{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,17]],"date-time":"2026-09-17T22:36:10Z","timestamp":1789684570245,"version":"4.0.1"},"reference-count":30,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2024,4,25]],"date-time":"2024-04-25T00:00:00Z","timestamp":1714003200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004271","name":"Sapienza University of Rome","doi-asserted-by":"publisher","award":["RM12218161A53B1D"],"award-info":[{"award-number":["RM12218161A53B1D"]}],"id":[{"id":"10.13039\/501100004271","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JCM"],"abstract":"<jats:p>Objectives: Our aim was to investigate the clinical outcome of patients with well-differentiated gastric, duodenal, and rectal neuroendocrine tumors after treatment with incomplete endoscopic resection due to the finding of microscopic positive resection margins (R1). Methods: This is a retrospective analysis of consecutive patients with type 1 gastric, non-ampullary non-functioning duodenal, or rectal neuroendocrine neoplasms with positive R1 margins after endoscopic resection. The rate of tumor recurrence and progression-free survival were considered to be the study\u2019s main endpoints. Statistical analysis was performed using MedCalc\u00ae v.17 software and a p-value of &lt;0.05 was considered significant. A Cox proportional-hazard regression was performed to identify risk factors for disease recurrence\/progression. Results: After evaluating 110 patients, a total of 58 patients were included in the final analysis (15 gastric NENs, 12 duodenal NENs, and 31 rectal NENs). After evidence of endoscopic R1 resection had been gathered, 26 patients (44.8%) underwent an endoscopic\/surgical extension of the previous resection. Tumor progression (all local recurrences) occurred in five out of fifty-eight patients (8.6%) with a median PFS of 36 months. There were no tumor-related deaths. G2 grading and the gastric primary tumor site were the only features significantly associated with the risk of recurrence of the disease (HR: 11.97 [95% CI: 1.22\u2013116.99], HR: 12.54 [95% CI: 1.28\u2013122.24], respectively). Conclusions: Tumor progression rarely occurs in patients with microscopic positive margin excision (R1) after endoscopic resection and does not seem to affect patients\u2019 clinical outcomes.<\/jats:p>","DOI":"10.3390\/jcm13092535","type":"journal-article","created":{"date-parts":[[2024,4,26]],"date-time":"2024-04-26T03:23:47Z","timestamp":1714101827000},"page":"2535","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":17,"title":["Clinical Outcome of Patients with Gastric, Duodenal, or Rectal Neuroendocrine Tumors after Incomplete Endoscopic Resection"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0009-0004-8128-1111","authenticated-orcid":false,"given":"Elisabetta","family":"Dell\u2019Unto","sequence":"first","affiliation":[{"name":"Digestive Disease Unit, Sant\u2019Andrea University Hospital, ENETS Center of Excellence or Rome, 00189 Rome, Italy"},{"name":"Department of Medical, Surgical Sciences and Translational Medicine, Sapienza University of Rome, 00189 Rome, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0002-0496-3229","authenticated-orcid":false,"given":"Matteo","family":"Marasco","sequence":"additional","affiliation":[{"name":"Digestive Disease Unit, Sant\u2019Andrea University Hospital, ENETS Center of Excellence or Rome, 00189 Rome, Italy"},{"name":"Department of Medical, Surgical Sciences and Translational Medicine, Sapienza University of Rome, 00189 Rome, Italy"},{"name":"PhD School in Translational Medicine and Oncology, Sapienza University of Rome, 00189 Rome, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mirta","family":"Mosca","sequence":"additional","affiliation":[{"name":"Department of Experimental, Diagnostic & Specialty Medicine (DIMES), University of Bologna, 40138 Bologna, Italy"},{"name":"Medical Oncology, IRCCS Azienda Ospedaliero, Universitaria of Bologna, 40138 Bologna, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7598-7220","authenticated-orcid":false,"given":"Camilla","family":"Gallo","sequence":"additional","affiliation":[{"name":"Division of Gastroenterology, Fondazione IRCCS San Gerardo dei Tintori, 20900 Monza, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2242-5048","authenticated-orcid":false,"given":"Gianluca","family":"Esposito","sequence":"additional","affiliation":[{"name":"Digestive Disease Unit, Sant\u2019Andrea University Hospital, ENETS Center of Excellence or Rome, 00189 Rome, Italy"},{"name":"Department of Medical, Surgical Sciences and Translational Medicine, Sapienza University of Rome, 00189 Rome, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria","family":"Rinzivillo","sequence":"additional","affiliation":[{"name":"Digestive Disease Unit, Sant\u2019Andrea University Hospital, ENETS Center of Excellence or Rome, 00189 Rome, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7110-9172","authenticated-orcid":false,"given":"Emanuela","family":"Pilozzi","sequence":"additional","affiliation":[{"name":"Department of Clinical and Molecular Medicine, UOC Anatomic Pathology, Sant\u2019Andrea Hospital, Sapienza University of Rome, 00189 Rome, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Federica","family":"Orr\u00f9","sequence":"additional","affiliation":[{"name":"Department of Clinical and Molecular Medicine, UOC Anatomic Pathology, Sant\u2019Andrea Hospital, Sapienza University of Rome, 00189 Rome, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4615-7340","authenticated-orcid":false,"given":"Davide","family":"Campana","sequence":"additional","affiliation":[{"name":"Department of Experimental, Diagnostic & Specialty Medicine (DIMES), University of Bologna, 40138 Bologna, Italy"},{"name":"Medical Oncology, IRCCS Azienda Ospedaliero, Universitaria of Bologna, 40138 Bologna, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3214-8192","authenticated-orcid":false,"given":"Sara","family":"Massironi","sequence":"additional","affiliation":[{"name":"Division of Gastroenterology, Fondazione IRCCS San Gerardo dei Tintori, 20900 Monza, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9120-5957","authenticated-orcid":false,"given":"Bruno","family":"Annibale","sequence":"additional","affiliation":[{"name":"Digestive Disease Unit, Sant\u2019Andrea University Hospital, ENETS Center of Excellence or Rome, 00189 Rome, Italy"},{"name":"Department of Medical, Surgical Sciences and Translational Medicine, Sapienza University of Rome, 00189 Rome, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2789-4289","authenticated-orcid":false,"given":"Francesco","family":"Panzuto","sequence":"additional","affiliation":[{"name":"Digestive Disease Unit, Sant\u2019Andrea University Hospital, ENETS Center of Excellence or Rome, 00189 Rome, Italy"},{"name":"Department of Medical, Surgical Sciences and Translational Medicine, Sapienza University of Rome, 00189 Rome, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,4,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"471","DOI":"10.3322\/caac.21493","article-title":"Gastroenteropancreatic Neuroendocrine Tumors","volume":"68","author":"Cives","year":"2018","journal-title":"CA A Cancer J. Clin."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1007\/s12022-022-09708-2","article-title":"Overview of the 2022 WHO Classification of Neuroendocrine Neoplasms","volume":"33","author":"Rindi","year":"2022","journal-title":"Endocr. Pathol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1335","DOI":"10.1001\/jamaoncol.2017.0589","article-title":"Trends in the Incidence, Prevalence, and Survival Outcomes in Patients with Neuroendocrine Tumors in the United States","volume":"3","author":"Dasari","year":"2017","journal-title":"JAMA Oncol."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Rossi, R.E., and Massironi, S. (2022). The Increasing Incidence of Neuroendocrine Neoplasms Worldwide: Current Knowledge and Open Issues. J. Clin. Med., 11.","DOI":"10.3390\/jcm11133794"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1634\/theoncologist.2016-0351","article-title":"Stage IV Gastro-Entero-Pancreatic Neuroendocrine Neoplasms: A Risk Score to Predict Clinical Outcome","volume":"22","author":"Panzuto","year":"2017","journal-title":"Oncol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"e13306","DOI":"10.1111\/jne.13306","article-title":"European Neuroendocrine Tumor Society (ENETS) 2023 guidance paper for gastroduodenal neuroendocrine tumours (NETs) G1\u2013G3","volume":"35","author":"Panzuto","year":"2023","journal-title":"J. Neuroendocr."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"e13105","DOI":"10.1111\/jne.13105","article-title":"ENETS standardized (synoptic) reporting for endoscopy in neuroendocrine tumors","volume":"34","author":"Borbath","year":"2023","journal-title":"J. Neuroendocr."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"e13309","DOI":"10.1111\/jne.13309","article-title":"European Neuroendocrine Tumor Society (ENETS) 2023 guidance paper for colorectal neuroendocrine tumours","volume":"35","author":"Rinke","year":"2023","journal-title":"J. Neuroendocr."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1055\/a-1811-7025","article-title":"Endoscopic submucosal dissection for superficial gastrointestinal lesions: European Society of Gastrointestinal Endoscopy (ESGE) Guideline\u2014Update 2022","volume":"54","author":"Bastiaansen","year":"2022","journal-title":"Endoscopy"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"757","DOI":"10.1007\/s00428-007-0452-1","article-title":"TNM staging of midgut and hindgut (neuro) endocrine tumors: A consensus proposal including a grading system","volume":"451","author":"Rindi","year":"2007","journal-title":"Virchows Arch."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1453","DOI":"10.1016\/S0140-6736(07)61602-X","article-title":"The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: Guidelines for reporting observational studies","volume":"370","author":"Altman","year":"2007","journal-title":"Lancet"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"World Medical Association (2013). World Medical Association Declaration of Helsinki: Ethical principles for medical research involving human subjects. JAMA, 310, 2191\u20132194.","DOI":"10.1001\/jama.2013.281053"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1327864","DOI":"10.3389\/fmed.2024.1327864","article-title":"Type 3 gastric neuroendocrine neoplasms: The rising promise of conservative endoscopic management","volume":"11","author":"Esposito","year":"2024","journal-title":"Front. Med."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"790","DOI":"10.1055\/s-0030-1256414","article-title":"Criteria for decision making after endoscopic resection of well-differentiated rectal carcinoids with regard to potential lymphatic spread","volume":"43","author":"Park","year":"2011","journal-title":"Endoscopy"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2021\/6679397","article-title":"Comparison of Endoscopic Techniques in the Management of Type I Gastric Neuroendocrine Neoplasia: A Systematic Review","volume":"2021","author":"Panzuto","year":"2021","journal-title":"Gastroenterol. Res. Pract."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"E1214","DOI":"10.1055\/a-1487-5594","article-title":"Comparison of endoscopic resection techniques for duodenal neuroendocrine tumors: Systematic review","volume":"9","author":"Brito","year":"2021","journal-title":"Endosc. Int. Open"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"412","DOI":"10.1055\/a-1751-5742","article-title":"Endoscopic management of subepithelial lesions including neuroendocrine neoplasms: European Society of Gastrointestinal Endoscopy (ESGE) Guideline","volume":"54","author":"Deprez","year":"2022","journal-title":"Endoscopy"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1111\/1751-2980.12279","article-title":"Long-term outcome of endoscopic and surgical resection for foregut neuroendocrine tumors","volume":"16","author":"Jung","year":"2015","journal-title":"J. Dig. Dis."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"890","DOI":"10.1016\/j.dld.2021.11.012","article-title":"Management of type-I gastric neuroendocrine neoplasms: A 10-years prospective single centre study","volume":"54","author":"Esposito","year":"2022","journal-title":"Dig. Liver Dis."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1480","DOI":"10.1002\/bjs.10901","article-title":"Clinicopathological features and outcome of type 3 gastric neuroendocrine tumours","volume":"105","author":"Min","year":"2018","journal-title":"Br. J. Surg."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"764","DOI":"10.1159\/000511613","article-title":"A \u201cWatch and Wait\u201d Strategy Involving Regular Endoscopic Surveillance Is Safe for Many Patients with Small, Sporadic, Grade 1, Non-Ampullary, Non-Functioning Duodenal Neuroendocrine Tumours","volume":"111","author":"Exarchou","year":"2021","journal-title":"Neuroendocrinology"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"378","DOI":"10.14309\/ajg.0000000000002516","article-title":"Systematic resection of the visible scar, after incomplete endoscopic resection of rectal neuroendocrine tumours","volume":"119","author":"Cheminel","year":"2023","journal-title":"Am. J. Gastroenterol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"785","DOI":"10.1080\/17474124.2023.2242261","article-title":"The meaning of R1 resection after endoscopic removal of gastric, duodenal and rectal neuroendocrine tumors","volume":"17","author":"Esposito","year":"2023","journal-title":"Expert Rev. Gastroenterol. Hepatol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1038\/s41572-024-00508-y","article-title":"Gastric neuroendocrine neoplasms","volume":"10","author":"Lamberti","year":"2024","journal-title":"Nat. Rev. Dis. Prim."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1016\/j.dld.2023.12.015","article-title":"Endoscopic management of gastric, duodenal and rectal NETs: Position paper from the Italian Association for Neuroendocrine Tumors (Itanet), Italian Society of Gastroenterology (SIGE), Italian Society of Digestive Endoscopy (SIED)","volume":"56","author":"Panzuto","year":"2024","journal-title":"Dig. Liver Dis."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"978","DOI":"10.1016\/j.dld.2015.07.155","article-title":"Intermittent treatment of recurrent type-1 gastric carcinoids with somatostatin analogues in patients with chronic autoimmune atrophic gastritis","volume":"47","author":"Massironi","year":"2015","journal-title":"Dig. Liver Dis."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1159\/000510962","article-title":"Selective Resection of Type 1 Gastric Neuroendocrine Neoplasms and the Risk of Progression in an Endoscopic Surveillance Programme","volume":"38","author":"Chin","year":"2021","journal-title":"Dig. Surg."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1007\/s12020-015-0584-z","article-title":"Clinical management of patients with gastric neuroendocrine neoplasms associated with chronic atrophic gastritis: A retrospective, multicentre study","volume":"51","author":"Campana","year":"2016","journal-title":"Endocrine"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1083","DOI":"10.1677\/ERC-08-0017","article-title":"Prognostic factors of long-term outcome in gastroenteropancreatic neuroendocrine tumours","volume":"15","author":"Pape","year":"2008","journal-title":"Endocrine-Related Cancer"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Magi, L., Mazzuca, F., Rinzivillo, M., Arrivi, G., Pilozzi, E., Prosperi, D., Iannicelli, E., Mercantini, P., Rossi, M., and Pizzichini, P. (2019). Multidisciplinary Management of Neuroendocrine Neoplasia: A Real-World Experience from a Referral Center. J. Clin. Med., 8.","DOI":"10.3390\/jcm8060910"}],"container-title":["Journal of Clinical Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0383\/13\/9\/2535\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:33:21Z","timestamp":1760106801000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0383\/13\/9\/2535"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,4,25]]},"references-count":30,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2024,5]]}},"alternative-id":["jcm13092535"],"URL":"https:\/\/doi.org\/10.3390\/jcm13092535","relation":{},"ISSN":["2077-0383"],"issn-type":[{"value":"2077-0383","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,4,25]]}}}