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Review

Improvements and future perspective in diagnostic tools for neuroendocrine neoplasms

ORCID Icon, , , , , , , , & show all
Pages 349-366 | Received 07 Dec 2023, Accepted 30 May 2024, Published online: 05 Jun 2024

References

  • Leotlela PD, Jauch A, Holtgreve-Grez H, et al. Genetics of neuroendocrine and carcinoid tumours. Endocr Relat Cancer. 2003 Dec;10(4):437–450. doi: 10.1677/erc.0.0100437
  • Rossi RE, Massironi S. The increasing incidence of neuroendocrine neoplasms worldwide: current knowledge and open issues. J Clin Med. 2022;11(13):3794, Switzerland. doi: 10.3390/jcm11133794
  • Koffas A, Giakoustidis A, Papaefthymiou A, et al. Diagnostic work-up and advancement in the diagnosis of gastroenteropancreatic neuroendocrine neoplasms. Front Surg. 2023;10:1064145. doi: 10.3389/fsurg.2023.1064145
  • Rindi G, Mete O, Uccella S, et al. Overview of the 2022 WHO classification of neuroendocrine neoplasms. Endocr Pathol. 2022 Mar;33(1):115–154. doi: 10.1007/s12022-022-09708-2
  • Khanna L, Prasad SR, Sunnapwar A, et al. Pancreatic neuroendocrine neoplasms: 2020 update on pathologic and imaging findings and classification. Radiographics. 2020 Sep;40(5):1240–1262. doi: 10.1148/rg.2020200025
  • Chang S, Choi D, Lee SJ, et al. Neuroendocrine neoplasms of the gastrointestinal tract: classification, pathologic basis, and imaging features. Radiographics. 2007 Nov;27(6):1667–1679. doi: 10.1148/rg.276075001
  • Tamm EP, Bhosale P, Lee JH, et al. State-of-the-art Imaging of pancreatic neuroendocrine tumors. Surg Oncol Clin N Am. 2016 Apr;25(2):375–400. doi: 10.1016/j.soc.2015.11.007
  • Javadi S, Menias CO, Korivi BR, et al. Pancreatic calcifications and calcified pancreatic masses: pattern recognition approach on CT. AJR Am J Roentgenol. 2017 Jul;209(1):77–87. doi: 10.2214/AJR.17.17862
  • Lee L, Ito T, Jensen RT. Imaging of pancreatic neuroendocrine tumors: recent advances, current status, and controversies. Expert Rev Anticancer Ther. 2018 Sep;18(9):837–860. doi: 10.1080/14737140.2018.1496822
  • d’Assignies G, Fina P, Bruno O, et al. High sensitivity of diffusion-weighted MR imaging for the detection of liver metastases from neuroendocrine tumors: comparison with T2-weighted and dynamic gadolinium-enhanced MR imaging. Radiology. 2013 Aug;268(2):390–399. doi: 10.1148/radiol.13121628
  • De Robertis R, Cingarlini S, Tinazzi Martini P, et al. Pancreatic neuroendocrine neoplasms: Magnetic resonance imaging features according to grade and stage. World J Gastroenterol. [2017 Jan 14];23(2):275–285. doi: 10.3748/wjg.v23.i2.275
  • Kellock T, Tuong B, Harris AC, et al. Diagnostic imaging of primary hepatic neuroendocrine tumors: a case and discussion of the literature. Case Rep Radiol. 2014;2014:156491. doi: 10.1155/2014/156491
  • Wang LX, Liu K, Lin GW, et al. Primary hepatic neuroendocrine tumors: comparing CT and MRI features with pathology. Cancer Imaging. [2015 Aug 15];15(1):13. doi: 10.1186/s40644-015-0046-0
  • Ma H, Kan Y, Yang JG. Clinical value of (68)Ga-DOTA-SSTR PET/CT in the diagnosis and detection of neuroendocrine tumors of unknown primary origin: a systematic review and meta-analysis. Acta Radiol. 2021 Sep;62(9):1217–1228. doi: 10.1177/0284185120958412
  • Singh S, Poon R, Wong R, et al. 68Ga PET imaging in patients with neuroendocrine tumors: a systematic review and meta-analysis. Clin Nucl Med. 2018 Nov;43(11):802–810. doi: 10.1097/RLU.0000000000002276
  • Yang J, Kan Y, Ge BH, et al. Diagnostic role of Gallium-68 DOTATOC and Gallium-68 DOTATATE PET in patients with neuroendocrine tumors: a meta-analysis. Acta Radiol. 2014 May;55(4):389–398. doi: 10.1177/0284185113496679
  • Barrio M, Czernin J, Fanti S, et al. The impact of Somatostatin Receptor-Directed PET/CT on the management of patients with neuroendocrine tumor: a systematic review and meta-analysis. J Nucl Med. 2017 May;58(5):756–761. doi: 10.2967/jnumed.116.185587
  • Duan H, Baratto L, Iagaru A. The role of PET/CT in the imaging of pancreatic neoplasms. Semin Ultrasound CT MR. 2019 Dec;40(6):500–508. doi: 10.1053/j.sult.2019.04.006
  • Papadakis GZ, Karantanas AH, Marias K, et al. Current status and future prospects of PET-imaging applications in patients with gastro-entero-pancreatic neuroendocrine tumors (GEP-NETs). Eur J Radiol. 2021 Oct;143:109932. doi: 10.1016/j.ejrad.2021.109932
  • Fortunati E, Argalia G, Zanoni L, et al. New PET radiotracers for the imaging of neuroendocrine neoplasms. Curr Treat Options Oncol. 2022 May;23(5):703–720. doi: 10.1007/s11864-022-00967-z
  • Severi S, Nanni O, Bodei L, et al. Role of 18FDG PET/CT in patients treated with 177Lu-DOTATATE for advanced differentiated neuroendocrine tumours. Eur J Nucl Med Mol Imaging. 2013 Jun;40(6):881–888. doi: 10.1007/s00259-013-2369-z
  • Gao J, Xu S, Ju H, et al. The potential application of MR-derived ADCmin values from (68)Ga-DOTATATE and (18)F-FDG dual tracer PET/MR as replacements for FDG PET in assessment of grade and stage of pancreatic neuroendocrine tumors. EJNMMI Res. [2023 Feb 8];13(1):10. doi: 10.1186/s13550-023-00960-z
  • Ambrosini V, Kunikowska J, Baudin E, et al. Consensus on molecular imaging and theranostics in neuroendocrine neoplasms. Eur J Cancer. 2021 Mar;146:56–73. doi: 10.1016/j.ejca.2021.01.008
  • Bozkurt MF, Virgolini I, Balogova S, et al. Guideline for PET/CT imaging of neuroendocrine neoplasms with (68)Ga-DOTA-conjugated somatostatin receptor targeting peptides and (18)F-DOPA. Eur J Nucl Med Mol Imaging. 2017 Aug;44(9):1588–1601. doi: 10.1007/s00259-017-3728-y
  • Pfeifer A, Knigge U, Mortensen J, et al. Clinical PET of neuroendocrine tumors using 64Cu-DOTATATE: first-in-humans study. J Nucl Med. 2012 Aug;53(8):1207–1215. doi: 10.2967/jnumed.111.101469
  • Hicks RJ, Jackson P, Kong G, et al. (64)Cu-SARTATE PET imaging of patients with neuroendocrine tumors demonstrates high tumor uptake and retention, potentially allowing prospective dosimetry for peptide receptor radionuclide therapy. J Nucl Med. 2019 Jun;60(6):777–785. doi: 10.2967/jnumed.118.217745
  • Nicolas GP, Beykan S, Bouterfa H, et al. Safety, biodistribution, and radiation dosimetry of (68)Ga-OPS202 in patients with gastroenteropancreatic neuroendocrine tumors: a prospective phase i imaging study. J Nucl Med. 2018 Jun;59(6):909–914. doi: 10.2967/jnumed.117.199737
  • Fani M, Nicolas GP, Wild D. Somatostatin receptor antagonists for imaging and therapy. J Nucl Med. 2017 Sep;58(Suppl Supplement 2):61s–66s. doi: 10.2967/jnumed.116.186783
  • Abstracts. J Neuroendocrinol. 2024;36(S1):e13383. doi: 10.1111/jne.13383
  • Pauwels E, Cleeren F, Tshibangu T, et al. (18)F-AlF-NOTA-Octreotide Outperforms (68)Ga-DOTATATE/NOC PET in neuroendocrine tumor patients: results from a prospective, multicenter study. J Nucl Med. 2023 Apr;64(4):632–638. doi: 10.2967/jnumed.122.264563
  • Long T, Yang N, Zhou M, et al. Clinical application of 18F-AlF-NOTA-Octreotide PET/CT in combination with 18F-FDG PET/CT for imaging neuroendocrine neoplasms. Clin Nucl Med. 2019 Jun;44(6):452–458. doi: 10.1097/RLU.0000000000002578
  • Van de Wiele C, Sathekge M, de Spiegeleer B, et al. PSMA-Targeting positron emission agents for imaging solid tumors other than non-prostate carcinoma: a systematic review. Int J Mol Sci. [2019 Oct 2];20(19):4886. doi: 10.3390/ijms20194886
  • Luong TV, Iversen P, Bouchelouche K, et al. 68Ga-prostate-specific membrane antigen uptake in a pancreatic neuroendocrine tumor. Clin Nucl Med. 2020 May;45(5):379–382. doi: 10.1097/RLU.0000000000002997
  • Hasenauer N, Higuchi T, Deschler-Baier B, et al. Visualization of tumor heterogeneity in advanced medullary thyroid carcinoma by dual-tracer molecular imaging: revealing the theranostic potential of SSTR- and PSMA-directed endoradiotherapy. Clin Nucl Med. [2022 Jul 1];47(7):651–652. doi: 10.1097/RLU.0000000000004082
  • Lindner T, Loktev A, Altmann A, et al. Development of quinoline-based theranostic ligands for the targeting of fibroblast activation protein. J Nucl Med. 2018 Sep;59(9):1415–1422. doi: 10.2967/jnumed.118.210443
  • Smit Duijzentkunst DA, Kwekkeboom DJ, Bodei L. Somatostatin receptor 2-targeting compounds. J Nucl Med. 2017 Sep;58(Suppl 2):54s–60s. doi: 10.2967/jnumed.117.191015
  • Shur JD, Doran SJ, Kumar S, et al. Radiomics in oncology: A practical guide. Radiographics. 2021 Oct;41(6):1717–1732. doi: 10.1148/rg.2021210037
  • Zwanenburg A, Vallières M, Abdalah MA, et al. The image biomarker standardization initiative: standardized quantitative radiomics for high-throughput image-based phenotyping. Radiology. 2020 May;295(2):328–338. doi: 10.1148/radiol.2020191145
  • De Muzio F, Pellegrino F, Fusco R, et al. Prognostic assessment of gastropancreatic neuroendocrine neoplasm: prospects and limits of radiomics. Diagnostics (Basel). [2023 Sep 7];13(18):2877. doi: 10.3390/diagnostics13182877
  • Guo C, Zhuge X, Wang Q, et al. The differentiation of pancreatic neuroendocrine carcinoma from pancreatic ductal adenocarcinoma: the values of CT imaging features and texture analysis. Cancer Imaging. [2018 Oct 17];18(1):37. doi: 10.1186/s40644-018-0170-8
  • Han X, Yang J, Luo J, et al. Application of CT-Based radiomics in discriminating pancreatic cystadenomas from pancreatic neuroendocrine tumors using machine learning methods. Front Oncol. 2021;11:606677. doi: 10.3389/fonc.2021.606677
  • Staal FCR, Aalbersberg EA, van der Velden D, et al. GEP-NET radiomics: a systematic review and radiomics quality score assessment. Eur Radiol. 2022 Oct;32(10):7278–7294. doi: 10.1007/s00330-022-08996-w
  • Pereira JA, Rosado E, Bali M, et al. Pancreatic neuroendocrine tumors: correlation between histogram analysis of apparent diffusion coefficient maps and tumor grade. Abdom Imaging. 2015 Oct;40(8):3122–3128. doi: 10.1007/s00261-015-0524-7
  • Granata V, Grassi R, Fusco R, et al. Assessment of ablation therapy in pancreatic cancer: the radiologist’s challenge. Front Oncol. 2020;10:560952. doi: 10.3389/fonc.2020.560952
  • De Robertis R, Maris B, Cardobi N, et al. Can histogram analysis of MR images predict aggressiveness in pancreatic neuroendocrine tumors? Eur Radiol. 2018 Jun;28(6):2582–2591. doi: 10.1007/s00330-017-5236-7
  • Calandrelli R, Boldrini L, Tran HE, et al. CT-based radiomics modeling for skull dysmorphology severity and surgical outcome prediction in children with isolated sagittal synostosis: a hypothesis-generating study. Radiol Med. 2022 Jun;127(6):616–626. doi: 10.1007/s11547-022-01493-6
  • Chen L, Wang W, Jin K, et al. Special issue “The advance of solid tumor research in China”: Prediction of Sunitinib efficacy using computed tomography in patients with pancreatic neuroendocrine tumors. Int J Cancer. 2023 Jan 1;152(1):90–99. doi: 10.1002/ijc.34294
  • Werner RA, Lapa C, Ilhan H, et al. Survival prediction in patients undergoing radionuclide therapy based on intratumoral somatostatin-receptor heterogeneity. Oncotarget. 2017 Jan 24;8(4):7039–7049. doi: 10.18632/oncotarget.12402
  • Laudicella R, Comelli A, Liberini V, et al. [68Ga]DOTATOC PET/CT Radiomics to Predict the Response in GEP-NETs Undergoing [177Lu]DOTATOC PRRT: The “Theragnomics” Concept. Cancers (Basel). 2022 Feb 16;14(4):984. doi: 10.3390/cancers14040984
  • Zilli A, Arcidiacono PG, Conte D, et al. Clinical impact of endoscopic ultrasonography on the management of neuroendocrine tumors: lights and shadows. Dig Liver Dis. 2018 Jan;50(1):6–14. doi: 10.1016/j.dld.2017.10.007
  • Massironi S, Gallo C, Laffusa A, et al. Endoscopic techniques for gastric neuroendocrine tumors: An update. World J Gastrointest Endosc. 2023 Mar 16;15(3):103–113. doi: 10.4253/wjge.v15.i3.103
  • Rossi RE, Elvevi A, Gallo C, et al. Endoscopic techniques for diagnosis and treatment of gastro-entero-pancreatic neuroendocrine neoplasms: Where we are. World J Gastroenterol. 2022 Jul 14;28(26):3258–3273. doi: 10.3748/wjg.v28.i26.3258
  • Egashira A, Morita M, Kumagai R, et al. Neuroendocrine carcinoma of the esophagus: Clinicopathological and immunohistochemical features of 14 cases. PLoS One. 2017;12(3):e0173501. doi: 10.1371/journal.pone.0173501
  • Vanoli A, La Rosa S, Miceli E, et al. Prognostic Evaluations Tailored to Specific Gastric Neuroendocrine Neoplasms: Analysis Of 200 Cases with Extended Follow-Up. Neuroendocrinology. 2018;107(2):114–126. doi: 10.1159/000489902
  • Zhang XF, Wu XN, Tsilimigras DI, et al. Duodenal neuroendocrine tumors: Impact of tumor size and total number of lymph nodes examined. J Surg Oncol. 2019 Dec;120(8):1302–1310. doi: 10.1002/jso.25753
  • de Mestier L, Lorenzo D, Fine C, et al. Endoscopic, transanal, laparoscopic, and transabdominal management of rectal neuroendocrine tumors. Best Pract Res Clin Endocrinol Metab. 2019 Oct;33(5):101293. doi: 10.1016/j.beem.2019.101293
  • Singh R, Yao K, Anagnostopoulos G, et al. Microcarcinoid tumor diagnosed with high-resolution magnification endoscopy and narrow band imaging. Endoscopy. 2008 Sep;40(Suppl 2):E12. doi: 10.1055/s-2007-995393
  • Sato Y. Endoscopic diagnosis and management of type I neuroendocrine tumors. World J Gastrointest Endosc. 2015 Apr 16;7(4):346–353. doi: 10.4253/wjge.v7.i4.346
  • Hirai M, Matsumoto K, Ueyama H, et al. A case of neuroendocrine tumor G1 with unique histopathological growth progress. World J Gastrointest Endosc. 2013 Dec 16;5(12):605–609. doi: 10.4253/wjge.v5.i12.605
  • Matsueda K, Uedo N, Kitamura M, et al. Endoscopic features of gastric neuroendocrine carcinoma. J Gastroenterol Hepatol. 2023 Oct;38(10):1808–1817. doi: 10.1111/jgh.16309
  • Kim GH, Yi K, Joo DC, et al. Magnifying Endoscopy with Narrow-Band Imaging for Duodenal Neuroendocrine Tumors. J Clin Med. 2023 Apr 24;12(9):3106.
  • Lin CK, Chung CS, Huang WC. Rectal carcinoid tumour observed by magnifying colonoscopy with narrow band imaging. Dig Liver Dis. 2014 Jul;46(7):e7. doi: 10.1016/j.dld.2013.12.003
  • Yantiss RK, Odze RD, Farraye FA, et al. Solitary versus multiple carcinoid tumors of the ileum: a clinical and pathologic review of 68 cases. Am J Surg Pathol. 2003 Jun;27(6):811–817. doi: 10.1097/00000478-200306000-00013
  • Bonekamp D, Raman SP, Horton KM, et al. Role of computed tomography angiography in detection and staging of small bowel carcinoid tumors. World J Radiol. 2015 Sep 28;7(9):220–235. doi: 10.4329/wjr.v7.i9.220
  • van Tuyl SA, van Noorden JT, Timmer R, et al. Detection of small-bowel neuroendocrine tumors by video capsule endoscopy. Gastrointest Endosc. 2006 Jul;64(1):66–72. doi: 10.1016/j.gie.2006.01.054
  • Rossi RE, Conte D, Elli L, et al. Endoscopic techniques to detect small-bowel neuroendocrine tumors: A literature review. United Eur Gastroenterol J. 2017 Feb;5(1):5–12. doi: 10.1177/2050640616658220
  • Rondonotti E, Pennazio M, Toth E, et al. Small-bowel neoplasms in patients undergoing video capsule endoscopy: a multicenter European study. Endoscopy. 2008 Jun;40(6):488–495. doi: 10.1055/s-2007-995783
  • Furnari M, Buda A, Delconte G, et al. The role of wireless capsule endoscopy (WCE) in the detection of occult primary neuroendocrine tumors. J Gastrointestin Liver Dis. 2017 Jun;26(2):151–156. doi: 10.15403/jgld.2014.1121.262.wce
  • Rossi RE, Elli L, Branchi F, et al. Double-Balloon Enteroscopy in Detecting Small-Bowel Neuroendocrine Neoplasms: A Single-Center Prospective Study. Digestion. 2021;102(5):722–730. doi: 10.1159/000511850
  • Tominaga K, Kamimura K, Yokoyama J, et al. Usefulness of Capsule Endoscopy and Double-balloon Enteroscopy for the Diagnosis of Multiple Carcinoid Tumors in the Small Intestine: Case Reports and a Literature Review. Intern Med. 2019 Mar 1;58(5):655–659. doi: 10.2169/internalmedicine.1700-18
  • Bellutti M, Fry LC, Schmitt J, et al. Detection of neuroendocrine tumors of the small bowel by double balloon enteroscopy. Dig Dis Sci. 2009 May;54(5):1050–1058. doi: 10.1007/s10620-008-0456-y
  • Niederle B, Pape UF, Costa F, et al. ENETS Consensus Guidelines Update for Neuroendocrine Neoplasms of the Jejunum and Ileum. Neuroendocrinology. 2016;103(2):125–138. doi: 10.1159/000443170
  • Yoon JY, Kumta NA, Kim MK. The Role of Endoscopy in Small Bowel Neuroendocrine Tumors. Clin Endosc. 2021 Nov;54(6):818–824. doi: 10.5946/ce.2020.296
  • Kos-Kudła B, Castaño JP, Denecke T, et al. European Neuroendocrine Tumour Society (ENETS) 2023 guidance paper for nonfunctioning pancreatic neuroendocrine tumours. J Neuroendocrinology. 2023 Oct;5(12):e13343. doi: 10.1111/jne.13343
  • Falconi M, Eriksson B, Kaltsas G, et al. ENETS Consensus Guidelines Update for the Management of Patients with Functional Pancreatic Neuroendocrine Tumors and Non-Functional Pancreatic Neuroendocrine Tumors. Neuroendocrinology. 2016;103(2):153–171. doi: 10.1159/000443171
  • Manta R, Nardi E, Pagano N, et al. Pre-operative Diagnosis of Pancreatic Neuroendocrine Tumors with Endoscopic Ultrasonography and Computed Tomography in a Large Series. J Gastrointestin Liver Dis. 2016 Sep;25(3):317–321. doi: 10.15403/jgld.2014.1121.253.ned
  • Tacelli M, Bina N, Crinò SF, et al. Reliability of grading preoperative pancreatic neuroendocrine tumors on EUS specimens: a systematic review with meta-analysis of aggregate and individual data. Gastrointest Endosc. 2022 Dec;96(6):898–908.e23. doi: 10.1016/j.gie.2022.07.014
  • Fujimori N, Osoegawa T, Lee L, et al. Efficacy of endoscopic ultrasonography and endoscopic ultrasonography-guided fine-needle aspiration for the diagnosis and grading of pancreatic neuroendocrine tumors. Scand J Gastroenterol. 2016;51(2):245–252. doi: 10.3109/00365521.2015.1083050
  • Leiman G. My approach to pancreatic fine needle aspiration. J Clin Pathol. 2007 Jan;60(1):43–49. doi: 10.1136/jcp.2005.034959
  • Crinò SF, Ammendola S, Meneghetti A, et al. Comparison between EUS-guided fine-needle aspiration cytology and EUS-guided fine-needle biopsy histology for the evaluation of pancreatic neuroendocrine tumors. Pancreatology. 2021 Mar;21(2):443–450. doi: 10.1016/j.pan.2020.12.015
  • Paiella S, Landoni L, Rota R, et al. Endoscopic ultrasound-guided fine-needle aspiration for the diagnosis and grading of pancreatic neuroendocrine tumors: a retrospective analysis of 110 cases. Endoscopy. 2020 Nov; 52(11):988–994. doi: 10.1055/a-1180-8614
  • Pezzilli R, Partelli S, Cannizzaro R, et al. Ki-67 prognostic and therapeutic decision driven marker for pancreatic neuroendocrine neoplasms (PNENs): A systematic review. Adv Med Sci. 2016 Mar;61(1):147–153. doi: 10.1016/j.advms.2015.10.001
  • Rimbaş M, Crino SF, Gasbarrini A, et al. EUS-guided fine-needle tissue acquisition for solid pancreatic lesions: Finally moving from fine-needle aspiration to fine-needle biopsy?. Endosc Ultrasound. 2018;7:137–140, China. doi: 10.4103/eus.eus_23_18
  • Delconte G, Cavalcoli F, Magarotto A, et al. Does ProCore fine-needle biopsy really improve the clinical outcome of endoscopic ultrasound-guided sampling of pancreatic masses? Dig Dis. 2022;40(1):78–84. doi: 10.1159/000516177
  • Eusebi LH, Thorburn D, Toumpanakis C, et al. Endoscopic ultrasound-guided fine-needle aspiration vs fine-needle biopsy for the diagnosis of pancreatic neuroendocrine tumors. Endosc Int Open. 2019 Nov;7(11):E1393–e1399. doi: 10.1055/a-0967-4684
  • Leeds JS, Nayar MK, Bekkali NLH, et al. Endoscopic ultrasound-guided fine-needle biopsy is superior to fine-needle aspiration in assessing pancreatic neuroendocrine tumors. Endosc Int Open. 2019 Oct;7(10):E1281–e1287. doi: 10.1055/a-0990-9611
  • Dietrich CF, Ignee A, Braden B, et al. Improved differentiation of pancreatic tumors using contrast-enhanced endoscopic ultrasound. Clin Gastroenterol Hepatol. 2008 May;6(5):590–597.e1. doi: 10.1016/j.cgh.2008.02.030
  • Malagò R, D’Onofrio M, Zamboni GA, et al. Contrast-enhanced sonography of nonfunctioning pancreatic neuroendocrine tumors. AJR Am J Roentgenol. 2009 Feb;192(2):424–430. doi: 10.2214/AJR.07.4043
  • Ishikawa R, Kamata K, Hara A, et al. Utility of contrast-enhanced harmonic endoscopic ultrasonography for predicting the prognosis of pancreatic neuroendocrine neoplasms. Dig Endosc. 2021 Jul;33(5):829–839. doi: 10.1111/den.13862
  • Dietrich CF, Săftoiu A, Jenssen C. Real time elastography endoscopic ultrasound (RTE-EUS), a comprehensive review. European Journal of Radiology. 2014 Mar;83(3):405–414. doi: 10.1016/j.ejrad.2013.03.023
  • Havre RF, Ødegaard S, Gilja OH, et al. Characterization of solid focal pancreatic lesions using endoscopic ultrasonography with real-time elastography. Scand J Gastroenterol. 2014 Jun;49(6):742–751. doi: 10.3109/00365521.2014.905627
  • Iglesias-Garcia J, Larino-Noia J, Abdulkader I, et al. Quantitative endoscopic ultrasound elastography: an accurate method for the differentiation of solid pancreatic masses. Gastroenterology. 2010 Oct;139(4):1172–1180. doi: 10.1053/j.gastro.2010.06.059
  • Ignee A, Jenssen C, Arcidiacono PG, et al. Endoscopic ultrasound elastography of small solid pancreatic lesions: a multicenter study. Endoscopy. 2018 Nov;50(11):1071–1079. doi: 10.1055/a-0588-4941
  • Panzuto F, Ramage J, Pritchard DM, et al. European Neuroendocrine Tumor Society (ENETS) 2023 guidance paper for gastroduodenal neuroendocrine tumours (NETs) G1–G3. J Neuroendocrinol. 2023 May 20;35(8):e13306. doi: 10.1111/jne.13306
  • Hosseini F, Asadi F, Emami H, et al. Machine learning applications for early detection of esophageal cancer: a systematic review. BMC Med Inform Decis Mak. 2023 Jul 17;23(1):124. doi: 10.1186/s12911-023-02235-y
  • Horie Y, Yoshio T, Aoyama K, et al. Diagnostic outcomes of esophageal cancer by artificial intelligence using convolutional neural networks. Gastrointest Endosc. 2019 Jan;89(1):25–32. doi: 10.1016/j.gie.2018.07.037
  • Pannala R, Krishnan K, Melson J, et al. Artificial intelligence in gastrointestinal endoscopy. VideoGIE. 2020 Dec;5(12):598–613. doi: 10.1016/j.vgie.2020.08.013
  • Byrne MF, Chapados N, Soudan F, et al. Real-time differentiation of adenomatous and hyperplastic diminutive colorectal polyps during analysis of unaltered videos of standard colonoscopy using a deep learning model. Gut. 2019 Jan;68(1):94–100. doi: 10.1136/gutjnl-2017-314547
  • Kuwahara T, Hara K, Mizuno N, et al. Usefulness of deep learning analysis for the diagnosis of malignancy in intraductal papillary mucinous neoplasms of the pancreas. Clin Transl Gastroenterol. 2019 May 22;10(5):1–8. doi: 10.14309/ctg.0000000000000045
  • Hirai K, Kuwahara T, Furukawa K, et al. Artificial intelligence-based diagnosis of upper gastrointestinal subepithelial lesions on endoscopic ultrasonography images. Gastric Cancer. 2022 Mar;25(2):382–391. doi: 10.1007/s10120-021-01261-x
  • Mariën L, Islam O, Chhajlani S, et al. The quest for circulating biomarkers in neuroendocrine neoplasms: a clinical perspective. Curr Treat Options Oncol. 2023 Nov 22;24(12):1833–1851. doi: 10.1007/s11864-023-01147-3
  • Fang JM, Li J, Shi J. An update on the diagnosis of gastroenteropancreatic neuroendocrine neoplasms. World J Gastroenterol. 2022 Mar 14;28(10):1009–1023. doi: 10.3748/wjg.v28.i10.1009
  • Sansone A, Lauretta R, Vottari S, et al. Specific and non-specific biomarkers in neuroendocrine gastroenteropancreatic tumors. Cancers (Basel). 2019 Aug 4;11(8):1113. doi: 10.3390/cancers11081113
  • Modlin IM, Bodei L, Kidd M. Neuroendocrine tumor biomarkers: From monoanalytes to transcripts and algorithms. Best Pract Res Clin Endocrinol Metab. 2016 Jan;30(1):59–77. doi: 10.1016/j.beem.2016.01.002
  • Bevere M, Masetto F, Carazzolo ME, et al. An overview of circulating biomarkers in neuroendocrine neoplasms: a clinical guide. Diagnostics (Basel). 2023 Aug 31;13(17):2820. doi: 10.3390/diagnostics13172820
  • Kidd M, Bodei L, Modlin IM. Chromogranin A: any relevance in neuroendocrine tumors?. Curr Opin Endocrinol Diabetes Obes. 2016 Feb;23(1):28–37. doi: 10.1097/MED.0000000000000215
  • Rossi RE, Ciafardini C, Sciola V, et al. Chromogranin A in the follow-up of gastroenteropancreatic neuroendocrine neoplasms: is it really game over? a systematic review and meta-analysis. Pancreas. 2018 Nov;47(10):1249–1255. doi: 10.1097/MPA.0000000000001184
  • Fuksiewicz M, Kowalska M, Kolasińska-Ćwikła A, et al. Prognostic value of chromogranin A in patients with GET/NEN in the pancreas and the small intestine. Endocr Connect. 2018 Jun;7(6):803–810. doi: 10.1530/EC-18-0059
  • Komarnicki P, Gut P, Musiałkiewicz J, et al. NT-proBNP as a neuroendocrine tumor biomarker: beyond heart failure. Endocr Connect. 2023 Oct 1;12(10). doi: 10.1530/EC-23-0249
  • Pavel M, Öberg K, Falconi M, et al. Gastroenteropancreatic neuroendocrine neoplasms: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2020 Jul;31(7):844–860. doi: 10.1016/j.annonc.2020.03.304
  • Hofland J, Falconi M, Christ E, et al. European Neuroendocrine Tumor Society 2023 guidance paper for functioning pancreatic neuroendocrine tumour syndromes. J Neuroendocrinol. 2023 Aug;35(8):e13318. doi: 10.1111/jne.13318
  • Modlin IM, Kidd M, Malczewska A, et al. The NETest: the clinical utility of multigene blood analysis in the diagnosis and management of neuroendocrine tumors. Endocrinol Metab Clin North Am. 2018 Sep;47(3):485–504. doi: 10.1016/j.ecl.2018.05.002
  • Puliani G, Di Vito V, Feola T, et al. NETest: a systematic review focusing on the prognostic and predictive role. Neuroendocrinology. 2022;112:523–536. doi: 10.1159/000518873 Switzerland: © 2021 S. Karger AG, Basel.
  • Öberg K, Califano A, Strosberg JR, et al. A meta-analysis of the accuracy of a neuroendocrine tumor mRNA genomic biomarker (NETest) in blood. Ann Oncol. 2020 Feb;31(2):202–212. doi: 10.1016/j.annonc.2019.11.003
  • Khan MS, Kirkwood A, Tsigani T, et al. Circulating tumor cells as prognostic markers in neuroendocrine tumors. J Clin Oncol. 2013 Jan 20;31(3):365–372. doi: 10.1200/JCO.2012.44.2905
  • Mandair D, Khan MS, Lopes A, et al. Prognostic threshold for circulating tumor cells in patients with pancreatic and midgut neuroendocrine tumors. J Clin Endocrinol Metab. 2021 Mar 8;106(3):872–882. doi: 10.1210/clinem/dgaa822
  • Meyer T, Caplin M, Khan MS, et al. Circulating tumour cells and tumour biomarkers in functional midgut neuroendocrine tumours. J Neuroendocrinol. 2022 Apr;34(4):e13096. doi: 10.1111/jne.13096
  • Rizzo FM, Vesely C, Childs A, et al. Circulating tumour cells and their association with bone metastases in patients with neuroendocrine tumours. Br J Cancer. 2019 Feb;120(3):294–300. doi: 10.1038/s41416-018-0367-4
  • Geisler L, Mohr R, Lambrecht J, et al. The role of miRNA in the pathophysiology of neuroendocrine tumors. Int J Mol Sci. 2021 Aug 9;22(16):8569. doi: 10.3390/ijms22168569
  • Lee YS, Kim H, Kim HW, et al. High expression of MicroRNA-196a indicates poor prognosis in resected pancreatic neuroendocrine tumor. Medicine (Baltimore). 2015 Dec;94(50):e2224. doi: 10.1097/MD.0000000000002224
  • Havasi A, Sur D, Cainap SS, et al. Current and new challenges in the management of pancreatic neuroendocrine tumors: the role of miRNA-based approaches as new reliable biomarkers. Int J Mol Sci. 2022 Jan 20;23(3):1109. doi: 10.3390/ijms23031109
  • Malczewska A, Frampton AE, Mato Prado M, et al. Circulating MicroRNAs in small-bowel neuroendocrine tumors: a potential tool for diagnosis and assessment of effectiveness of surgical resection. Ann Surg. 2021 Jul 1;274(1):e1–e9. doi: 10.1097/SLA.0000000000003502
  • Szilágyi M, Pös O, Márton É, et al. Circulating cell-free nucleic acids: main characteristics and clinical application. Int J Mol Sci. 2020 Sep 17;21(18):6827. doi: 10.3390/ijms21186827
  • Zakka K, Nagy R, Drusbosky L, et al. Blood-based next-generation sequencing analysis of neuroendocrine neoplasms. Oncotarget. 2020 May 12;11(19):1749–1757. doi: 10.18632/oncotarget.27588
  • Smolkova B, Kataki A, Earl J, et al. Liquid biopsy and preclinical tools for advancing diagnosis and treatment of patients with pancreatic neuroendocrine neoplasms. Crit Rev Oncol Hematol. 2022 Dec;180:103865. doi: 10.1016/j.critrevonc.2022.103865
  • Prakash V, Gao L, Park SJ. Evolving applications of circulating tumor DNA in Merkel cell carcinoma. Cancers (Basel). 2023 Jan 18;15(3):609. doi: 10.3390/cancers15030609
  • Rosiek V, Janas K, Kos-Kudła B. Association between biomarkers (VEGF-R2, VEGF-R3, VCAM-1) and treatment duration in patients with neuroendocrine tumors receiving therapy with first-generation somatostatin analogues. Biomedicines. 2023 Mar 10;11(3):842. doi: 10.3390/biomedicines11030842
  • Pavel ME, Hassler G, Baum U, et al. Circulating levels of angiogenic cytokines can predict tumour progression and prognosis in neuroendocrine carcinomas. Clin Endocrinol (Oxf). 2005 Apr 62;(4):434–443. doi: 10.1111/j.1365-2265.2005.02238.x
  • Rindi G, Klöppel G, Alhman H, et al. TNM staging of foregut (neuro)endocrine tumors: a consensus proposal including a grading system. Virchows Arch. 2006 Oct 449;(4):395–401. doi: 10.1007/s00428-006-0250-1
  • Rindi G, Klöppel G, Couvelard A, et al. TNM staging of midgut and hindgut (neuro) endocrine tumors: a consensus proposal including a grading system. Virchows Arch. 2007 Oct 451;(4):757–762. doi: 10.1007/s00428-007-0452-1
  • Zhang Q, Huang J, He Y, et al. Insulinoma-associated protein 1(INSM1) is a superior marker for the diagnosis of gastroenteropancreatic neuroendoerine neoplasms: a meta-analysis. Endocrine. 2021 Oct 74;(1):61–71. doi: 10.1007/s12020-021-02754-6
  • Jeong SY, Park YS, Lee J, et al. Tumor mutation burden in gastro-entero-pancreatic-neuroendocrine neoplasms. J Gastrointest Oncol. 2023 Aug 31;14(4):1707–1714. doi: 10.21037/jgo-22-1190
  • Ghabi EM, Habib JR, Shoucair S, et al. Detecting somatic mutations for well-differentiated pancreatic neuroendocrine tumors in endoscopic ultrasound-guided fine needle aspiration with next-generation sequencing. Ann Surg Oncol. 2023 Nov;30(12):7720–7730. doi: 10.1245/s10434-023-13965-8
  • Ciobanu OA, Martin SC, Herlea V, et al. Insights into epigenetic changes related to genetic variants and cells-of-origin of pancreatic neuroendocrine tumors: an algorithm for practical workup. Cancers (Basel). 2022 Sep 13;14(18):4444. doi: 10.3390/cancers14184444
  • Di Domenico A, Pipinikas CP, Maire RS, et al. Epigenetic landscape of pancreatic neuroendocrine tumours reveals distinct cells of origin and means of tumour progression. Commun Biol. 2020 Dec 7;3(1):740. doi: 10.1038/s42003-020-01479-y
  • Marinoni I, Kurrer AS, Vassella E, et al. Loss of DAXX and ATRX are associated with chromosome instability and reduced survival of patients with pancreatic neuroendocrine tumors. Gastroenterology. 2014 Feb;146(2):453–60.e5. doi: 10.1053/j.gastro.2013.10.020
  • Uemura J, Okano K, Oshima M, et al. Immunohistochemically detected expression of ATRX, TSC2, and PTEN predicts clinical outcomes in patients with grade 1 and 2 pancreatic neuroendocrine tumors. Ann Surg. 2021 Dec 1;274(6):e949–e956. doi: 10.1097/SLA.0000000000003624
  • Mastrosimini MG, Manfrin E, Remo A, et al. Endoscopic ultrasound fine-needle biopsy to assess DAXX/ATRX expression and alternative lengthening of telomeres status in non-functional pancreatic neuroendocrine tumors. Pancreatology. 2023 Jun;23(4):429–436. doi: 10.1016/j.pan.2023.05.002
  • Konukiewitz B, Schlitter AM, Jesinghaus M, et al. Somatostatin receptor expression related to TP53 and RB1 alterations in pancreatic and extrapancreatic neuroendocrine neoplasms with a Ki67-index above 20. Mod Pathol. 2017 Apr;30(4):587–598. doi: 10.1038/modpathol.2016.217
  • Ewang-Emukowhate M, Subramaniam K, Lam F, et al. Plasma or serum 5-hydroxyindoleacetic acid can be used interchangeably in patients with neuroendocrine tumours. Scand J Clin Lab Invest. 2023 Dec;83(8):576–581. doi: 10.1080/00365513.2023.2286645
  • Park HY, Kwon MJ, Kang HS, et al. Targeted next-generation sequencing of well-differentiated rectal, gastric, and appendiceal neuroendocrine tumors to identify potential targets. Hum Pathol. 2019 May;87:83–94. doi: 10.1016/j.humpath.2019.02.007
  • Francis JM, Kiezun A, Ramos AH, et al. Somatic mutation of CDKN1B in small intestine neuroendocrine tumors. Nat Genet. 2013 Dec;45(12):1483–1486. doi: 10.1038/ng.2821
  • van Riet J, van de Werken HJG, Cuppen E, et al. The genomic landscape of 85 advanced neuroendocrine neoplasms reveals subtype-heterogeneity and potential therapeutic targets. Nat Commun. 2021 Jul 29;12(1):p. 4612.
  • Pavel M, Dromain C, Ronot M, et al. The use of deep learning models to predict progression-free survival in patients with neuroendocrine tumors. Future Oncol. 2023 Oct;19(32):2185–2199. doi: 10.2217/fon-2022-1136
  • Genus TSE, Bouvier C, Wong KF, et al. Impact of neuroendocrine morphology on cancer outcomes and stage at diagnosis: a UK nationwide cohort study 2013-2015. Br J Cancer. 2019 Nov;121(11):966–972. doi: 10.1038/s41416-019-0606-3

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