{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T04:41:53Z","timestamp":1790052113135,"version":"4.0.1"},"reference-count":24,"publisher":"Bioscientifica","issue":"9","content-domain":{"domain":["erc.bioscientifica.com"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2024,6,10]]},"abstract":"<jats:p>The predictive value of the extent of peri-operative lymph node (LN) sampling in relation to disease relapse in patients with pulmonary carcinoid (PC) is unknown. Furthermore, post-surgery follow-up recommendations rely on institutional retrospective studies with short follow-ups. We aimed to address these shortcomings by examining the relation between LN sampling and relapse in a population-based cohort with long-term follow-up. By combining the Dutch nationwide pathology and cancer registries, all patients with surgically resected PC (2003\u20132012) were included in this analysis (last update 2020). The extent of surgical LN dissection was scored for the number of LN samples, location (hilar\/mediastinal), and completeness of resection according to European Society of Thoracic Surgeons (ESTS) guidelines. Relapse-free interval (RFI) was evaluated using Kaplan Meier and multivariate regression analysis. 662 patients were included. The median follow-up was 87.5 months. Relapse occurred in 10% of patients, mostly liver (51.8%) and locoregional sites (45%). The median RFI was 48.1 months (95% CI 36.8\u201359.4). Poor prognostic factors were atypical carcinoid, pN1\/2, and R1\/R2 resection. In 546 patients LN dissection data could be retrieved; at least one N2 LN was examined in 44% and completeness according to ESTS in merely 7%. In 477 cN0 patients, 5.9% had pN1 and 2.5% had pN2 disease. In conclusion, relapse occurred in 10% of PC patients with a median RFI of 48.1 months thereby underscoring the necessity of long-term follow-up. Extended mediastinal LN sampling was rarely performed but systematic nodal evaluation is recommended as it provides prognostic information on distant relapse.<\/jats:p>","DOI":"10.1530\/erc-23-0202","type":"journal-article","created":{"date-parts":[[2024,6,10]],"date-time":"2024-06-10T07:15:38Z","timestamp":1718003738000},"update-policy":"https:\/\/doi.org\/10.1530\/crossmarkpolicy-8","source":"Crossref","is-referenced-by-count":7,"title":["Disease relapse in relation to lymph node sampling in lung carcinoid patients"],"prefix":"10.1530","volume":"31","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3699-2534","authenticated-orcid":true,"given":"Laura","family":"Moonen","sequence":"first","affiliation":[{"name":"Department of Pathology, GROW School for Oncology and Reproduction, Maastricht University Medical Center+, Maastricht, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jules L","family":"Derks","sequence":"additional","affiliation":[{"name":"Department of Pathology, GROW School for Oncology and Reproduction, Maastricht University Medical Center+, Maastricht, The Netherlands"},{"name":"Department of Pulmonary Medicine, Erasmus MC Cancer Institute, University Medical Center, Rotterdam, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lisa M","family":"Hillen","sequence":"additional","affiliation":[{"name":"Department of Pulmonary Diseases, GROW School for Oncology and Reproduction, Maastricht University Medical Center+, Maastricht, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robert Jan","family":"van Suylen","sequence":"additional","affiliation":[{"name":"Pathology-DNA, Jeroen Bosch Hospital, s\u2019Hertogenbosch, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael A","family":"den Bakker","sequence":"additional","affiliation":[{"name":"Department of Pathology, Erasmus Medical Center, Rotterdam, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jan H von der","family":"Th\u00fcsen","sequence":"additional","affiliation":[{"name":"Department of Pathology, Maasstad Hospital, Rotterdam, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ronald A","family":"Damhuis","sequence":"additional","affiliation":[{"name":"Department of Research, Comprehensive Cancer Association, Utrecht, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wieneke A","family":"Buikhuisen","sequence":"additional","affiliation":[{"name":"Department of Thoracic Oncology, Netherlands Cancer Institute Amsterdam, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Esther C","family":"van den Broek","sequence":"additional","affiliation":[{"name":"PALGA (Dutch Nationwide Pathology Databank), Houten, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jos","family":"Maessen","sequence":"additional","affiliation":[{"name":"Department of Cardiothoracic Surgery, Maastricht University Medical Center+, Maastricht, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexander P W M","family":"Maat","sequence":"additional","affiliation":[{"name":"Department of Cardiothoracic Surgery, Erasmus MC, University Medical Center Rotterdam, Rotterdam, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paul","family":"van Schil","sequence":"additional","affiliation":[{"name":"Department of Thoracic and Vascular Surgery, Antwerp University Hospital, Antwerp, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3016-2989","authenticated-orcid":true,"given":"Ernst J M","family":"Speel","sequence":"additional","affiliation":[{"name":"Department of Pathology, GROW School for Oncology and Reproduction, Maastricht University Medical Center+, Maastricht, The Netherlands"},{"name":"Department of Pathology, Maasstad Hospital, Rotterdam, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"A-M C","family":"Dingemans","sequence":"additional","affiliation":[{"name":"Department of Pulmonary Diseases, GROW School for Oncology and Reproduction, Maastricht University Medical Center+, Maastricht, The Netherlands"},{"name":"Department of Pulmonary Medicine, Erasmus MC Cancer Institute, University Medical Center, Rotterdam, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"416","reference":[{"key":"bib1","series-title":"European Journal of Cardio-Thoracic Surgery","first-page":"549","article-title":"Long-term outcomes and prognostic factors of patients with surgically treated pulmonary carcinoid: our institutional experience with 104 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(https:\/\/doi.org\/10.1016\/j.jtho.2021.05.020)"},{"key":"bib9","series-title":"European Journal of Cardio-Thoracic Surgery","first-page":"156","article-title":"Long-term outcome after resection for bronchial carcinoid tumors","volume":"18","author":"Ferguson","year":"2000","unstructured":"Ferguson MKLandreneau RJHazelrigg SRAltorki NKNaunheim KSZwischenberger JBKent M & Yim AP2000Long-term outcome after resection for bronchial carcinoid tumors. European Journal of Cardio-Thoracic Surgery18156\u2013161. (https:\/\/doi.org\/10.1016\/s1010-7940(0000493-0)"},{"key":"bib10","series-title":"Journal of Thoracic and Cardiovascular Surgery","first-page":"303","article-title":"Bronchial carcinoid tumors: surgical management and long-term outcome","volume":"123","author":"Filosso","year":"2002","unstructured":"Filosso PLRena ODonati GCasadio CRuffini EPapalia EOliaro A & Maggi G2002Bronchial carcinoid tumors: surgical management and long-term outcome. Journal of Thoracic and Cardiovascular Surgery123303\u2013309. (https:\/\/doi.org\/10.1067\/mtc.2002.119886)"},{"issue":"Supplement 15","key":"bib11","series-title":"Journal of Thoracic Disease","first-page":"S1435","article-title":"Surgical treatment of low and intermediate grade lung net","volume":"9","author":"Garc\u00eda-Yuste","year":"2017","unstructured":"Garc\u00eda-Yuste MMatilla JMCa\u00f1izares MAMolins LGuijarro R, Members of the Spanish Multi-centric Study of Neuroendocrine Tumours of the Lung & Spanish Society of Pneumonology and Thoracic Surgery (EMETNE-SEPAR)2017Surgical treatment of low and intermediate grade lung net. Journal of Thoracic Disease9(Supplement 15) S1435\u2013S1441. (https:\/\/doi.org\/10.21037\/jtd.2017.09.83)"},{"key":"bib12","series-title":"European Journal of Cardio-Thoracic Surgery","first-page":"787","article-title":"ESTS guidelines for intraoperative lymph node staging in non-small cell lung cancer","volume":"30","author":"Lardinois","year":"2006","unstructured":"Lardinois DDe Leyn PVan Schil PPorta RRWaller DPasslick BZielinski MJunker KRendina EARis H-B, et al.2006ESTS guidelines for intraoperative lymph node staging in non-small cell lung cancer. European Journal of Cardio-Thoracic Surgery30787\u2013792. 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(https:\/\/doi.org\/10.1016\/j.athoracsur.2013.05.047)"},{"key":"bib14","series-title":"Journal of Thoracic Oncology","first-page":"610","article-title":"Preoperative biopsy diagnosis in pulmonary carcinoids, a shot in the dark","volume":"16","author":"Moonen","year":"2021","unstructured":"Moonen LDerks JLHermans BCBunnik IMHillen LMvan Suylen RJden Bakker MAvon der Th\u00fcsen JHDamhuis RAvan den Broek EC, et al.2021Preoperative biopsy diagnosis in pulmonary carcinoids, a shot in the dark. Journal of Thoracic Oncology16610\u2013618. (https:\/\/doi.org\/10.1016\/j.jtho.2020.12.004)"},{"key":"bib15","series-title":"Pancreas","first-page":"784","article-title":"NANETS consensus guideline for the diagnosis and management of neuroendocrine tumors: well-differentiated neuroendocrine tumors of the thorax (includes lung and thymus)","volume":"39","author":"Phan","year":"2010","unstructured":"Phan AT\u00d6berg KChoi JHarrison Jr LHHassan MMStrosberg JRKrenning EPKocha WWoltering EAMaples WJ, et al.2010NANETS consensus guideline for the diagnosis and management of neuroendocrine tumors: well-differentiated neuroendocrine tumors of the thorax (includes lung and thymus). Pancreas39784\u2013798. (https:\/\/doi.org\/10.1097\/MPA.0b013e3181ec1380)"},{"key":"bib16","series-title":"Journal of Thoracic Oncology","first-page":"1618","article-title":"The IASLC lung cancer staging project: the new database to inform the eighth edition of the TNM classification of lung cancer","volume":"9","author":"Rami-Porta","year":"2014","unstructured":"Rami-Porta RBolejack VGiroux DJChansky KCrowley JAsamura HGoldstraw P & International Association for the Study of Lung Cancer Staging and Prognostic Factors Committee, Advisory Board Members and Participating Institutions2014The IASLC lung cancer staging project: the new database to inform the eighth edition of the TNM classification of lung cancer. Journal of Thoracic Oncology91618\u20131624. (https:\/\/doi.org\/10.1097\/JTO.0000000000000334)"},{"key":"bib17","series-title":"European Journal of Cardio-Thoracic Surgery","first-page":"186","article-title":"Outcome and surgical strategy in bronchial carcinoid tumors: single institution experience with 252 patients","volume":"31","author":"Rea","year":"2007","unstructured":"Rea FRizzardi GZuin AMarulli GNicotra SBulf RSchiavon M & Sartori F2007Outcome and surgical strategy in bronchial carcinoid tumors: single institution experience with 252 patients. European Journal of Cardio-Thoracic Surgery31186\u2013191. (https:\/\/doi.org\/10.1016\/j.ejcts.2006.10.040)"},{"key":"bib18","series-title":"Lung Cancer","first-page":"85","article-title":"Endobronchial and surgical treatment of pulmonary carcinoid tumors: a systematic literature review","volume":"134","author":"Reuling","year":"2019","unstructured":"Reuling EDickhoff CPlaisier PBonjer H & Daniels J2019Endobronchial and surgical treatment of pulmonary carcinoid tumors: a systematic literature review. Lung Cancer13485\u201395. (https:\/\/doi.org\/10.1016\/j.lungcan.2019.04.016)"},{"key":"bib19","series-title":"Journal of Thoracic Oncology","first-page":"993","article-title":"Characterization, prognosis, and treatment of patients with metastatic lung carcinoid tumors","volume":"14","author":"Robelin","year":"2019","unstructured":"Robelin PHadoux JForestier JPlanchard DHervieu VBerdelou AScoazec J-YValette P-JLeboulleux SDucreux M, et al.2019Characterization, prognosis, and treatment of patients with metastatic lung carcinoid tumors. Journal of Thoracic Oncology14993\u20131002. (https:\/\/doi.org\/10.1016\/j.jtho.2019.02.002)"},{"key":"bib20","series-title":"Journal of Thoracic Oncology","first-page":"1577","article-title":"Commonwealth neuroendocrine tumour research collaboration and the North American neuroendocrine tumor society guidelines for the diagnosis and management of patients with lung neuroendocrine tumors: an international collaborative endorsement and update of the 2015 European Neuroendocrine Tumor Society expert consensus guidelines","volume":"15","author":"Singh","year":"2020","unstructured":"Singh SBergsland EKCard CMHope TAKunz PLLaidley DTLawrence BLeyden SMetz DCMichael M, et al.2020Commonwealth neuroendocrine tumour research collaboration and the North American neuroendocrine tumor society guidelines for the diagnosis and management of patients with lung neuroendocrine tumors: an international collaborative endorsement and update of the 2015 European Neuroendocrine Tumor Society expert consensus guidelines. Journal of Thoracic Oncology151577\u20131598. (https:\/\/doi.org\/10.1016\/j.jtho.2020.06.021)"},{"key":"bib21","series-title":"American Journal of Surgical Pathology","first-page":"1429","article-title":"Interobserver variability for the WHO classification of pulmonary carcinoids","volume":"38","author":"Swarts","year":"2014","unstructured":"Swarts DRvan Suylen R-Jden Bakker MAvan Oosterhout MFThunnissen FBVolante MDingemans A-MCScheltinga MRBootsma GPPouwels HM, et al.2014Interobserver variability for the WHO classification of pulmonary carcinoids. American Journal of Surgical Pathology381429\u20131436. (https:\/\/doi.org\/10.1097\/PAS.0000000000000300)"},{"key":"bib22","series-title":"Journal of Thoracic Oncology","first-page":"1240","article-title":"Introduction to the 2015 World Health Organization classification of tumors of the lung, pleura, thymus, and heart","volume":"10","author":"Travis","year":"2015","unstructured":"Travis WDBrambilla EBurke APMarx A & Nicholson AG2015Introduction to the 2015 World Health Organization classification of tumors of the lung, pleura, thymus, and heart. Journal of Thoracic Oncology101240\u20131242. (https:\/\/doi.org\/10.1097\/JTO.0000000000000663)"},{"key":"bib23","series-title":"Journal of Thoracic Oncology","first-page":"1049","article-title":"The IASLC Lung Cancer Staging Project: proposals regarding the relevance of TNM in the pathologic staging of small cell lung cancer in the forthcoming (seventh) edition of the TNM classification for lung cancer","volume":"4","author":"Vallieres","year":"2009","unstructured":"Vallieres EShepherd FACrowley JVan Houtte PPostmus PECarney DChansky KShaikh ZGoldstraw P & International Association for the Study of Lung Cancer International Staging Committee and Participating Institutions2009The IASLC Lung Cancer Staging Project: proposals regarding the relevance of TNM in the pathologic staging of small cell lung cancer in the forthcoming (seventh) edition of the TNM classification for lung cancer. Journal of Thoracic Oncology41049\u20131059. (https:\/\/doi.org\/10.1097\/JTO.0b013e3181b27799)"},{"key":"bib24","series-title":"Journal of Thoracic Oncology","first-page":"184","article-title":"Evaluation of the prognostic significance of TNM staging guidelines in lung carcinoid tumors","volume":"14","author":"Yoon","year":"2019","unstructured":"Yoon JYSigel KMartin JJordan RBeasley MBSmith CKaufman AWisnivesky J & Kim MK2019Evaluation of the prognostic significance of TNM staging guidelines in lung carcinoid tumors. Journal of Thoracic Oncology14184\u2013192. 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