Pulmonary carcinoid tumours: incidence, histology, and surgical outcome. A population-based study

  • Astridur Petursdottir
  • Johanna Sigurdardottir
  • Bjorn M. Fridriksson
  • Arni Johnsen
  • Helgi J. Isaksson
  • Hronn Hardardottir
  • Steinn Jonsson
  • Tomas GudbjartssonEmail author
Original Article



Pulmonary carcinoids (PCs) represent only a minority of all primary pulmonary malignancies but they are the most common type of pulmonary malignancy diagnosed in children and adolescents. In this nationwide study, we analyzed data on all PC tumours in the Icelandic population over a 60-year period and concentrated especially on incidence and patient outcomes.


We studied all cases of PCs diagnosed in Iceland in the period 1955‒2015. Histological specimens were re-evaluated and the tumours were staged according to the TNM system (seventh edition). Survival was estimated using the Kaplan–Meier method, with a mean follow-up of 15.7 years.


Altogether, 88 patients (median age 51.0 years, 65.9% women) were diagnosed with PCs in the study period. The incidence increased from 0.19/100,000/year in the first decade (1955‒1964) to 0.58/100,000/year in the last decade (2005‒2015), with a mean increase of 29.0% per decade of the study period (p < 0.001). The rise in incidental detection was, however, not significant. The median tumour diameter was 2.2 cm (range 0.4‒7.0) and typical histology was seen in 74 patients (84.1%). The other 14 patients (15.9%) had atypical histology. In all, 90.9% of the patients underwent pulmonary resection, 81.2% of them with lobectomy, with all of them surviving at least 30 days postoperatively. Most patients (n = 52, 62.7%) were stage IA at diagnosis, 15 (18.1%) were stage IB, nine (10.8%) were stage IIA, and three were stage IIIA (3.6%). Four patients (4.8%) had distant metastases (stage IV), two of whom had typical histology. Five-year survival was 89.8% for all patients: 93.2% for patients with typical histology and 70.7% for those with atypical histology.


The incidence of PCs in Iceland has increased significantly over the last six decades, which cannot be explained by a rise in incidental detection at chest imaging. Most patients have localized disease and a favourable histology, where the long-term outcome is excellent.


Carcinoid tumour Pulmonary Incidence Survival Histology Nationwide 



  1. 1.
    Naalsund AR, Strom E, Lund M, Strand TE. Carcinoid lung tumors—incidence, treatment and outcomes: a population-based study. Eur J Cardiothorac Surg. 2011;39:565–9.PubMedCrossRefGoogle Scholar
  2. 2.
    Skuladottir HH, Hansen H, Olsen J. Pulmonary neuroendocrine tumors: Incidence and prognosis of histological subtypes. A population-based study in Denmark. Lung Cancer. 2002;37(2):127–35.PubMedCrossRefGoogle Scholar
  3. 3.
    Rekhtman N. Neuroendocrine tumors of the lung: an update. Arch Pathol Lab Med. 2010;134(11):1628–38.PubMedGoogle Scholar
  4. 4.
    Hallgrimsson J, Jonsson T, Johannsson J. Bronchopulmonary carcinoids in Iceland 1955–1984. A retrospective clinical and histopathologic study. Scand J Thorac Cardiovasc Surg. 1989;23(3):275–8.PubMedCrossRefGoogle Scholar
  5. 5.
    Gatta G, Ciccolallo L, Kunkler I, Capocaccia R, Berrino F, Coleman M, et al. Survival from rare cancer in adults: a population-based study. Lancet Oncol. 2006;7(2):132–40.PubMedCrossRefGoogle Scholar
  6. 6.
    Alsina M, Marcos-Gragera R, Capdevila J, Buxó M, Ortiz R, Barretina P, et al. Neuroendocrine tumors: a population-based study of incidence and survival in Girona Province, 1994–2004. Cancer Epidemiol. 2011;35(6):49–544.CrossRefGoogle Scholar
  7. 7.
    Fink G, Krelbaum T, Yellin A, Bendayan D, Saute M, Glazer M, et al. Pulmonary carcinoid: presentation, diagnosis, and outcome in 142 cases in Israel and review of 640 cases from the literature. Chest. 2001;119(6):1647–51.PubMedCrossRefGoogle Scholar
  8. 8.
    Hauso O, Gustafsson B, Kidd M, Waldum H, Drozdov I, Chan A, et al. Neuroendocrine tumor epidemiology: contrasting Norway and North America. Cancer. 2008;113(10):2655–64.PubMedCrossRefGoogle Scholar
  9. 9.
    Levi F, Te V, Randimbison L, Rindi G, La Vecchia C. Epidemiology of carcinoid neoplasms in Vaud, Switzerland, 1974–97. Br J Cancer. 2000;83(7):952–5.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Modlin I, Lye K, Kidd M. A 5-decade analysis of 13,715 carcinoid tumors. Cancer. 2003;97(4):934–59.PubMedCrossRefGoogle Scholar
  11. 11.
    Yao J, Hassan M, Phan A, Dagohoy C, Leary C, Mares J, et al. 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.CrossRefGoogle Scholar
  12. 12.
    Hemminki K, Li X. Familial carcinoid tumors and subsequent cancer: a nation-wide epidemiologic study from Sweden. Int J Cancer. 2001;94(3):444–8.PubMedCrossRefGoogle Scholar
  13. 13.
    Hemminki K, Li X. Incidence trends and risk factors of carcinoid tumors: a nationwide epidemiologic study from Sweden. Cancer. 2001;92(8):2204–10.PubMedCrossRefGoogle Scholar
  14. 14.
    Hassan M, Phan A, Li D, Dagohoy C, Leary C, Yao J. Risk factors associated with neuroendocrine tumors: A U.S.-based case-control study. Int J Cancer. 2008;123(4):867–73.PubMedCrossRefGoogle Scholar
  15. 15.
    Filosso P, Rena O, Donati G, Casadio C, Ruffini E, Papalia E, et al. Bronchial carcinoid tumors: surgical management and long-term outcome. J Thorac Cardiovasc Surg. 2002;123(2):303–9.PubMedCrossRefGoogle Scholar
  16. 16.
    Hartman G, Schochat S. Primary pulmonary neoplasms of childhood: a review. Ann Thorac Surg. 1983;36(1):108–19.PubMedCrossRefGoogle Scholar
  17. 17.
    Wang L, Wilkins EJ, Bode H. Bronchial carcinoid tumors in pediatric patients. Chest. 1993;103(5):1426–8.PubMedCrossRefGoogle Scholar
  18. 18.
    Travis W, Brambilla E, Müller-Hermelink H, Harris C, editors. Pathology and genetics of tumours of the lung, pleura, thymus and heart. Lyon: IARC Press; 2004.Google Scholar
  19. 19.
    Arrigoni M, Woolner L, Bernatz P. Atypical carcinoid tumors of the lung. J Thorac Cardiovasc Surg. 1972;64(3):413–21.PubMedPubMedCentralGoogle Scholar
  20. 20.
    Travis W, Colby T, Corrin B, Shimosato Y, Brambilla E. Histological typing of lung and pleural tumours. New York: Springer; 1999.CrossRefGoogle Scholar
  21. 21.
    Lim E, Yap Y, De Stavola B, Nicholson A, Goldstraw P. The impact of stage and cell type on the prognosis of pulmonary neuroendocrine tumors. J Thorac Cardiovasc Surg. 2005;130(4):969–72.PubMedCrossRefGoogle Scholar
  22. 22.
    Cao C, Yan T, Kennedy C, Hendel N, Bannon P, McCaughan B. Bronchopulmonary Carcinoid Tumors: Long-term outcomes after resection. Ann Thorac Surg. 2011;91(2):339–43.PubMedCrossRefGoogle Scholar
  23. 23.
    Sigurdardottir J, Isaksson H, Johannsson K, Jonsson S, Gudbjartsson T. Vefjagerð krabbalíkisæxla í lungum spáir ekki fyrir um klíníska hegðum - Niðurstöður úr íslenskri rannsókn. Icelandic Med J. 2008;94(2):125–30.Google Scholar
  24. 24.
    Froudarakis M, Fournel P, Burgard D, Bouros D, Boucheron S, Siafakas N, et al. Bronchial carcinoids. A review of 22 cases. Oncology. 1996;53(2):152–8.CrossRefGoogle Scholar
  25. 25.
    Bertino E, Confer P, Colonna J, Ross P, Otterson G. Pulmonary neuroendocrine/carcinoid tumors: a review article. Cancer. 2009;115:4434–41.PubMedCrossRefGoogle Scholar
  26. 26.
    Caplin M, Baudin E, Ferolla P, Filosso P, Garcia-Yuste M, Lim E, et al. Pulmonary neuroendocrine (carcinoid) tumors: European Neuroendocrine Tumor Society expert consensus and recommendations for best practice for typical and atypical pulmonary carcinoids. Ann Oncol. 2015;26(8):1604–20.PubMedCrossRefGoogle Scholar
  27. 27.
    Edge S, Byrd D, Compton C, Fritz A. AJCC cancer staging manual. 7th ed. New York: Springer; 2010.Google Scholar
  28. 28.
    Anderson R, Rosenberg H. Age standardization of death rates: implementation of the year 2000 standard. Natl Vital Stat Rep. 1998;47(3):1–16 (20).PubMedGoogle Scholar
  29. 29.
    Keshgegian A, Wheeler J. Estrogen receptor protein in malignant carcinoid tumor. Cancer. 1980;45:293–6.PubMedCrossRefGoogle Scholar
  30. 30.
    Gustafsson B, Kidd M, Chan A, Malfertheiner M, Modlin I. Bronchopulmonary neuroendocrine tumors. Cancer. 2008;113:5–21.PubMedCrossRefGoogle Scholar
  31. 31.
    Greenberg R, Baumgarten B, Clark W, Isacson P, McKeen K. Prognostic factors for gastrointestinal and bronchopulmonary tumors. Cancer. 1987;60:2476–83.PubMedCrossRefGoogle Scholar
  32. 32.
    Soga J, Yakuwa Y. Bronchopulmonary carcinoids: an analysis of 1,875 reported cases with special reference to a comparison between typical carcinoids and atypical varieties. Ann Thorac Cardiovasc Surg. 1999;5:211–9.PubMedGoogle Scholar
  33. 33.
    Kayser K, Kayser C, Rahn W, Bovin N, Gabius H. Carcinoid tumors of the lung: immuno- and ligandohistochemistry, analysis of integrated optical density, syntactic structure analysis, clinical data, and prognosis of patients treated surgically. J Surg Oncol. 1996;63(2):99–106.PubMedCrossRefGoogle Scholar
  34. 34.
    Schlüter C, Duchrow M, Wohlenberg C, Becker M, Key G, Flad H, et al. The cell proliferation-associated antigen of antibody Ki-67: a very large, ubiquitous nuclear protein with numerous repeated elements, representing a new kind of cell cycle-maintaining proteins. J Cell Biol. 1993;123(3):513–22.PubMedCrossRefGoogle Scholar
  35. 35.
    Rindi G, Klöppel G, Alhman H, Caplin M, Couvelard A, de Herder W, et al. TNM staging of foregut (neuro)endocrine tumors: a consensus proposal including a grading system. Virchows Arch. 2006;449(4):395–401.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Guiu S, Michiels S, Andre F, Cortes J, Denkert C, Di Leo A, et al. Molecular subclasses of breast cancer: how do we define them? The IMPAKT 2012 Working Group Statement. Ann Oncol. 2012;23(12):2997–3006.PubMedCrossRefGoogle Scholar
  37. 37.
    Travis W, Brambilla E, Burke A, Marx A, Nicholson A, editors. WHO classification of tumours of the lung, pleura, thymus and heart. 4th ed. Lyon: World Health Organization Classification of Tumours. 4. útg. IARC Press; 2015.Google Scholar
  38. 38.
    Travis W, Brambilla E, Nicholson A, Yatabe Y, Austin J, Beasley M, et al. The 2015 World Health Organization classification of lung tumors: impact of genetic, clinical and radiologic advances since the 2004 classification. J Thorac Oncol. 2015;10(9):1243–60.PubMedCrossRefGoogle Scholar
  39. 39.
    Travis W, Giroux D, Chansky K, Crowley J, Asamura H, Brambilla E, et al. The IASLC Lung Cancer Staging Project: proposals for the inclusion of broncho-pulmonary carcinoid tumors in the forthcoming (seventh) edition of the TNM Classification for Lung Cancer. J Thorac Oncol. 2008;3(11):1213–23.PubMedCrossRefGoogle Scholar
  40. 40.
    Cattoni M, Vallieres E, Brown L, Sakeshik A, Margaritora S, Siciliani A, et al. Improvement in TNM staging of pulmonary neuroendocrine tumors requires histology and regrouping of tumor size. J Thorac Cardiovasc Surg. 2018;155(1):405–13.PubMedCrossRefGoogle Scholar
  41. 41.
    Lee M-C, Aly R, Adusumilli P. New staging system for pulmonary neuroendocrine tumors: a clinical and pathologic necessity. J Thorac Cardiovasc Surg. 2018;155(1):367–8.PubMedCrossRefGoogle Scholar
  42. 42.
    Kay F, Kandathil A, Batra K, Saboo S, Abbara S, Rajiah P. Revisions to the tumor, node, metastasis staging of lung cancer (8th edition): rationale, radiologic findings and clinical implications. World J Radiol. 2017;9(6):269–79.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Ferguson M, Landreneau R, Hazelrigg S, Altorki N, Naunheim K, Zwischenberger J, et al. Long-term outcome after resection for bronchial carcinoid tumors. Eur J Cardiothorac Surg. 2000;18(2):156–61.PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Sadowski S, Christ E, Bedat B, Kollar A, Karenovics W, Perren A, et al. Nationwide multicenter study on the management of pulmonary endocrine (carcinoid) tumors. Endocr Connect. 2018;7(1):8–15.PubMedCrossRefGoogle Scholar

Copyright information

© The Japanese Association for Thoracic Surgery 2019

Authors and Affiliations

  • Astridur Petursdottir
    • 1
  • Johanna Sigurdardottir
    • 4
  • Bjorn M. Fridriksson
    • 1
  • Arni Johnsen
    • 5
  • Helgi J. Isaksson
    • 3
  • Hronn Hardardottir
    • 2
  • Steinn Jonsson
    • 2
    • 5
  • Tomas Gudbjartsson
    • 1
    • 5
    Email author
  1. 1.Department of Cardiothoracic SurgeryLandspitali University HospitalReykjavikIceland
  2. 2.Department of PulmonologyLandspitali University HospitalReykjavikIceland
  3. 3.Department of PathologyLandspitali University HospitalReykjavikIceland
  4. 4.Department of SurgeryVasteras County HospitalReykjavikIceland
  5. 5.Faculty of MedicineUniversity of IcelandReykjavikIceland

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