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Open Access 18-03-2022 | Carcinoid Tumor | Original Article

Prognostic significance of laterality in lung neuroendocrine tumors

Authors: Anna La Salvia, Irene Persano, Alessandra Siciliani, Monica Verrico, Massimiliano Bassi, Roberta Modica, Alessandro Audisio, Isabella Zanata, Beatrice Trabalza Marinucci, Elena Trevisi, Giulia Puliani, Maria Rinzivillo, Elena Parlagreco, Roberto Baldelli, Tiziana Feola, Franz Sesti, Paola Razzore, Rossella Mazzilli, Massimiliano Mancini, Francesco Panzuto, Marco Volante, Elisa Giannetta, Carmen Romero, Marialuisa Appetecchia, Andrea Isidori, Federico Venuta, Maria Rosaria Ambrosio, Maria Chiara Zatelli, Mohsen Ibrahim, Annamaria Colao, Maria Pia Brizzi, Rocío García-Carbonero, Antongiulio Faggiano

Published in: Endocrine | Issue 3/2022

Abstract

Purpose:

Well-differentiated lung neuroendocrine tumors (Lu-NET) are classified as typical (TC) and atypical (AC) carcinoids, based on mitotic counts and necrosis. However, prognostic factors, other than tumor node metastasis (TNM) stage and the histopathological diagnosis, are still lacking. The current study is aimed to identify potential prognostic factors to better stratify lung NET, thus, improving patients’ treatment strategy and follow-up.

Methods:

A multicentric retrospective study, including 300 Lung NET, all surgically removed, from Italian and Spanish Institutions.

Results:

Median age 61 years (13–86), 37.7% were males, 25.0% were AC, 42.0% were located in the lung left parenchyma, 80.3% presented a TNM stage I-II. Mitotic count was ≥2 per 10 high-power field (HPF) in 24.7%, necrosis in 13.0%. Median overall survival (OS) was 46.1 months (0.6–323), median progression-free survival (PFS) was 36.0 months (0.3–323). Female sex correlated with a more indolent disease (T1; N0; lower Ki67; lower mitotic count and the absence of necrosis). Left-sided primary tumors were associated with higher mitotic count and necrosis. At Cox-multivariate regression model, age, left-sided tumors, nodal (N) positive status and the diagnosis of AC resulted independent negative prognostic factors for PFS and OS.

Conclusions:

This study highlights that laterality is an independent prognostic factors in Lu-NETs, with left tumors being less frequent but showing a worse prognosis than right ones. A wider spectrum of clinical and pathological prognostic factors, including TNM stage, age and laterality is suggested. These parameters could help clinicians to personalize the management of Lu-NET.

Available only for authorised users

WHO Classification of Tumors Editorial Board. Thoracic tumours. 5th edn. (International Agency for Research on Cancer World Health Organisation, Lyon, 2021).

J. Wang, L. Ye, H. Cai, M. Jin, Comparative study of large cell neuroendocrine carcinoma and small cell lung carcinoma in high-grade neuroendocrine tumors of the lung: a large population-based study. J. Cancer 10(18), 4226–4236 (2019). https://doi.org/10.7150/jca.33367CrossRefPubMedPubMedCentral

P.L. Filosso, O. Rena, G. Donati, C. Casadio, E. Ruffini, E. Papalia et al. Bronchial carcinoid tumors: surgical management and long-term outcome. J. Thorac. Cardiovasc. Surg. 123(2), 303–309 (2002). https://doi.org/10.1067/mtc.2002.119886CrossRefPubMed

M.E. Caplin, E. Baudin, P. Ferolla, P. Filosso, M. Garcia-Yuste, E. Lim 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. Off. J. Eur. SocMed. Oncol. 26(8), 1604–1620 (2015). https://doi.org/10.1093/annonc/mdv041CrossRef

E.M. Wolin, Challenges in the diagnosis and management of well-differentiated neuroendocrine tumors of the lung (typical and atypical carcinoid): current status and future considerations. The Oncologist 20(10), 1123–1131 (2015). https://doi.org/10.1634/theoncologist.2015-0198CrossRefPubMedPubMedCentral

O. Abdel-Rahman, Modified staging system for pulmonary carcinoids on the basis of lung cancer TNM system. Clin. Transl. Oncol. Off. Publ. Fed. Span Oncol. Soc. Natl Cancer Inst. Mex. 20(5), 670–677 (2018). https://doi.org/10.1007/s12094-017-1759-2CrossRef

P.J. Kneuertz, M.K. Kamel, B.M. Stiles, B.E. Lee, M. Rahouma, S.W. Harrison et al. Incidence and prognostic significance of carcinoid lymph node metastases. Ann. Thorac. Surg. 106(4), 981–988 (2018). https://doi.org/10.1016/j.athoracsur.2018.05.044CrossRefPubMed

M. Cattoni, E. Vallières, L.M. Brown, A.A. Sarkeshik, S. Margaritora, A. Siciliani et al. Improvement in TNM staging of pulmonary neuroendocrine tumors requires histology and regrouping of tumor size. J. Thorac. Cardiovasc. Surg. 155(1), 405–413 (2018). https://doi.org/10.1016/j.jtcvs.2017.08.102CrossRefPubMed

A.S. Jackson, A. Rosenthal, M. Cattoni, A.J. Bograd, A.S. Farivar, R.W. Aye et al. Staging system for neuroendocrine tumors of the lung needs to incorporate histologic grade. Ann. Thorac. Surg. 109(4), 1009–1018 (2020). https://doi.org/10.1016/j.athoracsur.2019.09.053CrossRefPubMed

10.

H. Qiu, B.-M. Jin, Z.-F. Wang, B. Xu, Q.-F. Zheng, L. Zhang et al. MEN1 deficiency leads to neuroendocrine differentiation of lung cancer and disrupts the DNA damage response. Nat. Commun. 11(1), 1009 (2020). https://doi.org/10.1038/s41467-020-14614-4CrossRefPubMedPubMedCentral

11.

L. Fernandez-Cuesta, M. Peifer, X. Lu, R. Sun, L. Ozretić, D. Seidal et al. Frequent mutations in chromatin-remodelling genes in pulmonary carcinoids. Nat. Commun. 5, 3518 (2014). https://doi.org/10.1038/ncomms4518CrossRefPubMed

12.

M. Velinovic, R. Jankovic, D. Jovanovic, V. Skodric Trifunovic, D. Gavrilovic, J. Stojsic et al. Tumor characteristics, expressions of ERCC1, Bax, p53, IGF1R, Bcl2, Bcl2/Bax and prognostic factors for overall survival in patients with lung carcinoid. J. BUON 24(1), 256–266 (2019).PubMed

13.

A.K. Walch, H.F. Zitzelsberger, M.M. Aubele, A.E. Mattis, M. Bauchinger, S. Candidus et al. Typical and atypical carcinoid tumors of the lung are characterized by 11q deletions as detected by comparative genomic hybridization. Am. J. Pathol. 153(4), 1089–1098 (1998). https://doi.org/10.1016/S0002-9440(10)65653-2CrossRefPubMedPubMedCentral

14.

D. Moris, I. Ntanasis-Stathopoulos, D.I. Tsilimigras, M.A. Adam, C.-F.J. Yang, D. Harpole et al. Insights into novel prognostic and possible predictive biomarkers of lung neuroendocrine tumors. Cancer Genom. Proteom. 15(2), 153–163 (2018). https://doi.org/10.21873/cgp.20073CrossRef

15.

M. Simbolo, A. Mafficini, K.O. Sikora, M. Fassan, S. Barbi, V. Corbo et al. Lung neuroendocrine tumours: deep sequencing of the four World Health Organization histotypes reveals chromatin-remodelling genes as major players and a prognostic role for TERT, RB1, MEN1 and KMT2D. J. Pathol. 241(4), 488–500 (2017). https://doi.org/10.1002/path.4853CrossRefPubMed

16.

N. Alcala, N. Leblay, A.A.G. Gabriel, L. Mangiante, D. Hervas, T. Giffon et al. Integrative and comparative genomic analyses identify clinically relevant pulmonary carcinoid groups and unveil the supra-carcinoids. Nat. Commun. 10(1), 3407 (2019). https://doi.org/10.1038/s41467-019-11276-9CrossRefPubMedPubMedCentral

17.

J.Y. Kim, S.-M. Hong, J.Y. Ro, Recent updates on grading and classification of neuroendocrine tumors. Ann. Diagn. Pathol. 29, 11–16 (2017). https://doi.org/10.1016/j.anndiagpath.2017.04.005CrossRefPubMed

18.

M. Volante, G. Gatti, M. Papotti, Classification of lung neuroendocrine tumors: lights and shadows. Endocrine 50(2), 315–319 (2015). https://doi.org/10.1007/s12020-015-0578-xCrossRefPubMed

19.

B.C.M. Hermans, J.L. Derks, L. Moonen, C.H.J. Habraken, J. der Thüsen, L.M. von, Hillen et al. Pulmonary neuroendocrine neoplasms with well differentiated morphology and high proliferative activity: illustrated by a case series and review of the literature. Lung Cancer Amst. Neth. 150, 152–158 (2020). https://doi.org/10.1016/j.lungcan.2020.10.015CrossRef

20.

T. Feola, R. Centello, F. Sesti, G. Puliani, M. Verrico, V. Di Vito et al. Neuroendocrine carcinomas with atypical proliferation index and clinical behavior: a systematic review. Cancers 13(6), 1247 (2021). https://doi.org/10.3390/cancers13061247CrossRefPubMedPubMedCentral

21.

N. Oka, A. Kasajima, B. Konukiewitz, A. Sakurada, Y. Okada, T. Kameya et al. Classification and prognostic stratification of bronchopulmonary neuroendocrine neoplasms. Neuroendocrinology 110(5), 393–403 (2020). https://doi.org/10.1159/000502776CrossRefPubMed

22.

A. Kasajima, B. Konukiewitz, N. Oka, H. Suzuki, A. Sakurada, Y. Okada et al. Clinicopathological profiling of lung carcinoids with a Ki67 Index > 20. Neuroendocrinology 108(2), 109–120 (2019). https://doi.org/10.1159/000495806CrossRefPubMed

23.

M.T. Siddiqui, Pulmonary neuroendocrine neoplasms: a review of clinicopathologic and cytologic features. Diagn. Cytopathol. 38(8), 607–617 (2010). https://doi.org/10.1002/dc.21244CrossRefPubMed

24.

G. Pelosi, A. Fabbri, M. Cossa, A. Sonzogni, B. Valeri, L. Righi et al. What clinicians are asking pathologists when dealing with lung neuroendocrine neoplasms? Semin. Diagn. Pathol. 32(6), 469–479 (2015). https://doi.org/10.1053/j.semdp.2015.10.009CrossRefPubMed

25.

L. Righi, M. Volante, I. Rapa, S. Vatrano, G. Pelosi, M. Papotti, Therapeutic biomarkers in lung neuroendocrine neoplasia. Endocr. Pathol. 25(4), 371–377 (2014). https://doi.org/10.1007/s12022-014-9335-6CrossRefPubMed

26.

A.E. Hendifar, A.M. Marchevsky, R. Tuli, Neuroendocrine tumors of the lung: current challenges and advances in the diagnosis and management of well-differentiated disease. J. Thorac. Oncol. Off. Publ. Int. Assoc. Study Lung Cancer 12(3), 425–436 (2017). https://doi.org/10.1016/j.jtho.2016.11.2222CrossRef

27.

S. Singh, E.K. Bergsland, C.M. Card, T.A. Hope, P.L. Kunz, D.T. Laidley et al. 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. J Thorac Oncol Off Publ Int Assoc Study. Lung Cancer 15(10), 1577–1598 (2020). https://doi.org/10.1016/j.jtho.2020.06.021CrossRef

28.

E. Baudin, A.R. Hayes, J.-Y. Scoazec, P.L. Filosso, E. Lim, G. Kaltsas et al. Unmet medical needs in pulmonary neuroendocrine (carcinoid) neoplasms. Neuroendocrinology. 108(1), 7–17 (2019). https://doi.org/10.1159/000493980CrossRefPubMed

29.

S.B. Edge, C.C. Compton, The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann. Surg. Oncol. 17(6), 1471–1474 (2010). https://doi.org/10.1245/s10434-010-0985-4CrossRefPubMed

30.

M. Piñeros, D.M. Parkin, K. Ward, E. Chokunonga, M. Ervik, H. Farrugia et al. Essential TNM: a registry tool to reduce gaps in cancer staging information. Lancet Oncol. 20(2), e103–e111 (2019). https://doi.org/10.1016/S1470-2045(18)30897-0CrossRefPubMed

31.

R. Rami-Porta, H. Asamura, W.D. Travis, V.W. Rusch, Lung cancer - major changes in the American Joint Committee on Cancer eighth edition cancer staging manual. CA Cancer J. Clin. 67(2), 138–155 (2017). https://doi.org/10.3322/caac.21390CrossRefPubMed

32.

G.N. Hortobagyi, S.B. Edge, A. Giuliano, New and important changes in the TNM staging system for breast cancer. Am. Soc. Clin. Oncol. Educ. Book Am. Soc. Clin. Oncol. Annu. Meet. 38, 457–467 (2018). https://doi.org/10.1200/EDBK_201313CrossRef

33.

A. Dasari, C. Shen, D. Halperin, B. Zhao, S. Zhou, Y. Xu et al. Trends in the incidence, prevalence, and survival outcomes in patients with neuroendocrine tumors in the United States. JAMA Oncol. 3(10), 1335 (2017). https://doi.org/10.1001/jamaoncol.2017.0589CrossRefPubMedPubMedCentral

34.

A. Dasari, K. Mehta, L.A. Byers, H. Sorbye, J.C. Yao, Comparative study of lung and extrapulmonary poorly differentiated neuroendocrine carcinomas: a SEER database analysis of 162,983 cases. Cancer 124(4), 807–815 (2018). https://doi.org/10.1002/cncr.31124CrossRefPubMed

35.

J.Y. Yoon, K. Sigel, J. Martin, R. Jordan, M.B. Beasley, C. Smith et al. Evaluation of the prognostic significance of tnm staging guidelines in lung carcinoid tumors. J. Thorac. Oncol. Off. Publ. Int. Assoc. Study Lung Cancer 14(2), 184–192 (2019). https://doi.org/10.1016/j.jtho.2018.10.166CrossRef

36.

J.K. Dermawan, C.F. Farver, The prognostic significance of the 8th edition TNM staging of pulmonary carcinoid tumors: a single institution study with long-term follow-up. Am. J. Surg. Pathol. 43(9), 1291–1296 (2019). https://doi.org/10.1097/PAS.0000000000001268CrossRefPubMed

37.

C.F. Thomas, H.D. Tazelaar, J.R. Jett, Typical and atypical pulmonary carcinoids: outcome in patients presenting with regional lymph node involvement. Chest 119(4), 1143–1150 (2001). https://doi.org/10.1378/chest.119.4.1143CrossRefPubMed

38.

H. Asamura, T. Kameya, Y. Matsuno, M. Noguchi, H. Tada, Y. Ishikawa et al. Neuroendocrine neoplasms of the lung: a prognostic spectrum. J. Clin. Oncol. 24(1), 70–76 (2006). https://doi.org/10.1200/JCO.2005.04.1202CrossRefPubMed

39.

G. Fink, T. Krelbaum, A. Yellin, D. Bendayan, M. Saute, M. Glazer et al. Pulmonary carcinoid: presentation, diagnosis, and outcome in 142 cases in Israel and review of 640 cases from the literature. Chest 119(6), 1647–1651 (2001). https://doi.org/10.1378/chest.119.6.1647CrossRefPubMed

40.

W.D. Travis, W. Rush, D.B. Flieder, R. Falk, M.V. Fleming, A.A. Gal et al. Survival analysis of 200 pulmonary neuroendocrine tumors with clarification of criteria for atypical carcinoid and its separation from typical carcinoid. Am. J. Surg. Pathol. 22(8), 934–944 (1998). https://doi.org/10.1097/00000478-199808000-00003CrossRefPubMed

41.

F. Davini, A. Gonfiotti, C. Comin, A. Caldarella, F. Mannini, A. Janni, Typical and atypical carcinoid tumours: 20-year experience with 89 patients. J. Cardiovasc. Surg. (Torino) 50(6), 807–811 (2009).

42.

F. Marciello, O. Mercier, P. Ferolla, J.-Y. Scoazec, P.L. Filosso, A. Chapelier et al. Natural history of localized and locally advanced atypical lung carcinoids after complete resection: a joined French-Italian Retrospective Multicenter Study. Neuroendocrinology 106(3), 264–273 (2018). https://doi.org/10.1159/000480015CrossRefPubMed

43.

J.C. Yao, M. Hassan, A. Phan, C. Dagohoy, C. Leary, J.E. Mares 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. 26(18), 3063–3072 (2008). https://doi.org/10.1200/JCO.2007.15.4377CrossRefPubMed

44.

C. Kesrouani, C. Ghorra, M. Rassy, H.R. Kourie, J. Kattan, Distribution and characteristics of pulmonary neuroendocrine tumors: single institution experience in Lebanon. Asian Pac. J. Cancer Prev. APJCP 17(5), 2579–2581 (2016)PubMed

45.

N. Pendleton, M.F. Jefferson, G.R. Dixon, M.W. Myskow, M.A. Horan, Correlates of tumor size, sex, cell type, and metastasis of resected non-small cell lung cancer and age. J. Gerontol. A Biol. Sci. Med. Sci. 51(1), B50–B53 (1996). https://doi.org/10.1093/gerona/51a.1.b50CrossRefPubMed

46.

P.L. Filosso, E. Ruffini, S. Di Gangi, F. Guerrera, G. Bora, G. Ciccone et al. Prognostic factors in neuroendocrine tumours of the lung: a single-centre experience. Eur. J. Cardio-Thorac. Surg. Off. J. Eur. Assoc. Cardio-Thorac. Surg. 45(3), 521–526 (2014). https://doi.org/10.1093/ejcts/ezt442CrossRef

47.

M. Chiappetta, I. Sperduti, L.P. Ciavarella, G. Leuzzi, E. Bria, F. Mucilli et al. Prognostic score for survival with pulmonary carcinoids: the importance of associating clinical with pathological characteristics. Interact. Cardiovasc. Thorac. Surg. 31(3), 315–323 (2020). https://doi.org/10.1093/icvts/ivaa114CrossRefPubMed

48.

V.E. Georgakopoulou, E. Zygouris, C. Nikokiris, C. Damaskos, A. Pierrakou, N. Garmpis et al. Predictive indicators of survival in patients with surgically resected lung carcinoid tumors at a Greek Medical Center. Cureus 12(9), e10300 (2020). https://doi.org/10.7759/cureus.10300CrossRefPubMedPubMedCentral

49.

G. Muscogiuri, B. Altieri, M. Albertelli, A. Dotto, R. Modica, L. Barrea et al. Epidemiology of pancreatic neuroendocrine neoplasms: a sex perspective. Endocrine 69(2), 441–450 (2020). https://doi.org/10.1007/s12020-020-02331-3CrossRefPubMed

50.

Z. Yang, W. Wang, J. Lu, G. Pan, Z. Pan, Q. Chen et al. Gastric neuroendocrine tumors (G-Nets): incidence, prognosis and recent trend toward improved survival. Cell Physiol. Biochem. Int. J. Exp. Cell Physiol. Biochem. Pharmacol. 45(1), 389–396 (2018). https://doi.org/10.1159/000486915CrossRef

51.

D. Valvi, X. Mei, M. Gupta, M.B. Shah, A. Ancheta, F. Marti et al. Younger age is associated with improved survival in patients undergoing liver transplantation alone for metastatic neuroendocrine tumors. J. Gastrointest. Surg. Off. J. Soc. Surg. Aliment. Tract 25(6), 1487–1493 (2021). https://doi.org/10.1007/s11605-020-04708-1CrossRef

52.

L. Cao, Z.-W. Li, M. Wang, T.-T. Zhang, B. Bao, Y.-P. Liu, Clinicopathological characteristics, treatment and survival of pulmonary large cell neuroendocrine carcinoma: a SEER population-based study. PeerJ. 7, e6539 (2019)CrossRef

53.

M. Peri, E. Botteri, E. Pisa, F. De Marinis, A. Ungaro, F. Spada et al. A single-institution retrospective analysis of metachronous and synchronous metastatic bronchial neuroendocrine tumors. J. Thorac. Dis. 10(7), 3928–3939 (2018). https://doi.org/10.21037/jtd.2018.06.78CrossRefPubMedPubMedCentral

54.

B.-S. Wu, Y. Hu, J. Sun, J.-L. Wang, P. Wang, W.-W. Dong et al. Analysis on the characteristics and prognosis of pulmonary neuroendocrine tumors. Asian Pac. J. Cancer Prev. APJCP 15(5), 2205–2210 (2014). https://doi.org/10.7314/apjcp.2014.15.5.2205CrossRefPubMed

55.

G. Rindi, D.S. Klimstra, B. Abedi-Ardekani, S.L. Asa, F.T. Bosman, E. Brambilla et al. A common classification framework for neuroendocrine neoplasms: an International Agency for Research on Cancer (IARC) and World Health Organization (WHO) expert consensus proposal. Mod. Pathol. 31(12), 1770–1786 (2018). https://doi.org/10.1038/s41379-018-0110-yCrossRefPubMedPubMedCentral

56.

S. La Rosa, S. Uccella, Classification of neuroendocrine neoplasms: lights and shadows. Rev. Endocr. Metab. Disord. 22(3), 527–538 (2021). https://doi.org/10.1007/s11154-020-09612-2CrossRefPubMed

57.

O. Sazonova, V. Manem, M. Orain, B. Khoshkrood-Mansoori, N. Gaudreault, P. Desmeules et al. Transcriptomic data helps refining classification of pulmonary carcinoid tumors with increased mitotic counts. Mod. Pathol. 33(9), 1712–1721 (2020). https://doi.org/10.1038/s41379-020-0538-8CrossRefPubMed

58.

M. Rubino, J.Y. Scoazec, E. Pisa, M. Faron, L. Spaggiari, J. Hadoux et al. Lung carcinoids with high proliferative activity: further support for the identification of a new tumor category in the classification of lung neuroendocrine neoplasms. Lung Cancer Amst. Neth. 148, 149–158 (2020). https://doi.org/10.1016/j.lungcan.2020.08.001CrossRef

59.

S.Y. Yang, M.S. Cho, N.K. Kim, Difference between right-sided and left-sided colorectal cancers: from embryology to molecular subtype. Expert Rev. Anticancer. Ther. 18(4), 351–358 (2018). https://doi.org/10.1080/14737140.2018.1442217CrossRefPubMed

60.

S. Guo, K. Yao, X. He, S. Wu, Y. Ye, J. Chen, C.L. Wu, Prognostic significance of laterality in renal cell carcinoma: A population-based study from the surveillance, epidemiology, and end results (SEER) database. Cancer Med. 8(12), 5629–5637 (2019). https://doi.org/10.1002/cam4.2484CrossRefPubMedPubMedCentral

61.

B.I. Gustafsson, M. Kidd, A. Chan, M.V. Malfertheiner, I.M. Modlin, Bronchopulmonary neuroendocrine tumors. Cancer 113(1), 5–21 (2008). https://doi.org/10.1002/cncr.23542CrossRefPubMed

62.

C.J. Yang, S.A. Shah, B.K. Lin, K.W. VanDusen, D.Y. Chan, W.D. Tan, D.N. Ranney, T.A. Cox ML,D’Amico, M.F. Berry, Right-sided versus left-sided pneumonectomy after induction therapy for non-small cell lung cancer. Ann. Thorac. Surg. 107(4), 1074–1081 (2019). https://doi.org/10.1016/j.athoracsur.2018.10.009CrossRefPubMed

Title: Prognostic significance of laterality in lung neuroendocrine tumors
Authors: Anna La Salvia
Irene Persano
Alessandra Siciliani
Monica Verrico
Massimiliano Bassi
Roberta Modica
Alessandro Audisio
Isabella Zanata
Beatrice Trabalza Marinucci
Elena Trevisi
Giulia Puliani
Maria Rinzivillo
Elena Parlagreco
Roberto Baldelli
Tiziana Feola
Franz Sesti
Paola Razzore
Rossella Mazzilli
Massimiliano Mancini
Francesco Panzuto
Marco Volante
Elisa Giannetta
Carmen Romero
Marialuisa Appetecchia
Andrea Isidori
Federico Venuta
Maria Rosaria Ambrosio
Maria Chiara Zatelli
Mohsen Ibrahim
Annamaria Colao
Maria Pia Brizzi
Rocío García-Carbonero
Antongiulio Faggiano
Publication date: 18-03-2022
Publisher: Springer US
Keywords: Carcinoid Tumor
Neuroendocrine Tumor
Published in: Endocrine / Issue 3/2022
Print ISSN: 1355-008X
Electronic ISSN: 1559-0100
DOI: https://doi.org/10.1007/s12020-022-03015-w

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Prognostic significance of laterality in lung neuroendocrine tumors

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