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Gastric Neuroendocrine Tumors

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Neuroendocrine Neoplasia Management

Abstract

Gastric neuroendocrine tumors are diagnosed increasingly often and classified into three types with important differences in terms of behavior, therapeutic approach, and prognosis. They are non-functioning, well-differentiated neoplasms with a low to moderate proliferation index. Generally slow-growing and indolent, they can be very aggressive. The risk of metastatic spread correlates with size, infiltration beyond the submucosa, proliferative activity, and the presence of lympho-angioinvasion.

Type I and II arise in the context of hypergastrinemia. The former are associated with chronic atrophic gastritis, the latter with Zollinger–Ellison syndrome in multiple endocrine neoplasia type 1. Usually small and multiple, they are mostly successfully managed by endoscopic resection, reserving surgery for those with muscularis propria invasion or metastatic spread. Type I may respond to somatostatin analogs and to Netazepide, a competitive gastrin/cholecystokinin 2 receptor antagonist. They require a regular endoscopic surveillance because of recurring and because of the increased risk of adenocarcinoma development in gastric atrophy.

Type III are sporadic, frequently metastatic at diagnosis and with the worst prognosis. Surgical resection is the treatment of choice although endoscopic resection may be considered for small and superficial lesions.

Treatment options for advanced lesions include somatostatin analogs, chemotherapy, molecular targeted agents, locoregional therapies, peptide-receptor radionuclide therapy, and surgery.

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References

  1. WHO Classification of Tumours. Digestive system tumours, vol. 1. 5th ed. Lyon: IARC; 2019.

    Google Scholar 

  2. Bierley J, Gospodarowicz MK, Wittekind C, International Union Against Cancer. TNM classification of malignant tumours. 8th ed. Oxford; Hoboken, NJ: Wiley-Blackwell; 2017.

    Google Scholar 

  3. Modlin IM, Oberg K, Chung DC, Jensen RT, de Herder WW, Thakker RV, Caplin M, Delle Fave G, Kaltsas GA, Krenning EP, Moss SF, Nilsson O, Rindi G, Salazar R, Ruszniewski P, Sundin A. Gastroenteropancreatic neuroendocrine tumours. Lancet Oncol. 2008;9(1):61–72. https://doi.org/10.1016/S1470-2045(07)70410-2.

    Article  CAS  PubMed  Google Scholar 

  4. Kaltsas GA, Besser GM, Grossman AB. The diagnosis and medical management of advanced neuroendocrine tumors. Endocr Rev. 2004;25(3):458–511. https://doi.org/10.1210/er.2003-0014.

    Article  CAS  PubMed  Google Scholar 

  5. Kidd M, Gustafsson B, Modlin IM. Gastric carcinoids (neuroendocrine neoplasms). Gastroenterol Clin North Am. 2013;42(2):381–97. https://doi.org/10.1016/j.gtc.2013.01.009.

    Article  PubMed  Google Scholar 

  6. Kaltsas G, Grozinsky-Glasberg S, Alexandraki KI, Thomas D, Tsolakis AV, Gross D, Grossman AB. Current concepts in the diagnosis and management of type 1 gastric neuroendocrine neoplasms. Clin Endocrinol (Oxf). 2014;81(2):157–68. https://doi.org/10.1111/cen.12476.

    Article  Google Scholar 

  7. O’Connor JM, Marmissolle F, Bestani C, Pesce V, Belli S, Dominichini E, Mendez G, Price P, Giacomi N, Pairola A, Loria FS, Huertas E, Martin C, Patane K, Poleri C, Rosenberg M, Cabanne A, Kujaruk M, Caino A, Zamora V, Mariani J, Dioca M, Parma P, Podesta G, Andriani O, Gondolesi G, Roca E. Observational study of patients with gastroenteropancreatic and bronchial neuroendocrine tumors in Argentina: Results from the large database of a multidisciplinary group clinical multicenter study. Mol Clin Oncol. 2014;2(5):673–84. https://doi.org/10.3892/mco.2014.332.

    Article  PubMed  PubMed Central  Google Scholar 

  8. 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. https://doi.org/10.1002/cncr.29099.

    Article  PubMed  Google Scholar 

  9. Yao JC, Hassan M, Phan A, Dagohoy C, Leary C, Mares JE, Abdalla EK, Fleming JB, Vauthey JN, Rashid A, Evans DB. 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. https://doi.org/10.1200/JCO.2007.15.4377.

    Article  PubMed  Google Scholar 

  10. Niederle MB, Hackl M, Kaserer K, Niederle B. Gastroenteropancreatic neuroendocrine tumours: the current incidence and staging based on the WHO and European Neuroendocrine tumour society classification: an analysis based on prospectively collected parameters. Endocr Relat Cancer. 2010;17(4):909–18. https://doi.org/10.1677/ERC-10-0152.

    Article  PubMed  Google Scholar 

  11. Modlin IM, Lye KD, Kidd M. A 50-year analysis of 562 gastric carcinoids: small tumor or larger problem? Am J Gastroenterol. 2004;99(1):23–32. https://doi.org/10.1046/j.1572-0241.2003.04027.x.

    Article  PubMed  Google Scholar 

  12. Dasari A, Shen C, Halperin D, Zhao B, Zhou S, Xu Y, Shih T, Yao JC. Trends in the incidence, prevalence, and survival outcomes in patients with Neuroendocrine tumors in the United States. JAMA Oncol. 2017;3(10):1335–42. https://doi.org/10.1001/jamaoncol.2017.0589.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Assarzadegan N, Montgomery E. What is new in 2019 World Health Organization (WHO) classification of tumors of the digestive system: review of selected updates on neuroendocrine neoplasms, appendiceal tumors, and molecular testing. Arch Pathol Lab Med. 2020. https://doi.org/10.5858/arpa.2019-0665-RA.

  14. Grozinsky-Glasberg S, Thomas D, Strosberg JR, Pape UF, Felder S, Tsolakis AV, Alexandraki KI, Fraenkel M, Saiegh L, Reissman P, Kaltsas G, Gross DJ. Metastatic type 1 gastric carcinoid: a real threat or just a myth? World J Gastroenterol. 2013;19(46):8687–95. https://doi.org/10.3748/wjg.v19.i46.8687.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. 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. https://doi.org/10.3748/wjg.v25.i35.5376.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Spampatti MP, Massironi S, Rossi RE, Conte D, Sciola V, Ciafardini C, Ferrero S, Lodi L, Peracchi M. Unusually aggressive type 1 gastric carcinoid: a case report with a review of the literature. Eur J Gastroenterol Hepatol. 2012;24(5):589–93. https://doi.org/10.1097/MEG.0b013e328350fae8.

    Article  PubMed  Google Scholar 

  17. Rindi G, Luinetti O, Cornaggia M, Capella C, Solcia E. Three subtypes of gastric argyrophil carcinoid and the gastric neuroendocrine carcinoma: a clinicopathologic study. Gastroenterology. 1993;104(4):994–1006. https://doi.org/10.1016/0016-5085(93)90266-f.

    Article  CAS  PubMed  Google Scholar 

  18. Grozinsky-Glasberg S, Alexandraki KI, Angelousi A, Chatzellis E, Sougioultzis S, Kaltsas G. Gastric carcinoids. Endocrinol Metab Clin North Am. 2018;47(3):645–60. https://doi.org/10.1016/j.ecl.2018.04.013.

    Article  PubMed  Google Scholar 

  19. Vannella L, Sbrozzi-Vanni A, Lahner E, Bordi C, Pilozzi E, Corleto VD, Osborn JF, Delle Fave G, Annibale B. Development of type I gastric carcinoid in patients with chronic atrophic gastritis. Aliment Pharmacol Ther. 2011;33(12):1361–9. https://doi.org/10.1111/j.1365-2036.2011.04659.x.

    Article  CAS  PubMed  Google Scholar 

  20. Dias AR, Azevedo BC, Alban LBV, Yagi OK, Ramos MFKP, Jacob CE, Barchi LC, Cecconello I, Ribeiro U Jr, Zilberstein B. Gastric neuroendocrine tumor: review and update. Arq Bras Cir Dig. 2017;30(2):150–4. https://doi.org/10.1590/0102-6720201700020016.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Cadiot G, Lehy T, Mignon M. Gastric endocrine cell proliferation and fundic argyrophil carcinoid tumors in patients with the Zollinger-Ellison syndrome. Acta Oncol. 1993;32(2):135–40. https://doi.org/10.3109/02841869309083902.

    Article  CAS  PubMed  Google Scholar 

  22. Norton JA, Melcher ML, Gibril F, Jensen RT. Gastric carcinoid tumors in multiple endocrine neoplasia-1 patients with Zollinger-Ellison syndrome can be symptomatic, demonstrate aggressive growth, and require surgical treatment. Surgery. 2004;136(6):1267–74. https://doi.org/10.1016/j.surg.2004.06.057.

    Article  PubMed  Google Scholar 

  23. Gibril F, Schumann M, Pace A, Jensen RT. Multiple endocrine neoplasia type 1 and Zollinger-Ellison syndrome: a prospective study of 107 cases and comparison with 1009 cases from the literature. Medicine (Baltimore). 2004;83(1):43–83. Erratum in: Medicine (Baltimore). 2004 May;83(3):175. https://doi.org/10.1097/01.md.0000112297.72510.32.

    Article  Google Scholar 

  24. Cadiot G, Vissuzaine C, Potet F, Mignon M. Fundic argyrophil carcinoid tumor in a patient with sporadic-type Zollinger-Ellison syndrome. Dig Dis Sci. 1995;40(6):1275–8. https://doi.org/10.1007/BF02065537.

    Article  CAS  PubMed  Google Scholar 

  25. Cavalcoli F, Zilli A, Conte D, Ciafardini C, Massironi S. Gastric neuroendocrine neoplasms and proton pump inhibitors: fact or coincidence? Scand J Gastroenterol. 2015;50(11):1397–403. https://doi.org/10.3109/00365521.2015.1054426.

    Article  CAS  PubMed  Google Scholar 

  26. Rindi G, Bordi C, Rappel S, La Rosa S, Stolte M, Solcia E. Gastric carcinoids and neuroendocrine carcinomas: pathogenesis, pathology, and behavior. World J Surg. 1996;20(2):168–72. https://doi.org/10.1007/s002689900026.

    Article  CAS  PubMed  Google Scholar 

  27. Bordi C, D’Adda T, Azzoni C, Canavese G, Brandi ML. Gastrointestinal endocrine tumors: recent developments. Endocr Pathol. 1998;9:99–115. https://doi.org/10.1007/BF02782603.

    Article  Google Scholar 

  28. Basuroy R, Srirajaskanthan R, Prachalias A, Quaglia A, Ramage JK. Review article: the investigation and management of gastric neuroendocrine tumours. Aliment Pharmacol Ther. 2014;39(10):1071–84. https://doi.org/10.1111/apt.12698.

    Article  CAS  PubMed  Google Scholar 

  29. Scherübl H, Cadiot G, Jensen RT, Rösch T, Stölzel U, Klöppel G. Neuroendocrine tumors of the stomach (gastric carcinoids) are on the rise: small tumors, small problems? Endoscopy. 2010;42(8):664–71. https://doi.org/10.1055/s-0030-1255564.

    Article  PubMed  Google Scholar 

  30. Rindi G, Azzoni C, La Rosa S, Klersy C, Paolotti D, Rappel S, Stolte M, Capella C, Bordi C, Solcia E. ECL cell tumor and poorly differentiated endocrine carcinoma of the stomach: prognostic evaluation by pathological analysis. Gastroenterology. 1999;116(3):532–42. https://doi.org/10.1016/s0016-5085(99)70174-5.

    Article  CAS  PubMed  Google Scholar 

  31. La Rosa S, Vanoli A. Gastric neuroendocrine neoplasms and related precursor lesions. J Clin Pathol. 2014;67(11):938–48. https://doi.org/10.1136/jclinpath-2014-202515.

    Article  PubMed  Google Scholar 

  32. Li TT, Qiu F, Qian ZR, Wan J, Qi XK, Wu BY. Classification, clinicopathologic features and treatment of gastric neuroendocrine tumors. World J Gastroenterol. 2014;20(1):118–25. https://doi.org/10.3748/wjg.v20.i1.118.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Sato Y, Iwafuchi M, Ueki J, Yoshimura A, Mochizuki T, Motoyama H, Sugimura K, Honma T, Narisawa R, Ichida T, Asakura H, Van Thiel DH. Gastric carcinoid tumors without autoimmune gastritis in Japan: a relationship with helicobacter pylori infection. Dig Dis Sci. 2002;47(3):579–85. https://doi.org/10.1023/a:1017972204219.

    Article  PubMed  Google Scholar 

  34. Modlin IM, Lye KD, Kidd M. Carcinoid tumors of the stomach. Surg Oncol. 2003;12(2):153–72. https://doi.org/10.1016/s0960-7404(03)00034-3.

    Article  PubMed  Google Scholar 

  35. Delle Fave G, Kwekkeboom DJ, Van Cutsem E, Rindi G, Kos-Kudla B, Knigge U, Sasano H, Tomassetti P, Salazar R, Ruszniewski P, Barcelona Consensus Conference Participants. ENETS consensus guidelines for the management of patients with gastroduodenal neoplasms. Neuroendocrinology. 2012;95(2):74–87. https://doi.org/10.1159/000335595.

    Article  CAS  PubMed  Google Scholar 

  36. Borch K, Renvall H, Liedberg G. Gastric endocrine cell hyperplasia and carcinoid tumors in pernicious anemia. Gastroenterology. 1985;88(3):638–48. https://doi.org/10.1016/0016-5085(85)90131-3.

    Article  CAS  PubMed  Google Scholar 

  37. Stockbrügger RW, Menon GG, Beilby JO, Mason RR, Cotton PB. Gastroscopic screening in 80 patients with pernicious anaemia. Gut. 1983;24(12):1141–7. https://doi.org/10.1136/gut.24.12.1141.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Thomas RM, Baybick JH, Elsayed AM, Sobin LH. Gastric carcinoids. An immunohistochemical and clinicopathologic study of 104 patients. Cancer. 1994;73(8):2053–8. https://doi.org/10.1002/1097-0142(19940415)73:8<2053::aid-cncr2820730807>3.0.co;2-0.

    Article  CAS  PubMed  Google Scholar 

  39. Marignani M, Delle Fave G, Mecarocci S, Bordi C, Angeletti S, D'Ambra G, Aprile MR, Corleto VD, Monarca B, Annibale B. High prevalence of atrophic body gastritis in patients with unexplained microcytic and macrocytic anemia: a prospective screening study. Am J Gastroenterol. 1999;94(3):766–72. https://doi.org/10.1111/j.1572-0241.1999.00949.x.

    Article  CAS  PubMed  Google Scholar 

  40. Sato Y. Endoscopic diagnosis and management of type I neuroendocrine tumors. World J Gastrointest Endosc. 2015;7(4):346–53. https://doi.org/10.4253/wjge.v7.i4.346.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Merola E, Sbrozzi-Vanni A, Panzuto F, D’Ambra G, Di Giulio E, Pilozzi E, Capurso G, Lahner E, Bordi C, Annibale B, Delle FG. Type I gastric carcinoids: a prospective study on endoscopic management and recurrence rate. Neuroendocrinology. 2012;95(3):207–13. https://doi.org/10.1159/000329043.

    Article  CAS  PubMed  Google Scholar 

  42. Chin JL, O’Toole D. Diagnosis and management of upper gastrointestinal neuroendocrine tumors. Clin Endosc. 2017;50(6):520–9. https://doi.org/10.5946/ce.2017.181.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Crosby DA, Donohoe CL, Fitzgerald L, Muldoon C, Hayes B, O’Toole D, Reynolds JV. Gastric neuroendocrine tumours. Dig Surg. 2012;29(4):331–48. https://doi.org/10.1159/000342988.

    Article  PubMed  Google Scholar 

  44. Ito T, Igarashi H, Jensen RT. Zollinger-Ellison syndrome: recent advances and controversies. Curr Opin Gastroenterol. 2013;29(6):650–61. https://doi.org/10.1097/MOG.0b013e328365efb1.

    Article  PubMed  PubMed Central  Google Scholar 

  45. O'Toole D, Delle Fave G, Jensen RT. Gastric and duodenal neuroendocrine tumours. Best Pract Res Clin Gastroenterol. 2012;26(6):719–35. https://doi.org/10.1016/j.bpg.2013.01.002.

    Article  CAS  PubMed  Google Scholar 

  46. Borch K, Ahrén B, Ahlman H, Falkmer S, Granérus G, Grimelius L. Gastric carcinoids: biologic behavior and prognosis after differentiated treatment in relation to type. Ann Surg. 2005;242(1):64–73. https://doi.org/10.1097/01.sla.0000167862.52309.7d.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Attili F, Capurso G, Vanella G, Fuccio L, Delle Fave G, Costamagna G, Larghi A. Diagnostic and therapeutic role of endoscopy in gastroenteropancreatic neuroendocrine neoplasms. Dig Liver Dis. 2014;46(1):9–17. https://doi.org/10.1016/j.dld.2013.04.007.

    Article  PubMed  Google Scholar 

  48. Delle Fave G, O'Toole D, Sundin A, Taal B, Ferolla P, Ramage JK, Ferone D, Ito T, Weber W, Zheng-Pei Z, De Herder WW, Pascher A, Ruszniewski P, Vienna Consensus Conference Participants. ENETS consensus guidelines update for gastroduodenal neuroendocrine neoplasms. Neuroendocrinology. 2016;103(2):119–24. https://doi.org/10.1159/000443168.

    Article  CAS  PubMed  Google Scholar 

  49. de Mestier L, Lepage C, Baudin E, Coriat R, Courbon F, Couvelard A, Do Cao C, Frampas E, Gaujoux S, Gincul R, Goudet P, Lombard-Bohas C, Poncet G, Smith D, Ruszniewski P, Lecomte T, Bouché O, Walter T, Cadiot G, Thésaurus National de Cancérologie Digestive (TNCD). Digestive Neuroendocrine Neoplasms (NEN): French Intergroup clinical practice guidelines for diagnosis, treatment and follow-up (SNFGE, GTE, RENATEN, TENPATH, FFCD, GERCOR, UNICANCER, SFCD, SFED, SFRO, SFR). Dig Liver Dis. 2020;52(5):473–92. https://doi.org/10.1016/j.dld.2020.02.011.

    Article  PubMed  Google Scholar 

  50. Zilli A, Arcidiacono PG, Conte D, Massironi S. Clinical impact of endoscopic ultrasonography on the management of neuroendocrine tumors: lights and shadows. Dig Liver Dis. 2018;50(1):6–14. https://doi.org/10.1016/j.dld.2017.10.007.

    Article  PubMed  Google Scholar 

  51. Bahri H, Laurence L, Edeline J, Leghzali H, Devillers A, Raoul JL, Cuggia M, Mesbah H, Clement B, Boucher E, Garin E. High prognostic value of 18F-FDG PET for metastatic gastroenteropancreatic neuroendocrine tumors: a long-term evaluation. J Nucl Med. 2014;55(11):1786–90. https://doi.org/10.2967/jnumed.114.144386.

    Article  CAS  PubMed  Google Scholar 

  52. Singh Ospina N, Donegan D, Rodriguez-Gutierrez R, Al-Hilli Z, Young WF Jr. Assessing for multiple endocrine Neoplasia type 1 in patients evaluated for Zollinger-Ellison syndrome-clues to a safer diagnostic process. Am J Med. 2017;130(5):603–5. https://doi.org/10.1016/j.amjmed.2016.11.035.

    Article  PubMed  Google Scholar 

  53. Poitras P, Gingras MH, Rehfeld JF. The Zollinger-Ellison syndrome: dangers and consequences of interrupting antisecretory treatment. Clin Gastroenterol Hepatol. 2012;10(2):199–202. https://doi.org/10.1016/j.cgh.2011.08.012.

    Article  PubMed  Google Scholar 

  54. Oberg K, Couvelard A, Delle Fave G, Gross D, Grossman A, Jensen RT, Pape UF, Perren A, Rindi G, Ruszniewski P, Scoazec JY, Welin S, Wiedenmann B, Ferone D, Antibes Consensus Conference Participants. ENETS consensus guidelines for standard of care in neuroendocrine tumours: biochemical markers. Neuroendocrinology. 2017;105(3):201–11. https://doi.org/10.1159/000472254.

    Article  CAS  PubMed  Google Scholar 

  55. Vezzosi D, Walter T, Laplanche A, Raoul JL, Dromain C, Ruszniewski P, d’Herbomez M, Guigay J, Mitry E, Cadiot G, Leboulleux S, Lombard-Bohas C, Borson-Chazot F, Ducreux M, Baudin E. Chromogranin a measurement in metastatic well-differentiated gastroenteropancreatic neuroendocrine carcinoma: screening for false positives and a prospective follow-up study. Int J Biol Markers. 2011;26(2):94–101. https://doi.org/10.5301/JBM.2011.8327.

    Article  CAS  PubMed  Google Scholar 

  56. Korse CM, Muller M, Taal BG. Discontinuation of proton pump inhibitors during assessment of chromogranin a levels in patients with neuroendocrine tumours. Br J Cancer. 2011;105(8):1173–5. https://doi.org/10.1038/bjc.2011.380.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Lahner E, Zagari RM, Zullo A, Di Sabatino A, Meggio A, Cesaro P, Lenti MV, Annibale B, Corazza GR. Chronic atrophic gastritis: natural history, diagnosis and therapeutic management. A position paper by the Italian Society of Hospital Gastroenterologists and Digestive Endoscopists [AIGO], the Italian Society of Digestive Endoscopy [SIED], the Italian Society of Gastroenterology [SIGE], and the Italian Society of Internal Medicine [SIMI]. Dig Liver Dis. 2019;51(12):1621–32. https://doi.org/10.1016/j.dld.2019.09.016.

    Article  PubMed  Google Scholar 

  58. Ravizza D, Fiori G, Trovato C, Fazio N, Bonomo G, Luca F, Bodei L, Pelosi G, Tamayo D, Crosta C. Long-term endoscopic and clinical follow-up of untreated type 1 gastric neuroendocrine tumours. Dig Liver Dis. 2007;39(6):537–43. https://doi.org/10.1016/j.dld.2007.01.018.

    Article  CAS  PubMed  Google Scholar 

  59. Uygun A, Kadayifci A, Polat Z, Yilmaz K, Gunal A, Demir H, Bagci S. Long-term results of endoscopic resection for type I gastric neuroendocrine tumors. J Surg Oncol. 2014;109(2):71–4. https://doi.org/10.1002/jso.23477.

    Article  PubMed  Google Scholar 

  60. Chen WF, Zhou PH, Li QL, Xu MD, Yao LQ. Clinical impact of endoscopic submucosal dissection for gastric neuroendocrine tumors: a retrospective study from mainland China. Sci World J. 2012;2012:869769. https://doi.org/10.1100/2012/869769.

    Article  Google Scholar 

  61. Kim HH, Kim GH, Kim JH, Choi MG, 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. https://doi.org/10.1155/2014/253860.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Sato Y, Takeuchi M, Hashimoto S, Mizuno K, Kobayashi M, Iwafuchi M, Narisawa R, Aoyagi Y. Usefulness of endoscopic submucosal dissection for type I gastric carcinoid tumors compared with endoscopic mucosal resection. Hepatogastroenterology. 2013;60(126):1524–9. https://doi.org/10.5754/hge121185.

    Article  PubMed  Google Scholar 

  63. Zhou X, Xie H, Xie L, Li J, Cao W, Fu W. Endoscopic resection therapies for rectal neuroendocrine tumors: a systematic review and meta-analysis. J Gastroenterol Hepatol. 2014;29(2):259–68. https://doi.org/10.1111/jgh.12395.

    Article  PubMed  Google Scholar 

  64. Jeon SM, Lee JH, Hong SP, Kim TI, Kim WH, Cheon JH. Feasibility of salvage endoscopic mucosal resection by using a cap for remnant rectal carcinoids after primary EMR. Gastrointest Endosc. 2011;73(5):1009–14. https://doi.org/10.1016/j.gie.2010.12.029.

    Article  PubMed  Google Scholar 

  65. Meier B, Schmidt A, Glaser N, Meining A, Walter B, Wannhoff A, Riecken B, Caca K. Endoscopic full-thickness resection of gastric subepithelial tumors with the gFTRD-system: a prospective pilot study (RESET trial). Surg Endosc. 2020;34(2):853–60. https://doi.org/10.1007/s00464-019-06839-2.

    Article  PubMed  Google Scholar 

  66. Chen WC, Warner RR, Ward SC, Harpaz N, Divino CM, Itzkowitz SH, Kim MK. Management and disease outcome of type I gastric neuroendocrine tumors: the Mount Sinai experience. Dig Dis Sci. 2015;60(4):996–1003. https://doi.org/10.1007/s10620-014-3410-1.

    Article  CAS  PubMed  Google Scholar 

  67. Pimentel-Nunes P, Libânio D, Marcos-Pinto R, Areia M, Leja M, Esposito G, Garrido M, Kikuste I, Megraud F, Matysiak-Budnik T, Annibale B, Dumonceau JM, Barros R, Fléjou JF, Carneiro F, van Hooft JE, Kuipers EJ, Dinis-Ribeiro M. Management of epithelial precancerous conditions and lesions in the stomach (MAPS II): European Society of Gastrointestinal Endoscopy (ESGE), European Helicobacter and Microbiota Study Group (EHMSG), European Society of Pathology (ESP), and Sociedade Portuguesa de Endoscopia Digestiva (SPED) guideline update 2019. Endoscopy. 2019;51(4):365–88. https://doi.org/10.1055/a-0859-1883.

    Article  PubMed  Google Scholar 

  68. Jenny HE, Ogando PA, Fujitani K, Warner RR, Divino CM. Laparoscopic antrectomy: a safe and definitive treatment in managing type 1 gastric carcinoids. Am J Surg. 2016;211(4):778–82. https://doi.org/10.1016/j.amjsurg.2015.08.040.

    Article  PubMed  Google Scholar 

  69. Gladdy RA, Strong VE, Coit D, Allen PJ, Gerdes H, Shia J, Klimstra DS, Brennan MF, Tang LH. Defining surgical indications for type I gastric carcinoid tumor. Ann Surg Oncol. 2009;16(11):3154–60. https://doi.org/10.1245/s10434-009-0687-y.

    Article  PubMed  Google Scholar 

  70. Eriksson B, Oberg K. Summing up 15 years of somatostatin analog therapy in neuroendocrine tumors: future outlook. Ann Oncol. 1999;10(Suppl 2):S31–8. https://doi.org/10.1093/annonc/10.suppl_2.s31.

    Article  PubMed  Google Scholar 

  71. Massironi S, Zilli A, Fanetti I, Ciafardini C, Conte D, Peracchi M. Intermittent treatment of recurrent type-1 gastric carcinoids with somatostatin analogues in patients with chronic autoimmune atrophic gastritis. Dig Liver Dis. 2015;47(11):978–83. https://doi.org/10.1016/j.dld.2015.07.155.

    Article  CAS  PubMed  Google Scholar 

  72. Grozinsky-Glasberg S, Kaltsas G, Gur C, Gal E, Thomas D, Fichman S, Alexandraki K, Barak D, Glaser B, Shimon I, Gross DJ. Long-acting somatostatin analogues are an effective treatment for type 1 gastric carcinoid tumours. Eur J Endocrinol. 2008;159(4):475–82. https://doi.org/10.1530/EJE-08-0420.

    Article  CAS  PubMed  Google Scholar 

  73. Campana D, Nori F, Pezzilli R, Piscitelli L, Santini D, Brocchi E, Corinaldesi R, Tomassetti P. Gastric endocrine tumors type I: treatment with long-acting somatostatin analogs. Endocr Relat Cancer. 2008;15(1):337–42. https://doi.org/10.1677/ERC-07-0251.

    Article  CAS  PubMed  Google Scholar 

  74. Jianu CS, Fossmark R, Syversen U, Hauso Ø, Fykse V, Waldum HL. Five-year follow-up of patients treated for 1 year with octreotide long-acting release for enterochromaffin-like cell carcinoids. Scand J Gastroenterol. 2011;46(4):456–63. https://doi.org/10.3109/00365521.2010.539255.

    Article  PubMed  Google Scholar 

  75. Khuroo MS, Khuroo MS, Khuroo NS. Treatment of type I gastric neuroendocrine tumors with somatostatin analogs. J Gastroenterol Hepatol. 2010;25(3):548–54. https://doi.org/10.1111/j.1440-1746.2009.06131.x.

    Article  CAS  PubMed  Google Scholar 

  76. Thomas D, Tsolakis AV, Grozinsky-Glasberg S, Fraenkel M, Alexandraki K, Sougioultzis S, Gross DJ, Kaltsas G. Long-term follow-up of a large series of patients with type 1 gastric carcinoid tumors: data from a multicenter study. Eur J Endocrinol. 2013;168(2):185–93. https://doi.org/10.1530/EJE-12-0836.

    Article  CAS  PubMed  Google Scholar 

  77. Fossmark R, Sørdal Ø, Jianu CS, Qvigstad G, Nordrum IS, Boyce M, Waldum HL. Treatment of gastric carcinoids type 1 with the gastrin receptor antagonist netazepide (YF476) results in regression of tumours and normalisation of serum chromogranin a. Aliment Pharmacol Ther. 2012;36(11–12):1067–75. https://doi.org/10.1111/apt.12090.

    Article  CAS  PubMed  Google Scholar 

  78. Moore AR, Boyce M, Steele IA, Campbell F, Varro A, Pritchard DM. Netazepide, a gastrin receptor antagonist, normalises tumour biomarkers and causes regression of type 1 gastric neuroendocrine tumours in a nonrandomised trial of patients with chronic atrophic gastritis. PLoS One. 2013;8(10):e76462. https://doi.org/10.1371/journal.pone.0076462.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Boyce M, Moore AR, Sagatun L, Parsons BN, Varro A, Campbell F, Fossmark R, Waldum HL, Pritchard DM. Netazepide, a gastrin/cholecystokinin-2 receptor antagonist, can eradicate gastric neuroendocrine tumours in patients with autoimmune chronic atrophic gastritis. Br J Clin Pharmacol. 2017;83(3):466–75. https://doi.org/10.1111/bcp.13146.

    Article  CAS  PubMed  Google Scholar 

  80. 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. https://doi.org/10.1056/NEJM200008243430805.

    Article  CAS  PubMed  Google Scholar 

  81. Jensen RT, Cadiot G, Brandi ML, de Herder WW, Kaltsas G, Komminoth P, Scoazec JY, Salazar R, Sauvanet A, Kianmanesh R, Barcelona Consensus Conference Participants. ENETS consensus guidelines for the management of patients with digestive neuroendocrine neoplasms: functional pancreatic endocrine tumor syndromes. Neuroendocrinology. 2012;95(2):98–119. https://doi.org/10.1159/000335591.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Kwon YH, Jeon SW, Kim GH, Kim JI, Chung IK, Jee SR, Kim HU, Seo GS, Baik GH, Choi KD, Moon JS. Long-term follow up of endoscopic resection for type 3 gastric NET. World J Gastroenterol. 2013;19(46):8703–8. https://doi.org/10.3748/wjg.v19.i46.8703.

    Article  PubMed  PubMed Central  Google Scholar 

  83. Hirasawa T, Yamamoto N, Sano T. Is endoscopic resection appropriate for type 3 gastric neuroendocrine tumors? Retrospective multicenter study. Dig Endosc. 2020. https://doi.org/10.1111/den.13778.

  84. Ahmed M. Gastrointestinal neuroendocrine tumors in 2020. World J Gastrointest Oncol. 2020;12(8):791–807. https://doi.org/10.4251/wjgo.v12.i8.791.

    Article  PubMed  PubMed Central  Google Scholar 

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Ravizza, D., Fiori, G. (2021). Gastric Neuroendocrine Tumors. 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_13

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