(12):1497–507.PubMedPubMedCentral Danti G, Flammia F, Matteuzzi B, et al. Gastrointestinal neuroendocrine neoplasms (GI-NENs): hot topics in morphological, functional, and prognostic imaging. Radiol Med. 2021;126(12):1497–507.PubMedPubMedCentral
37.
go back to reference Ambrosini V, Kunikowska J, Baudin E, et al. Consensus on molecular imaging and theranostics in neuroendocrine neoplasms. Eur J Cancer. 2021;146:56–73.PubMedPubMedCentral Ambrosini V, Kunikowska J, Baudin E, et al. Consensus on molecular imaging and theranostics in neuroendocrine neoplasms. Eur J Cancer. 2021;146:56–73.PubMedPubMedCentral
38.
go back to reference Cuthbertson DJ, Barriuso J, Lamarca A, et al. The impact of (68)gallium DOTA PET/CT in managing patients with sporadic and familial pancreatic neuroendocrine tumours. Front Endocrinol (Lausanne). 2021;12:654975.PubMed Cuthbertson DJ, Barriuso J, Lamarca A, et al. The impact of (68)gallium DOTA PET/CT in managing patients with sporadic and familial pancreatic neuroendocrine tumours. Front Endocrinol (Lausanne). 2021;12:654975.PubMed
39.
go back to reference Kandathil A, Subramaniam R. Gastroenteropancreatic neuroendocrine tumor diagnosis: DOTATATE PET/CT. PET Clin. 2022;18(2):189–200.PubMed Kandathil A, Subramaniam R. Gastroenteropancreatic neuroendocrine tumor diagnosis: DOTATATE PET/CT. PET Clin. 2022;18(2):189–200.PubMed
40.
go back to reference Khatri W, Spiro E, Henderson A, Rowe SP, Solnes LB. Gastro-entero-pancreatic tumors: FDG positron emission tomography/computed tomography. PET Clin. 2023;18(2):243–50.PubMed Khatri W, Spiro E, Henderson A, Rowe SP, Solnes LB. Gastro-entero-pancreatic tumors: FDG positron emission tomography/computed tomography. PET Clin. 2023;18(2):243–50.PubMed
41.
go back to reference Fabritius MP, Soltani V, Cyran CC, et al. Diagnostic accuracy of SSR-PET/CT compared to histopathology in the identification of liver metastases from well-differentiated neuroendocrine tumors. Cancer Imaging. 2023;23(1):92.PubMedPubMedCentral Fabritius MP, Soltani V, Cyran CC, et al. Diagnostic accuracy of SSR-PET/CT compared to histopathology in the identification of liver metastases from well-differentiated neuroendocrine tumors. Cancer Imaging. 2023;23(1):92.PubMedPubMedCentral
42.
go back to reference Sampathirao N, Basu S. MIB-1 index-stratified assessment of dual-tracer PET/CT with (68)Ga-DOTATATE and (18)F-FDG and multimodality anatomic imaging in metastatic neuroendocrine tumors of unknown primary in a PRRT workup setting. J Nucl Med Technol. 2017;45(1):34–41.PubMed Sampathirao N, Basu S. MIB-1 index-stratified assessment of dual-tracer PET/CT with (68)Ga-DOTATATE and (18)F-FDG and multimodality anatomic imaging in metastatic neuroendocrine tumors of unknown primary in a PRRT workup setting. J Nucl Med Technol. 2017;45(1):34–41.PubMed
43.
go back to reference Bucau M, Laurent-Bellue A, Poté N, et al. 18F-FDG uptake in well-differentiated neuroendocrine tumors correlates with both Ki-67 and VHL pathway inactivation. Neuroendocrinology. 2018;106(3):274–82.PubMed Bucau M, Laurent-Bellue A, Poté N, et al. 18F-FDG uptake in well-differentiated neuroendocrine tumors correlates with both Ki-67 and VHL pathway inactivation. Neuroendocrinology. 2018;106(3):274–82.PubMed
44.
go back to reference Chan DL, Pavlakis N, Schembri GP, et al. Dual somatostatin receptor/FDG PET/CT imaging in metastatic neuroendocrine tumours: proposal for a novel grading scheme with prognostic significance. Theranostics. 2017;7(5):1149–58.PubMedPubMedCentral Chan DL, Pavlakis N, Schembri GP, et al. Dual somatostatin receptor/FDG PET/CT imaging in metastatic neuroendocrine tumours: proposal for a novel grading scheme with prognostic significance. Theranostics. 2017;7(5):1149–58.PubMedPubMedCentral
45.
go back to reference Squires MH 3rd, Volkan Adsay N, Schuster DM, et al. Octreoscan versus FDG-PET for neuroendocrine tumor staging: a biological approach. Ann Surg Oncol. 2015;22(7):2295–301.PubMed Squires MH 3rd, Volkan Adsay N, Schuster DM, et al. Octreoscan versus FDG-PET for neuroendocrine tumor staging: a biological approach. Ann Surg Oncol. 2015;22(7):2295–301.PubMed
46.
go back to reference Alexandraki KI, Tsoli M, Kyriakopoulos G, et al. Current concepts in the diagnosis and management of neuroendocrine neoplasms of unknown primary origin. Minerva Endocrinol. 2019;44(4):378–86.PubMed Alexandraki KI, Tsoli M, Kyriakopoulos G, et al. Current concepts in the diagnosis and management of neuroendocrine neoplasms of unknown primary origin. Minerva Endocrinol. 2019;44(4):378–86.PubMed
47.
go back to reference Eriksson J, Norlén O, Ögren M, Garmo H, Ihre-Lundgren C, Hellman P. Primary small intestinal neuroendocrine tumors are highly prevalent and often multiple before metastatic disease develops. Scand J Surg. 2021;110(1):44–50.PubMed Eriksson J, Norlén O, Ögren M, Garmo H, Ihre-Lundgren C, Hellman P. Primary small intestinal neuroendocrine tumors are highly prevalent and often multiple before metastatic disease develops. Scand J Surg. 2021;110(1):44–50.PubMed
48.
go back to reference Keck KJ, Maxwell JE, Utria AF, et al. The distal predilection of small bowel neuroendocrine tumors. Ann Surg Oncol. 2018;25(11):3207–13.PubMedPubMedCentral Keck KJ, Maxwell JE, Utria AF, et al. The distal predilection of small bowel neuroendocrine tumors. Ann Surg Oncol. 2018;25(11):3207–13.PubMedPubMedCentral
49.
go back to reference Maxwell JE, Sherman SK, Stashek KM, O’Dorisio TM, Bellizzi AM, Howe JR. A practical method to determine the site of unknown primary in metastatic neuroendocrine tumors. Surgery. 2014;156(6):1359–65 (discussion 1365-1356).PubMed Maxwell JE, Sherman SK, Stashek KM, O’Dorisio TM, Bellizzi AM, Howe JR. A practical method to determine the site of unknown primary in metastatic neuroendocrine tumors. Surgery. 2014;156(6):1359–65 (discussion 1365-1356).PubMed
50.
go back to reference Gupta A, Lubner MG, Liu JB, Richards ES, Pickhardt PJ. Small bowel neuroendocrine neoplasm: what surgeons want to know. Abdom Radiol (NY). 2022;47(12):4005–15.PubMed Gupta A, Lubner MG, Liu JB, Richards ES, Pickhardt PJ. Small bowel neuroendocrine neoplasm: what surgeons want to know. Abdom Radiol (NY). 2022;47(12):4005–15.PubMed
51.
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.PubMed 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.PubMed
52.
go back to reference Elias D, Lefevre JH, Duvillard P, et al. Hepatic metastases from neuroendocrine tumors with a “thin slice” pathological examination: they are many more than you think. Ann Surg. 2010;251(2):307–10.PubMed Elias D, Lefevre JH, Duvillard P, et al. Hepatic metastases from neuroendocrine tumors with a “thin slice” pathological examination: they are many more than you think. Ann Surg. 2010;251(2):307–10.PubMed
53.
go back to reference Chan DL, Dixon M, Law CHL, et al. Outcomes of cytoreductive surgery for metastatic low-grade neuroendocrine tumors in the setting of extrahepatic metastases. Ann Surg Oncol. 2018;25(6):1768–74.PubMed Chan DL, Dixon M, Law CHL, et al. Outcomes of cytoreductive surgery for metastatic low-grade neuroendocrine tumors in the setting of extrahepatic metastases. Ann Surg Oncol. 2018;25(6):1768–74.PubMed
55.
go back to reference Raphael MJ, Chan DL, Law C, Singh S. Principles of diagnosis and management of neuroendocrine tumours. CMAJ. 2017;189(10):E398-e404.PubMedPubMedCentral Raphael MJ, Chan DL, Law C, Singh S. Principles of diagnosis and management of neuroendocrine tumours. CMAJ. 2017;189(10):E398-e404.PubMedPubMedCentral
56.
go back to reference Koea J. Management of locally advanced and unresectable small bowel neuroendocrine tumours. World J Surg. 2021;45(1):219–24.PubMed Koea J. Management of locally advanced and unresectable small bowel neuroendocrine tumours. World J Surg. 2021;45(1):219–24.PubMed
57.
go back to reference Kaçmaz E, Chen JW, Tanis PJ, Nieveen van Dijkum EJM, Engelsman AF. Postoperative morbidity and mortality after surgical resection of small bowel neuroendocrine neoplasms: a systematic review and meta-analysis. J Neuroendocrinol. 2021;33(8):e13008.PubMedPubMedCentral Kaçmaz E, Chen JW, Tanis PJ, Nieveen van Dijkum EJM, Engelsman AF. Postoperative morbidity and mortality after surgical resection of small bowel neuroendocrine neoplasms: a systematic review and meta-analysis. J Neuroendocrinol. 2021;33(8):e13008.PubMedPubMedCentral
58.
go back to reference Manguso N, Johnson J, Harit A, et al. Prognostic factors associated with outcomes in small bowel neuroendocrine tumors. Am Surg. 2017;83(10):1174–8.PubMed Manguso N, Johnson J, Harit A, et al. Prognostic factors associated with outcomes in small bowel neuroendocrine tumors. Am Surg. 2017;83(10):1174–8.PubMed
59.
go back to reference Søreide JA, Kvaløy JT, Lea D, et al. The overriding role of surgery and tumor grade for long-term survival in patients with gastroenteropancreatic neuroendocrine neoplasms: a population-based cohort study. Cancer Rep (Hoboken). 2022;5(2):e1462.PubMed Søreide JA, Kvaløy JT, Lea D, et al. The overriding role of surgery and tumor grade for long-term survival in patients with gastroenteropancreatic neuroendocrine neoplasms: a population-based cohort study. Cancer Rep (Hoboken). 2022;5(2):e1462.PubMed
60.
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.PubMed Singh S, Moody L, Chan DL, et al. Follow-up recommendations for completely resected gastroenteropancreatic neuroendocrine tumors. JAMA Oncol. 2018;4(11):1597–604.PubMed
61.
go back to reference McGuinness MJ, Woodhouse B, Harmston C, et al. Survival of patients with small bowel neuroendocrine neoplasms in Auckland, Aotearoa New Zealand. ANZ J Surg. 2022;92(7–8):1748–53.PubMedPubMedCentral McGuinness MJ, Woodhouse B, Harmston C, et al. Survival of patients with small bowel neuroendocrine neoplasms in Auckland, Aotearoa New Zealand. ANZ J Surg. 2022;92(7–8):1748–53.PubMedPubMedCentral
62.
go back to reference Hallet J, Law C. Role of primary tumor resection for metastatic small bowel neuroendocrine tumors. World J Surg. 2021;45(1):213–8.PubMed Hallet J, Law C. Role of primary tumor resection for metastatic small bowel neuroendocrine tumors. World J Surg. 2021;45(1):213–8.PubMed
63.
go back to reference Zaidi MY, Lopez-Aguiar AG, Dillhoff M, et al. Prognostic role of lymph node positivity and number of lymph nodes needed for accurately staging small-bowel neuroendocrine tumors. JAMA Surg. 2019;154(2):134–40.PubMed Zaidi MY, Lopez-Aguiar AG, Dillhoff M, et al. Prognostic role of lymph node positivity and number of lymph nodes needed for accurately staging small-bowel neuroendocrine tumors. JAMA Surg. 2019;154(2):134–40.PubMed
64.
go back to reference Landry CS, Lin HY, Phan A, et al. Resection of at-risk mesenteric lymph nodes is associated with improved survival in patients with small bowel neuroendocrine tumors. World J Surg. 2013;37(7):1695–700.PubMed Landry CS, Lin HY, Phan A, et al. Resection of at-risk mesenteric lymph nodes is associated with improved survival in patients with small bowel neuroendocrine tumors. World J Surg. 2013;37(7):1695–700.PubMed
65.
go back to reference Lardière-Deguelte S, de Mestier L, Appéré F, et al. Toward a preoperative classification of lymph node metastases in patients with small intestinal neuroendocrine tumors in the era of intestinal-sparing surgery. Neuroendocrinology. 2016;103(5):552–9.PubMed Lardière-Deguelte S, de Mestier L, Appéré F, et al. Toward a preoperative classification of lymph node metastases in patients with small intestinal neuroendocrine tumors in the era of intestinal-sparing surgery. Neuroendocrinology. 2016;103(5):552–9.PubMed
66.
go back to reference Pasquer A, Walter T, Hervieu V, et al. Surgical management of small bowel neuroendocrine tumors: specific requirements and their impact on staging and prognosis. Ann Surg Oncol. 2015;22(Suppl 3):S742-749.PubMed Pasquer A, Walter T, Hervieu V, et al. Surgical management of small bowel neuroendocrine tumors: specific requirements and their impact on staging and prognosis. Ann Surg Oncol. 2015;22(Suppl 3):S742-749.PubMed
67.
go back to reference Pironi L. Definition, classification, and causes of short bowel syndrome. Nutr Clin Pract. 2023;38(Suppl 1):S9-s16.PubMed Pironi L. Definition, classification, and causes of short bowel syndrome. Nutr Clin Pract. 2023;38(Suppl 1):S9-s16.PubMed
68.
go back to reference Gong J, Guo Z, Li Y, et al. Stapled versus hand suture closure of loop ileostomy: a meta-analysis. Colorectal Dis. 2013;15(10):e561-568.PubMed Gong J, Guo Z, Li Y, et al. Stapled versus hand suture closure of loop ileostomy: a meta-analysis. Colorectal Dis. 2013;15(10):e561-568.PubMed
69.
go back to reference Madani R, Day N, Kumar L, Tilney HS, Gudgeon AM. Hand-sewn versus stapled closure of loop ileostomy: a meta-analysis. Dig Surg. 2019;36(3):183–94.PubMed Madani R, Day N, Kumar L, Tilney HS, Gudgeon AM. Hand-sewn versus stapled closure of loop ileostomy: a meta-analysis. Dig Surg. 2019;36(3):183–94.PubMed
70.
go back to reference Bennett S, Coburn N, Law C, et al. Upfront small bowel resection for small bowel neuroendocrine tumors with synchronous metastases: a propensity-score matched comparative population-based analysis. Ann Surg. 2022;276(5):e450–8.PubMed Bennett S, Coburn N, Law C, et al. Upfront small bowel resection for small bowel neuroendocrine tumors with synchronous metastases: a propensity-score matched comparative population-based analysis. Ann Surg. 2022;276(5):e450–8.PubMed
71.
go back to reference Almond LM, Hodson J, Ford SJ, et al. Role of palliative resection of the primary tumour in advanced pancreatic and small intestinal neuroendocrine tumours: a systematic review and meta-analysis. Eur J Surg Oncol. 2017;43(10):1808–15.PubMed Almond LM, Hodson J, Ford SJ, et al. Role of palliative resection of the primary tumour in advanced pancreatic and small intestinal neuroendocrine tumours: a systematic review and meta-analysis. Eur J Surg Oncol. 2017;43(10):1808–15.PubMed
72.
go back to reference Tsilimigras DI, Ntanasis-Stathopoulos I, Kostakis ID, et al. Is resection of primary midgut neuroendocrine tumors in patients with unresectable metastatic liver disease justified? A systematic review and meta-analysis. J Gastrointest Surg. 2019;23(5):1044–54.PubMed Tsilimigras DI, Ntanasis-Stathopoulos I, Kostakis ID, et al. Is resection of primary midgut neuroendocrine tumors in patients with unresectable metastatic liver disease justified? A systematic review and meta-analysis. J Gastrointest Surg. 2019;23(5):1044–54.PubMed
73.
go back to reference Baiu I, Visser BC. Minimally invasive small bowel cancer surgery. Surg Oncol Clin N Am. 2019;28(2):273–83.PubMed Baiu I, Visser BC. Minimally invasive small bowel cancer surgery. Surg Oncol Clin N Am. 2019;28(2):273–83.PubMed
74.
go back to reference Kaçmaz E, van Eeden S, Koppes JCC, et al. Value of laparoscopy for resection of small-bowel neuroendocrine neoplasms including central mesenteric lymphadenectomy. Dis Colon Rectum. 2021;64(10):1240–8.PubMed Kaçmaz E, van Eeden S, Koppes JCC, et al. Value of laparoscopy for resection of small-bowel neuroendocrine neoplasms including central mesenteric lymphadenectomy. Dis Colon Rectum. 2021;64(10):1240–8.PubMed
75.
go back to reference Pedrazzani C, Conti C, Valdegamberi A, et al. Is laparoscopic CME right hemicolectomy an optimal indication for NET of the right colon and terminal ileum? J Gastrointest Surg. 2021;25(1):333–6.PubMed Pedrazzani C, Conti C, Valdegamberi A, et al. Is laparoscopic CME right hemicolectomy an optimal indication for NET of the right colon and terminal ileum? J Gastrointest Surg. 2021;25(1):333–6.PubMed
76.
go back to reference Figueiredo MN, Maggiori L, Gaujoux S, et al. Surgery for small-bowel neuroendocrine tumors: is there any benefit of the laparoscopic approach? Surg Endosc. 2014;28(5):1720–6.PubMed Figueiredo MN, Maggiori L, Gaujoux S, et al. Surgery for small-bowel neuroendocrine tumors: is there any benefit of the laparoscopic approach? Surg Endosc. 2014;28(5):1720–6.PubMed
77.
go back to reference Dapri G, Bascombe NA. Three trocars laparoscopic right ileocolectomy for advanced small bowel neuroendocrine tumor. Surg Oncol. 2019;28:76–7.PubMed Dapri G, Bascombe NA. Three trocars laparoscopic right ileocolectomy for advanced small bowel neuroendocrine tumor. Surg Oncol. 2019;28:76–7.PubMed
78.
go back to reference Kaçmaz E, Klümpen HJ, Bemelman WA, Nieveen van Dijkum EJM, Engelsman AF, Tanis PJ. Evaluating nationwide application of minimally invasive surgery for treatment of small bowel neuroendocrine neoplasms. World J Surg. 2021;45(8):2463–70.PubMedPubMedCentral Kaçmaz E, Klümpen HJ, Bemelman WA, Nieveen van Dijkum EJM, Engelsman AF, Tanis PJ. Evaluating nationwide application of minimally invasive surgery for treatment of small bowel neuroendocrine neoplasms. World J Surg. 2021;45(8):2463–70.PubMedPubMedCentral
79.
go back to reference Norlén O, Edfeldt K, Akerstrom G, et al. Peritoneal carcinomatosis from small intestinal neuroendocrine tumors: clinical course and genetic profiling. Surgery. 2014;156(6):1512–21 (discussion 1521-1512).PubMed Norlén O, Edfeldt K, Akerstrom G, et al. Peritoneal carcinomatosis from small intestinal neuroendocrine tumors: clinical course and genetic profiling. Surgery. 2014;156(6):1512–21 (discussion 1521-1512).PubMed
80.
go back to reference Norlén O, Montan H, Hellman P, Stålberg P, Sundin A. Preoperative (68)Ga-DOTA-somatostatin analog-PET/CT hybrid imaging increases detection rate of intra-abdominal small intestinal neuroendocrine tumor lesions. World J Surg. 2018;42(2):498–505.PubMed Norlén O, Montan H, Hellman P, Stålberg P, Sundin A. Preoperative (68)Ga-DOTA-somatostatin analog-PET/CT hybrid imaging increases detection rate of intra-abdominal small intestinal neuroendocrine tumor lesions. World J Surg. 2018;42(2):498–505.PubMed
Metadata
Title
Surgery as a Principle and Technical Consideration for Primary Tumor Resection of Small Bowel Neuroendocrine Tumors
Authors
Kjetil Søreide, MD, PhD, FRCS (Edin), FACS, FEBS (Hon)
Stefan Stättner, MD, Priv.Doz., FRCS (Eng), FEBS (HPB, Hon Surg Onc)
Julie Hallet, MD, MSc, FRCSC, FSSO
Publication date
25-11-2023
Publisher
Springer International Publishing
Published in
Annals of Surgical Oncology / Issue 2/2024
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-023-14610-0

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