Disease relapse in relation to lymph node sampling in lung carcinoid patients

in Endocrine-Related Cancer
Authors:
Laura Moonen Department of Pathology, GROW School for Oncology and Reproduction, Maastricht University Medical Center+, Maastricht, The Netherlands

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Jules L Derks Department of Pathology, GROW School for Oncology and Reproduction, Maastricht University Medical Center+, Maastricht, The Netherlands
Department of Pulmonary Medicine, Erasmus MC Cancer Institute, University Medical Center, Rotterdam, The Netherlands

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Lisa M Hillen Department of Pulmonary Diseases, GROW School for Oncology and Reproduction, Maastricht University Medical Center+, Maastricht, The Netherlands

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Robert Jan van Suylen Pathology-DNA, Jeroen Bosch Hospital, s’Hertogenbosch, The Netherlands

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Michael A den Bakker Department of Pathology, Erasmus Medical Center, Rotterdam, The Netherlands

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Jan H von der Thüsen Department of Pathology, Maasstad Hospital, Rotterdam, The Netherlands

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Ronald A Damhuis Department of Research, Comprehensive Cancer Association, Utrecht, The Netherlands

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Wieneke A Buikhuisen Department of Thoracic Oncology, Netherlands Cancer Institute Amsterdam, The Netherlands

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Esther C van den Broek PALGA (Dutch Nationwide Pathology Databank), Houten, The Netherlands

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Jos Maessen Department of Cardiothoracic Surgery, Maastricht University Medical Center+, Maastricht, The Netherlands

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Alexander P W M Maat Department of Cardiothoracic Surgery, Erasmus MC, University Medical Center Rotterdam, Rotterdam, The Netherlands

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Paul van Schil Department of Thoracic and Vascular Surgery, Antwerp University Hospital, Antwerp, Belgium

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Ernst J M Speel Department of Pathology, GROW School for Oncology and Reproduction, Maastricht University Medical Center+, Maastricht, The Netherlands
Department of Pathology, Maasstad Hospital, Rotterdam, The Netherlands

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https://orcid.org/0000-0002-3016-2989
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A-M C Dingemans Department of Pulmonary Diseases, GROW School for Oncology and Reproduction, Maastricht University Medical Center+, Maastricht, The Netherlands
Department of Pulmonary Medicine, Erasmus MC Cancer Institute, University Medical Center, Rotterdam, The Netherlands

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Correspondence should be addressed to E J M Speel: ernstjan.speel@mumc.nl

*(E J M Speel and A-M C Dingemans contributed equally to this work)

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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 (2003–2012) 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 36.8–59.4). 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.

 

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  • Aydin E, Yazici U, Gulgosteren M, Agackiran Y, Kaya S, Gulhan E, Tastepe I & & Karaoglanoglu N 2011 Long-term outcomes and prognostic factors of patients with surgically treated pulmonary carcinoid: our institutional experience with 104 patients. European Journal of Cardio-Thoracic Surgery 39 549554. (https://doi.org/10.1016/j.ejcts.2010.08.010)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Baudin E, Caplin M, Garcia-Carbonero R, Fazio N, Ferolla P, Filosso P, Frilling A, de Herder W, Hörsch D, Knigge U, et al.2021 Lung and thymic carcinoids: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Annals of Oncology 32 439451. (https://doi.org/10.1016/j.annonc.2021.01.003)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Cañizares MA, Matilla J, Cueto A, Algar J, Muguruza I, Moreno-Mata N, Moreno-Balsalobre R, Guijarro R, Arrabal R, Garcia-Fontan E, et al.2014 Atypical carcinoid tumours of the lung: prognostic factors and patterns of recurrence. Thorax 69 648653. (https://doi.org/10.1136/thoraxjnl-2013-204102)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Caplin ME, Baudin E, Ferolla P, Filosso P, Garcia-Yuste M, Lim E, Oberg K, Pelosi G, Perren A, Rossi R, et al.2015 Pulmonary neuroendocrine (carcinoid) tumors: European Neuroendocrine Tumor Society expert consensus and recommendations for best practice for typical and atypical pulmonary carcinoids. Annals of Oncology 26 16041620. (https://doi.org/10.1093/annonc/mdv041)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Casparie M, Tiebosch A, Burger G, Blauwgeers H, Van de Pol A, van Krieken J & & Meijer G 2007 Pathology databanking and biobanking in the Netherlands, a central role for PALGA, the nationwide histopathology and cytopathology data network and archive. Cellular Oncology 29 1924. (https://doi.org/10.1155/2007/971816)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chughtai TS, Morin JE, Sheiner NM, Wilson JA & & Mulder DS 1997 Bronchial carcinoid—twenty years’ experience defines a selective surgical approach. Surgery 122 801808. (https://doi.org/10.1016/s0039-6060(9790090-8)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Cusumano G, Fournel L, Strano S, Damotte D, Charpentier MC, Galia A, Terminella A, Nicolosi M, Regnard JF & & Alifano M 2017 Surgical resection for pulmonary carcinoid: long-term results of multicentric study—the importance of pathological N status, more than we thought. Lung 195 789798. (https://doi.org/10.1007/s00408-017-0056-8)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Derks J, Rijnsburger N, Hermans B, Moonen L, Hillen L, von der Thüsen J, den Bakker M, van Suylen R, Speel E & & Dingemans A-M 2021 Clinical-pathological challenges in the classification of pulmonary neuroendocrine neoplasms and targets on the horizon for future clinical practice. Journal of Thoracic Oncology 16 16321646. (https://doi.org/10.1016/j.jtho.2021.05.020)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ferguson MK, Landreneau RJ, Hazelrigg SR, Altorki NK, Naunheim KS, Zwischenberger JB, Kent M & & Yim AP 2000 Long-term outcome after resection for bronchial carcinoid tumors. European Journal of Cardio-Thoracic Surgery 18 156161. (https://doi.org/10.1016/s1010-7940(0000493-0)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Filosso PL, Rena O, Donati G, Casadio C, Ruffini E, Papalia E, Oliaro A & & Maggi G 2002 Bronchial carcinoid tumors: surgical management and long-term outcome. Journal of Thoracic and Cardiovascular Surgery 123 303309. (https://doi.org/10.1067/mtc.2002.119886)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • García-Yuste M, Matilla JM, Cañizares MA, Molins L, Guijarro R, Members of the Spanish Multi-centric Study of Neuroendocrine Tumours of the Lung & Spanish Society of Pneumonology and Thoracic Surgery (EMETNE-SEPAR) 2017 Surgical treatment of low and intermediate grade lung net. Journal of Thoracic Disease 9(Supplement 15) S1435S1441. (https://doi.org/10.21037/jtd.2017.09.83)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lardinois D, De Leyn P, Van Schil P, Porta RR, Waller D, Passlick B, Zielinski M, Junker K, Rendina EA, Ris H-B, et al.2006 ESTS guidelines for intraoperative lymph node staging in non-small cell lung cancer. European Journal of Cardio-Thoracic Surgery 30 787792. (https://doi.org/10.1016/j.ejcts.2006.08.008)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lou F, Sarkaria I, Pietanza C, Travis W, Roh MS, Sica G, Healy D, Rusch V & & Huang J 2013 Recurrence of pulmonary carcinoid tumors after resection: implications for postoperative surveillance. Annals of Thoracic Surgery 96 11561162. (https://doi.org/10.1016/j.athoracsur.2013.05.047)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Moonen L, Derks JL, Hermans BC, Bunnik IM, Hillen LM, van Suylen RJ, den Bakker MA, von der Thüsen JH, Damhuis RA, van den Broek EC, et al.2021 Preoperative biopsy diagnosis in pulmonary carcinoids, a shot in the dark. Journal of Thoracic Oncology 16 610618. (https://doi.org/10.1016/j.jtho.2020.12.004)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Phan AT, Öberg K, Choi J, Harrison Jr LH, Hassan MM, Strosberg JR, Krenning EP, Kocha W, Woltering EA, Maples WJ, et al.2010 NANETS consensus guideline for the diagnosis and management of neuroendocrine tumors: well-differentiated neuroendocrine tumors of the thorax (includes lung and thymus). Pancreas 39 784798. (https://doi.org/10.1097/MPA.0b013e3181ec1380)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rami-Porta R, Bolejack V, Giroux DJ, Chansky K, Crowley J, Asamura H, Goldstraw P & International Association for the Study of Lung Cancer Staging and Prognostic Factors Committee, Advisory Board Members and Participating Institutions 2014 The IASLC lung cancer staging project: the new database to inform the eighth edition of the TNM classification of lung cancer. Journal of Thoracic Oncology 9 16181624. (https://doi.org/10.1097/JTO.0000000000000334)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rea F, Rizzardi G, Zuin A, Marulli G, Nicotra S, Bulf R, Schiavon M & & Sartori F 2007 Outcome and surgical strategy in bronchial carcinoid tumors: single institution experience with 252 patients. European Journal of Cardio-Thoracic Surgery 31 186191. (https://doi.org/10.1016/j.ejcts.2006.10.040)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Reuling E, Dickhoff C, Plaisier P, Bonjer H & & Daniels J 2019 Endobronchial and surgical treatment of pulmonary carcinoid tumors: a systematic literature review. Lung Cancer 134 8595. (https://doi.org/10.1016/j.lungcan.2019.04.016)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Robelin P, Hadoux J, Forestier J, Planchard D, Hervieu V, Berdelou A, Scoazec J-Y, Valette P-J, Leboulleux S, Ducreux M, et al.2019 Characterization, prognosis, and treatment of patients with metastatic lung carcinoid tumors. Journal of Thoracic Oncology 14 9931002. (https://doi.org/10.1016/j.jtho.2019.02.002)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Singh S, Bergsland EK, Card CM, Hope TA, Kunz PL, Laidley DT, Lawrence B, Leyden S, Metz DC, Michael M, et al.2020 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. Journal of Thoracic Oncology 15 15771598. (https://doi.org/10.1016/j.jtho.2020.06.021)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Swarts DR, van Suylen R-J, den Bakker MA, van Oosterhout MF, Thunnissen FB, Volante M, Dingemans A-MC, Scheltinga MR, Bootsma GP, Pouwels HM, et al.2014 Interobserver variability for the WHO classification of pulmonary carcinoids. American Journal of Surgical Pathology 38 14291436. (https://doi.org/10.1097/PAS.0000000000000300)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Travis WD, Brambilla E, Burke AP, Marx A & & Nicholson AG 2015 Introduction to the 2015 World Health Organization classification of tumors of the lung, pleura, thymus, and heart. Journal of Thoracic Oncology 10 12401242. (https://doi.org/10.1097/JTO.0000000000000663)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Vallieres E, Shepherd FA, Crowley J, Van Houtte P, Postmus PE, Carney D, Chansky K, Shaikh Z, Goldstraw P & International Association for the Study of Lung Cancer International Staging Committee and Participating Institutions 2009 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. Journal of Thoracic Oncology 4 10491059. (https://doi.org/10.1097/JTO.0b013e3181b27799)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Yoon JY, Sigel K, Martin J, Jordan R, Beasley MB, Smith C, Kaufman A, Wisnivesky J & & Kim MK 2019 Evaluation of the prognostic significance of TNM staging guidelines in lung carcinoid tumors. Journal of Thoracic Oncology 14 184192. (https://doi.org/10.1016/j.jtho.2018.10.166)

    • PubMed
    • Search Google Scholar
    • Export Citation