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New Surgical Strategies

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Neuroendocrine Neoplasia Management

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Abstract

The incidence of gastroenteropancreatic neuroendocrine neoplasms (GEP-NENs) has significantly increased over the last three decades. Surgery is the mainstay for their management as it represents the only possibility of reaching a definitive cure. GEP-NENs are characterized by a high level of heterogeneity, in terms of both clinical presentation and disease aggressiveness. Therefore, their surgical treatment should be tailored taking into account tumor and patient’s features. A surveillance strategy has been advocated for the management of incidentally discovered, asymptomatic, small lesions without radiological or endoscopic features of malignancy. On the other hand, formal resections associated to lymphadenectomy are the gold standard for patients with localized GEP-NENs for whom a conservative strategy is not feasible. Finally, surgery may play a role even for selected patients with metastatic or high-grade well-differentiated neoplasms, who could benefit from this strategy. Therefore, surgery should be included in a multimodal treatment approach for patients with advanced GEP-NENs.

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References

  1. Yao JC, Hassan M, Phan A, Dagohoy C, Leary C, Mares JE, et al. One hundred years after “carcinoid”: epidemiology of and prognostic factors for neuroendocrine tumors in 35,825 cases in the United States. J Clin Oncol. 2008;26(18):3063–72.

    Article  PubMed  Google Scholar 

  2. Dasari A, Shen C, Halperin D, Zhao B, Zhou S, Xu Y, 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.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Vagefi PA, Razo O, Deshpande V, McGrath DJ, Lauwers GY, Thayer SP, et al. Evolving patterns in the detection and outcomes of pancreatic neuroendocrine neoplasms: the Massachusetts General Hospital experience from 1977 to 2005. Arch Surg. 2007;142(4):347–54.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Cives M, Strosberg JR. Gastroenteropancreatic neuroendocrine tumors. CA Cancer J Clin. 2018;68(6):471–87.

    Article  PubMed  Google Scholar 

  5. Falconi M, Eriksson B, Kaltsas G, Bartsch DK, Capdevila J, Caplin M, et al. ENETS consensus guidelines update for the management of patients with functional pancreatic neuroendocrine tumors and non-functional pancreatic neuroendocrine tumors. Neuroendocrinology. 2016; https://doi.org/10.1159/000443171.

  6. Pape U-F, Perren A, Niederle B, Gross D, Gress T, Costa F, et al. ENETS Consensus Guidelines for the management of patients with neuroendocrine neoplasms from the jejuno-ileum and the appendix including goblet cell carcinomas. Neuroendocrinology. 2012;95(2):135–56.

    Article  CAS  PubMed  Google Scholar 

  7. Partelli S, Bartsch DK, Capdevila J, Chen J, Knigge U, Niederle B, 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.

    Article  CAS  PubMed  Google Scholar 

  8. Delle Fave G, O’Toole D, Sundin A, Taal B, Ferolla P, Ramage JK, et al. ENETS consensus guidelines update for gastroduodenal neuroendocrine neoplasms. Neuroendocrinology. 2016;103(2):119–24.

    Article  CAS  PubMed  Google Scholar 

  9. Howe JR, Merchant NB, Conrad C, Keutgen XM, Hallet J, Drebin JA, et al. The North American neuroendocrine tumor society consensus paper on the surgical management of pancreatic neuroendocrine tumors. Pancreas. 2020;49(1):1–33.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Ramage JK, De Herder WW, Delle Fave G, Ferolla P, Ferone D, Ito T, et al. ENETS consensus guidelines update for colorectal neuroendocrine neoplasms. Neuroendocrinology. 2016; https://doi.org/10.1159/000443166.

  11. Kuo EJ, Salem RR. Population-level analysis of pancreatic neuroendocrine tumors 2 cm or less in size. Ann Surg Oncol. 2013;20(9):2815–21.

    Article  PubMed  Google Scholar 

  12. Partelli S, Giannone F, Schiavo Lena M, Muffatti F, Andreasi V, Crippa S, et al. Is the real prevalence of pancreatic neuroendocrine tumors underestimated? A retrospective study on a large series of pancreatic specimens. Neuroendocrinology. 2019; https://doi.org/10.1159/000499606.

  13. Partelli S, Cirocchi R, Crippa S, Cardinali L, Fendrich V, Bartsch DK, et al. Systematic review of active surveillance versus surgical management of asymptomatic small non-functioning pancreatic neuroendocrine neoplasms. Br J Surg. 2017;104(1):34–41.

    Article  CAS  PubMed  Google Scholar 

  14. Partelli S, Mazza M, Andreasi V, Muffatti F, Crippa S, Tamburrino D, et al. Management of small asymptomatic nonfunctioning pancreatic neuroendocrine tumors: limitations to apply guidelines into real life. Surg (United States). 2019; https://doi.org/10.1016/j.surg.2019.04.003.

  15. Barenboim A, Lahat G, Nachmany I, Nakache R, Goykhman Y, Geva R, et al. Resection versus observation of small asymptomatic nonfunctioning pancreatic neuroendocrine tumors. J Gastrointest Surg. 2019; https://doi.org/10.1007/s11605-019-04285-y.

  16. Powers BD, Rothermel LD, Fleming JB, Strosberg JR, Anaya DA. A survival analysis of patients with localized, asymptomatic pancreatic neuroendocrine tumors: no surgical survival benefit when examining appropriately selected outcomes. J Gastrointest Surg. 2019; https://doi.org/10.1007/s11605-019-04433-4.

  17. Mintziras I, Keck T, Werner J, Fichtner-Feigl S, Wittel U, Senninger N, et al. Implementation of current ENETS guidelines for surgery of small (≤2 cm) pancreatic neuroendocrine neoplasms in the German surgical community: an analysis of the prospective DGAV StuDoQ|Pancreas registry. World J Surg. 2019; https://doi.org/10.1007/s00268-018-4751-2.

  18. Ariotti R, Partelli S, Muffatti F, Andreasi V, Della Sala F, Falconi M. How should incidental NEN of the pancreas and gastrointestinal tract be followed? Rev Endocr Metab Disord. 2018; https://doi.org/10.1007/s11154-018-9445-4.

  19. Sato Y, Hashimoto S, Mizuno K-I, Takeuchi M, Terai S. Management of gastric and duodenal neuroendocrine tumors. World J Gastroenterol. 2016;22(30):6817–28.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Sato Y, Takeuchi M, Hashimoto S, Mizuno K, Kobayashi M, Iwafuchi M, et al. Usefulness of endoscopic submucosal dissection for type I gastric carcinoid tumors compared with endoscopic mucosal resection. Hepato-Gastroenterology. 2013;60(126):1524–9.

    PubMed  Google Scholar 

  21. Kim HH, Kim GH, Kim JH, Choi M-G, Song GA, Kim SE. The efficacy of endoscopic submucosal dissection of type I gastric carcinoid tumors compared with conventional endoscopic mucosal resection. Gastroenterol Res Pract. 2014;2014:253860.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Merola E, Sbrozzi-Vanni A, Panzuto F, D’Ambra G, Di Giulio E, Pilozzi E, et al. Type I gastric carcinoids: a prospective study on endoscopic management and recurrence rate. Neuroendocrinology. 2012;95(3):207–13.

    Article  CAS  PubMed  Google Scholar 

  23. Tomassetti P, Migliori M, Caletti GC, Fusaroli P, Corinaldesi R, Gullo L. Treatment of type II gastric carcinoid tumors with somatostatin analogues. N Engl J Med. 2000;343(8):551–4.

    Article  CAS  PubMed  Google Scholar 

  24. Kulke MH, Anthony LB, Bushnell DL, de Herder WW, Goldsmith SJ, Klimstra DS, et al. NANETS treatment guidelines: well-differentiated neuroendocrine tumors of the stomach and pancreas. Pancreas. 2010;39(6):735–52.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Kwon YH, Jeon SW, Kim GH, Kim J, Chung I-K, Jee SR, et al. Long-term follow up of endoscopic resection for type 3 gastric NET. World J Gastroenterol. 2013;19(46):8703–8.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Min B-H, Hong M, Lee JH, Rhee P-L, Sohn TS, Kim S, et al. Clinicopathological features and outcome of type 3 gastric neuroendocrine tumours. Br J Surg. 2018;105(11):1480–6.

    Article  PubMed  Google Scholar 

  27. Fitzgerald TL, Dennis SO, Kachare SD, Vohra NA, Zervos EE. Increasing incidence of duodenal neuroendocrine tumors: incidental discovery of indolent disease? Surgery. 2015;158(2):466–71.

    Article  PubMed  Google Scholar 

  28. Margonis GA, Samaha M, Kim Y, Postlewait LM, Kunz P, Maithel S, et al. A multi-institutional analysis of duodenal neuroendocrine tumors: tumor biology rather than extent of resection dictates prognosis. J Gastrointest Surg. 2016;20(6):1098–105.

    Article  PubMed  Google Scholar 

  29. Mullen JT, Wang H, Yao JC, Lee JH, Perrier ND, Pisters PWT, et al. Carcinoid tumors of the duodenum. Surgery. 2005;138(6):971–8.

    Article  PubMed  Google Scholar 

  30. Niederle B, Pape U-F, Costa F, Gross D, Kelestimur F, Knigge U, et al. ENETS consensus guidelines update for neuroendocrine neoplasms of the jejunum and ileum. Neuroendocrinology. 2016;103(2):125–38.

    Article  CAS  PubMed  Google Scholar 

  31. Walsh JC, Schaeffer DF, Kirsch R, Pollett A, Manzoni M, Riddell RH, et al. Ileal “carcinoid” tumors-small size belies deadly intent: high rate of nodal metastasis in tumors </=1 cm in size. Hum Pathol. 2016;56:123–7.

    Article  PubMed  Google Scholar 

  32. Wang AY, Ahmad NA. Rectal carcinoids. Curr Opin Gastroenterol. 2006;22(5):529–35.

    Article  PubMed  Google Scholar 

  33. de Mestier L, Lorenzo D, Fine C, Cros J, Hentic O, Walter T, et al. Endoscopic, transanal, laparoscopic, and transabdominal management of rectal neuroendocrine tumors. Best Pract Res Clin Endocrinol Metab. 2019;33(5):101293.

    Article  PubMed  Google Scholar 

  34. Anthony LB, Strosberg JR, Klimstra DS, Maples WJ, O’Dorisio TM, Warner RRP, et al. The NANETS consensus guidelines for the diagnosis and management of gastrointestinal neuroendocrine tumors (nets): well-differentiated nets of the distal colon and rectum. Pancreas. 2010;39(6):767–74.

    Article  PubMed  Google Scholar 

  35. de Mestier L, Brixi H, Gincul R, Ponchon T, Cadiot G. Updating the management of patients with rectal neuroendocrine tumors. Endoscopy. 2013;45(12):1039–46.

    Article  PubMed  Google Scholar 

  36. He L, Deng T, Luo H. Efficacy and safety of endoscopic resection therapies for rectal carcinoid tumors: a meta-analysis. Yonsei Med J. 2015;56(1):72–81.

    Article  PubMed  Google Scholar 

  37. Gerard J-P, Andre T, Bibeau F, Conroy T, Legoux J-L, Portier G, et al. Rectal cancer: French Intergroup clinical practice guidelines for diagnosis, treatments and follow-up (SNFGE, FFCD, GERCOR, UNICANCER, SFCD, SFED, SFRO). Dig Liver Dis. 2017;49(4):359–67.

    Article  PubMed  Google Scholar 

  38. Caplin M, Sundin A, Nillson O, Baum RP, Klose KJ, Kelestimur F, et al. ENETS Consensus Guidelines for the management of patients with digestive neuroendocrine neoplasms: colorectal neuroendocrine neoplasms. Neuroendocrinology. 2012;95(2):88–97.

    Article  CAS  PubMed  Google Scholar 

  39. Kwaan MR, Goldberg JE, Bleday R. Rectal carcinoid tumors: review of results after endoscopic and surgical therapy. Arch Surg. 2008;143(5):471–5.

    Article  PubMed  Google Scholar 

  40. Park CH, Cheon JH, Kim JO, Shin JE, Jang BI, Shin SJ, et al. Criteria for decision making after endoscopic resection of well-differentiated rectal carcinoids with regard to potential lymphatic spread. Endoscopy. 2011;43(9):790–5.

    Article  CAS  PubMed  Google Scholar 

  41. Shah MH, Goldner WS, Halfdanarson TR, Bergsland E, Berlin JD, Halperin D, et al. NCCN guidelines insights: neuroendocrine and adrenal tumors, version 2. 2018. J Natl Compr Cancer Netw. 2018; https://doi.org/10.6004/jnccn.2018.0056.

  42. Zaidi MY, Lopez-Aguiar AG, Switchenko JM, Lipscomb J, Andreasi V, Partelli S, et al. A novel validated recurrence risk score to guide a pragmatic surveillance strategy after resection of pancreatic neuroendocrine tumors: an international study of 1006 patients. Ann Surg. 2019; https://doi.org/10.1097/SLA.0000000000003461.

  43. Genç CG, Jilesen AP, Partelli S, Falconi M, Muffatti F, Van Kemenade FJ, et al. A new scoring system to predict recurrent disease in grade 1 and 2 nonfunctional pancreatic neuroendocrine tumors. Ann Surg. 2018; https://doi.org/10.1097/SLA.0000000000002123.

  44. Partelli S, Gaujoux S, Boninsegna L, Cherif R, Crippa S, Couvelard A, et al. Pattern and clinical predictors of lymph node involvement in nonfunctioning pancreatic neuroendocrine tumors (NF-PanNETs). JAMA Surg. 2013; https://doi.org/10.1001/jamasurg.2013.3376.

  45. Bettini R, Partelli S, Boninsegna L, Capelli P, Crippa S, Pederzoli P, et al. Tumor size correlates with malignancy in nonfunctioning pancreatic endocrine tumor. Surgery. 2011;150(1):75–82.

    Article  PubMed  Google Scholar 

  46. Partelli S, Javed AA, Andreasi V, He J, Muffatti F, Weiss MJ, et al. The number of positive nodes accurately predicts recurrence after pancreaticoduodenectomy for nonfunctioning neuroendocrine neoplasms. Eur J Surg Oncol. 2018;44(6):778–83. https://doi.org/10.1016/j.ejso.2018.03.005.

    Article  PubMed  Google Scholar 

  47. Zhang X-F, Xue F, Dong D-H, Lopez-Aguiar AG, Poultsides G, Makris E, et al. New nodal staging for primary pancreatic neuroendocrine tumors: a multi-institutional and national data analysis. Ann Surg. 2019; https://doi.org/10.1097/SLA.0000000000003478.

  48. Lopez-Aguiar AG, Zaidi MY, Beal EW, Dillhoff M, Cannon JGD, Poultsides GA, et al. Defining the role of lymphadenectomy for pancreatic neuroendocrine tumors: an eight-institution study of 695 patients from the us neuroendocrine tumor study group. Ann Surg Oncol. 2019;26(8):2517–24.

    Article  PubMed  Google Scholar 

  49. Partelli S, Boninsegna L, Salvia R, Bassi C, Pederzoli P, Falconi M. Middle-preserving pancreatectomy for multicentric body-sparing lesions of the pancreas. Am J Surg. 2009;198(3):e49–53.

    Article  PubMed  Google Scholar 

  50. Andreasi V, Partelli S, Capurso G, Muffatti F, Balzano G, Crippa S, et al. Long-term pancreatic functional impairment after surgery for neuroendocrine neoplasms. J Clin Med. 2019;8(10) https://doi.org/10.3390/jcm8101611.

  51. Lim PW, Dinh KH, Sullivan M, Wassef WY, Zivny J, Whalen GF, et al. Thirty-day outcomes underestimate endocrine and exocrine insufficiency after pancreatic resection. HPB. 2016; https://doi.org/10.1016/j.hpb.2015.11.003.

  52. Huttner FJ, Koessler-Ebs J, Hackert T, Ulrich A, Buchler MW, Diener MK. Meta-analysis of surgical outcome after enucleation versus standard resection for pancreatic neoplasms. Br J Surg. 2015;102(9):1026–36.

    Article  CAS  PubMed  Google Scholar 

  53. Chua TC, Yang TX, Gill AJ, Samra JS. Systematic review and meta-analysis of enucleation versus standardized resection for small pancreatic lesions. Ann Surg Oncol. 2016;23(2):592–9.

    Article  PubMed  Google Scholar 

  54. Heeger K, Falconi M, Partelli S, Waldmann J, Crippa S, Fendrich V, et al. Increased rate of clinically relevant pancreatic fistula after deep enucleation of small pancreatic tumors. Langenbeck’s Arch Surg. 2014;399(3):315–21.

    Article  Google Scholar 

  55. Paiella S, De Pastena M, Faustini F, Landoni L, Pollini T, Bonamini D, et al. Central pancreatectomy for benign or low-grade malignant pancreatic lesions - a single-center retrospective analysis of 116 cases. Eur J Surg Oncol. 2019; https://doi.org/10.1016/j.ejso.2018.11.021.

  56. Balzano G, Maffi P, Nano R, Mercalli A, Melzi R, Aleotti F, et al. Autologous islet transplantation in patients requiring pancreatectomy: a broader spectrum of indications beyond chronic pancreatitis. Am J Transplant. 2016; https://doi.org/10.1111/ajt.13656.

  57. Balzano G, Maffi P, Nano R, Zerbi A, Venturini M, Melzi R, et al. Extending indications for islet autotransplantation in pancreatic surgery. Ann Surg. 2013;258(2):210–8.

    Article  PubMed  Google Scholar 

  58. Venturini M, Sallemi C, Colantoni C, Agostini G, Balzano G, Esposito A, et al. Single-centre experience of extending indications for percutaneous intraportal islet autotransplantation (PIPIAT) after pancreatic surgery to prevent diabetes: feasibility, radiological aspects, complications and clinical outcome. Br J Radiol. 2016;89(1064):20160246.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Kulke MH, Shah MH, Benson AB 3rd, Bergsland E, Berlin JD, Blaszkowsky LS, et al. Neuroendocrine tumors, version 1.2015. J Natl Compr Cancer Netw. 2015;13(1):78–108.

    Article  CAS  Google Scholar 

  60. Clements WM, Martin SP, Stemmerman G, Lowy AM. Ampullary carcinoid tumors: rationale for an aggressive surgical approach. J Gastrointest Surg. 2003;7(6):773–6.

    Article  PubMed  Google Scholar 

  61. Dogeas E, Cameron JL, Wolfgang CL, Hirose K, Hruban RH, Makary MA, et al. Duodenal and ampullary carcinoid tumors: size predicts necessity for lymphadenectomy. J Gastrointest Surg. 2017;21(8):1262–9.

    Article  PubMed  Google Scholar 

  62. Hartel M, Wente MN, Sido B, Friess H, Buchler MW. Carcinoid of the ampulla of Vater. J Gastroenterol Hepatol. 2005;20(5):676–81.

    Article  PubMed  Google Scholar 

  63. Partelli S, Tamburrino D, Cherif R, Muffatti F, Moggia E, Gaujoux S, et al. Risk and predictors of postoperative morbidity and mortality after pancreaticoduodenectomy for pancreatic neuroendocrine neoplasms: a comparative study with pancreatic ductal adenocarcinoma. Pancreas. 2019;48(4):504–9.

    Article  PubMed  Google Scholar 

  64. Norton JA, Fraker DL, Alexander HR, Gibril F, Liewehr DJ, Venzon DJ, et al. Surgery increases survival in patients with gastrinoma. Ann Surg. 2006;244(3):410–9.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Jensen RT, Niederle B, Mitry E, Ramage JK, Steinmuller T, Lewington V, et al. Gastrinoma (duodenal and pancreatic). Neuroendocrinology. 2006;84(3):173–82.

    Article  CAS  PubMed  Google Scholar 

  66. Albers MB, Manoharan J, Bartsch DK. Contemporary surgical management of the Zollinger-Ellison syndrome in multiple endocrine neoplasia type 1. Best Pract Res Clin Endocrinol Metab. 2019;33(5):101318.

    Article  PubMed  Google Scholar 

  67. Lopez CL, Falconi M, Waldmann J, Boninsegna L, Fendrich V, Goretzki PK, et al. Partial pancreaticoduodenectomy can provide cure for duodenal gastrinoma associated with multiple endocrine neoplasia type 1. Ann Surg. 2013;257(2):308–14.

    Article  PubMed  Google Scholar 

  68. Hughes MS, Azoury SC, Assadipour Y, Straughan DM, Trivedi AN, Lim RM, et al. Prospective evaluation and treatment of familial carcinoid small intestine neuroendocrine tumors (SI-NETs). Surgery. 2016;159(1):350–6.

    Article  PubMed  Google Scholar 

  69. de Mestier L, Lardiere-Deguelte S, Brixi H, O’Toole D, Ruszniewski P, Cadiot G, et al. Updating the surgical management of peritoneal carcinomatosis in patients with neuroendocrine tumors. Neuroendocrinology. 2015;101(2):105–11.

    Article  PubMed  CAS  Google Scholar 

  70. Gonzalez RS, Liu EH, Alvarez JR, Ayers GD, Washington MK, Shi C. Should mesenteric tumor deposits be included in staging of well-differentiated small intestine neuroendocrine tumors? Mod Pathol Off J US Can Acad Pathol Inc. 2014;27(9):1288–95.

    CAS  Google Scholar 

  71. Howe JR, Cardona K, Fraker DL, Kebebew E, Untch BR, Wang Y-Z, 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.

    Article  PubMed  PubMed Central  Google Scholar 

  72. Lardiere-Deguelte S, de Mestier L, Appere F, Vullierme M-P, Zappa M, Hoeffel C, 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.

    Article  CAS  PubMed  Google Scholar 

  73. Landry CS, Lin HY, Phan A, Charnsangavej C, Abdalla EK, Aloia T, 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.

    Article  PubMed  Google Scholar 

  74. Zaidi MY, Lopez-Aguiar AG, Dillhoff M, Beal E, Poultsides G, Makris E, 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.

    Article  PubMed  Google Scholar 

  75. Motz BM, Lorimer PD, Boselli D, Hill JS, Salo JC. Optimal lymphadenectomy in small bowel neuroendocrine tumors: analysis of the NCDB. J Gastrointest Surg. 2018;22(1):117–23.

    Article  PubMed  Google Scholar 

  76. McConnell YJ. Surgical management of rectal carcinoids: trends and outcomes from the Surveillance, Epidemiology, and End Results database (1988 to 2012). Am J Surg. 2016;211(5):877–85.

    Article  PubMed  Google Scholar 

  77. Wang Y-Z, Beyer DT, Hall M. Obturator canal lymph node metastasis from rectal carcinoid tumors: total mesorectal excision may be insufficient. J Gastrointest Surg. 2016;20(6):1247–52.

    Article  PubMed  Google Scholar 

  78. Zhang X-F, Lopez-Aguiar AG, Poultsides G, Makris E, Rocha F, Kanji Z, et al. Minimally invasive versus open distal pancreatectomy for pancreatic neuroendocrine tumors: an analysis from the U.S. neuroendocrine tumor study group. J Surg Oncol. 2019;120(2):231–40.

    PubMed  Google Scholar 

  79. Edwin B, Sahakyan MA, Abu Hilal M, Besselink MG, Braga M, Fabre JM, et al. Laparoscopic surgery for pancreatic neoplasms: the European association for endoscopic surgery clinical consensus conference. Surg Endosc. 2017; https://doi.org/10.1007/s00464-017-5414-3.

  80. Partelli S, Andreasi V, Rancoita PMV, Perez-Sanchez E, Muffatti F, Balzano G, et al. Outcomes after distal pancreatectomy for neuroendocrine neoplasms: a retrospective comparison between minimally invasive and open approach using propensity score weighting. Surg Endosc. 2020; https://doi.org/10.1007/s00464-020-07375-0.

  81. Tamburrino D, Partelli S, Renzi C, Crippa S, Muffatti F, Perali C, et al. Systematic review and meta-analysis on laparoscopic pancreatic resections for neuroendocrine neoplasms (PNENs). Expert Rev Gastroenterol Hepatol. 2017;11(1):65–73.

    Article  CAS  PubMed  Google Scholar 

  82. Alfieri S, Butturini G, Boggi U, Pietrabissa A, Morelli L, Vistoli F, et al. Short-term and long-term outcomes after robot-assisted versus laparoscopic distal pancreatectomy for pancreatic neuroendocrine tumors (pNETs): a multicenter comparative study. Langenbeck’s Arch Surg. 2019;404(4):459–68.

    Article  Google Scholar 

  83. Guerrini GP, Lauretta A, Belluco C, Olivieri M, Forlin M, Basso S, et al. Robotic versus laparoscopic distal pancreatectomy: an up-to-date meta-analysis. BMC Surg. 2017;17(1):105.

    Article  PubMed  PubMed Central  Google Scholar 

  84. Pasquer A, Walter T, Hervieu V, Forestier J, Scoazec J-Y, Lombard-Bohas C, 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):S742–9.

    Article  PubMed  Google Scholar 

  85. Moon CM, Huh KC, Jung S-A, Park DI, Kim WH, Jung HM, et al. Long-term clinical outcomes of rectal neuroendocrine tumors according to the pathologic status after initial endoscopic resection: a KASID multicenter study. Am J Gastroenterol. 2016;111(9):1276–85.

    Article  PubMed  Google Scholar 

  86. Heetfeld M, Chougnet CN, Olsen IH, Rinke A, Borbath I, Crespo G, et al. Characteristics and treatment of patients with G3 gastroenteropancreatic neuroendocrine neoplasms. Endocr Relat Cancer. 2015;22(4):657–64.

    Article  CAS  PubMed  Google Scholar 

  87. Perren A. WHO classification of tumours. Digestive system tumours. 5th ed. Lyon: IARC; 2019.

    Google Scholar 

  88. Garcia-Carbonero R, Rinke A, Valle JW, Fazio N, Caplin M, Gorbounova V, et al. ENETS consensus guidelines for the standards of care in neuroendocrine neoplasms. Systemic therapy 2: chemotherapy. Neuroendocrinology. 2017;105(3):281–94.

    Article  CAS  PubMed  Google Scholar 

  89. Strosberg JR, Coppola D, Klimstra DS, Phan AT, Kulke MH, Wiseman GA, et al. The NANETS consensus guidelines for the diagnosis and management of poorly differentiated (high-grade) extrapulmonary neuroendocrine carcinomas. Pancreas. 2010;39(6):799–800.

    Article  PubMed  PubMed Central  Google Scholar 

  90. Crippa S, Partelli S, Bassi C, Berardi R, Capelli P, Scarpa A, et al. Long-term outcomes and prognostic factors in neuroendocrine carcinomas of the pancreas: morphology matters. Surgery. 2016;159(3):862–71.

    Article  PubMed  Google Scholar 

  91. Haugvik S-P, Janson ET, Osterlund P, Langer SW, Falk RS, Labori KJ, et al. Surgical treatment as a principle for patients with high-grade pancreatic neuroendocrine carcinoma: a nordic multicenter comparative study. Ann Surg Oncol. 2016;23(5):1721–8.

    Article  PubMed  Google Scholar 

  92. Merola E, Rinke A, Partelli S, Gress TM, Andreasi V, Kollár A, et al. Surgery with radical intent: is there an indication for G3 neuroendocrine neoplasms? Ann Surg Oncol. 2019; https://doi.org/10.1245/s10434-019-08049-5.

  93. Yoshida T, Hijioka S, Hosoda W, Ueno M, Furukawa M, Kobayashi N, et al. Surgery for pancreatic neuroendocrine tumor G3 and carcinoma G3 should be considered separately. Ann Surg Oncol. 2019; https://doi.org/10.1245/s10434-019-07252-8.

  94. Merola E, Falconi M, Rinke A, Staettner S, Krendl F, Partelli S, et al. Radical intended surgery for highly selected stage IV neuroendocrine neoplasms G3. Am J Surg. 2020; https://doi.org/10.1016/j.amjsurg.2020.03.009.

  95. Pavel M, O’Toole D, Costa F, Capdevila J, Gross D, Kianmanesh R, et al. ENETS consensus guidelines update for the management of distant metastatic disease of intestinal, pancreatic, bronchial neuroendocrine neoplasms (NEN) and NEN of unknown primary site. Neuroendocrinology. 2016;103(2):172–85.

    Article  CAS  PubMed  Google Scholar 

  96. Frilling A, Li J, Malamutmann E, Schmid K-W, Bockisch A, Broelsch CE. Treatment of liver metastases from neuroendocrine tumours in relation to the extent of hepatic disease. Br J Surg. 2009;96(2):175–84.

    Article  CAS  PubMed  Google Scholar 

  97. Partelli S, Inama M, Rinke A, Begum N, Valente R, Fendrich V, et al. Long-term outcomes of surgical management of pancreatic neuroendocrine tumors with synchronous liver metastases. Neuroendocrinology. 2015;102(1–2):68–76.

    Article  CAS  PubMed  Google Scholar 

  98. Frilling A, Modlin IM, Kidd M, Russell C, Breitenstein S, Salem R, et al. Recommendations for management of patients with neuroendocrine liver metastases. Lancet Oncol. 2014;15(1):e8–21.

    Article  PubMed  Google Scholar 

  99. Kianmanesh R, Sauvanet A, Hentic O, Couvelard A, Levy P, Vilgrain V, et al. Two-step surgery for synchronous bilobar liver metastases from digestive endocrine tumors: a safe approach for radical resection. Ann Surg. 2008;247(4):659–65.

    Article  PubMed  Google Scholar 

  100. Partelli S, Cirocchi R, Rancoita PMV, Muffatti F, Andreasi V, Crippa S, et al. A systematic review and meta-analysis on the role of palliative primary resection for pancreatic neuroendocrine neoplasm with liver metastases. HPB. 2018;20(3):197–203. https://doi.org/10.1016/j.hpb.2017.10.014.

    Article  PubMed  Google Scholar 

  101. Tierney JF, Chivukula SV, Wang X, Pappas SG, Schadde E, Hertl M, et al. Resection of primary tumor may prolong survival in metastatic gastroenteropancreatic neuroendocrine tumors. Surgery. 2019;165(3):644–51.

    Article  PubMed  Google Scholar 

  102. Ye H, Xu HL, Shen Q, Zheng Q, Chen P. Palliative resection of primary tumor in metastatic nonfunctioning pancreatic neuroendocrine tumors. J Surg Res. 2019;243:578–87.

    Article  CAS  PubMed  Google Scholar 

  103. Bertani E, Fazio N, Radice D, Zardini C, Grana C, Bodei L, et al. Resection of the primary tumor followed by peptide receptor radionuclide therapy as upfront strategy for the treatment of G1–G2 pancreatic neuroendocrine tumors with unresectable liver metastases. Ann Surg Oncol. 2016; https://doi.org/10.1245/s10434-016-5550-3.

  104. Mayo SC, de Jong MC, Pulitano C, Clary BM, Reddy SK, Gamblin TC, et al. Surgical management of hepatic neuroendocrine tumor metastasis: results from an international multi-institutional analysis. Ann Surg Oncol. 2010;17(12):3129–36.

    Article  PubMed  Google Scholar 

  105. Sarmiento JM, Heywood G, Rubin J, Ilstrup DM, Nagorney DM, Que FG. Surgical treatment of neuroendocrine metastases to the liver: a plea for resection to increase survival. J Am Coll Surg. 2003;197(1):29–37.

    Article  PubMed  Google Scholar 

  106. McEntee GP, Nagorney DM, Kvols LK, Moertel CG, Grant CS. Cytoreductive hepatic surgery for neuroendocrine tumors. Surgery. 1990;108(6):1091–6.

    CAS  PubMed  Google Scholar 

  107. Maxwell JE, Sherman SK, O’Dorisio TM, Bellizzi AM, Howe JR. Liver-directed surgery of neuroendocrine metastases: what is the optimal strategy? Surgery. 2016;159(1):320–33.

    Article  PubMed  Google Scholar 

  108. Morgan RE, Pommier SJ, Pommier RF. Expanded criteria for debulking of liver metastasis also apply to pancreatic neuroendocrine tumors. Surgery. 2018;163(1):218–25.

    Article  PubMed  Google Scholar 

  109. Al-Toubah T, Partelli S, Cives M, Andreasi V, Silvestris F, Falconi M, et al. Local treatment for focal progression in metastatic neuroendocrine tumors. Endocr Relat Cancer. 2018; https://doi.org/10.1530/ERC-18-0462.

  110. Moris D, Tsilimigras DI, Ntanasis-Stathopoulos I, Beal EW, Felekouras E, Vernadakis S, et al. Liver transplantation in patients with liver metastases from neuroendocrine tumors: a systematic review. Surgery. 2017;162(3):525–36.

    Article  PubMed  Google Scholar 

  111. Mazzaferro V, Pulvirenti A, Coppa J. Neuroendocrine tumors metastatic to the liver: how to select patients for liver transplantation? J Hepatol. 2007;47(4):460–6.

    Article  PubMed  Google Scholar 

  112. Mazzaferro V, Sposito C, Coppa J, Miceli R, Bhoori S, Bongini M, et al. The long-term benefit of liver transplantation for hepatic metastases from neuroendocrine tumors. Am J Transplant. 2016;16(10):2892–902.

    Article  CAS  PubMed  Google Scholar 

  113. Le Treut YP, Gregoire E, Klempnauer J, Belghiti J, Jouve E, Lerut J, et al. Liver transplantation for neuroendocrine tumors in Europe-results and trends in patient selection: a 213-case European liver transplant registry study. Ann Surg. 2013;257(5):807–15.

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors are grateful to Gioja Bianca Costanza Fund for supporting the PhD Scholarship of Dr. Valentina Andreasi and the Research Fellowship of Dr. Francesca Muffatti. Authors thank the ERN EURACAN initiative.

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Authors and Affiliations

  1. Pancreatic Surgery Unit, Pancreas Translational & Clinical Research Center, San Raffaele Hospital Neuroendocrine Tumor Group (ENETS Center of Excellence), Vita-Salute San Raffaele University, IRCCS San Raffaele Scientific Institute, Milan, Italy

    Valentina Andreasi, Stefano Partelli, Francesca Muffatti & Massimo Falconi

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  1. Valentina Andreasi
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  2. Stefano Partelli
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  3. Francesca Muffatti
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  4. Massimo Falconi
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Corresponding author

Correspondence to Massimo Falconi .

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Editors and Affiliations

  1. Oncology Unit, Humanitas Gavazzeni, Bergamo, Italy

    Giordano Beretta

  2. ASST-Spedali Civili, University of Brescia, BRESCIA, Brescia, Italy

    Alfredo Berruti

  3. Nuclear Medicine, Humanitas Gavazzeni, BERGAMO, Bergamo, Italy

    Emilio Bombardieri

  4. GIT Med Oncology & Neuroendocrine Tumors, European Institute of Oncology, Milan, Italy

    Nicola Fazio

  5. General Surgery Unit, Humanitas Gavazzeni, Bergamo, Italy

    Orlando Goletti

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Andreasi, V., Partelli, S., Muffatti, F., Falconi, M. (2021). New Surgical Strategies. In: Beretta, G., Berruti, A., Bombardieri, E., Fazio, N., Goletti, O. (eds) Neuroendocrine Neoplasia Management. Springer, Cham. https://doi.org/10.1007/978-3-030-72830-4_8

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