Simultaneous pathological findings in biopsy specimens of patients with surgically resected lung carcinoids and their role in survival

Georgakopoulou,Vasiliki Epameinondas; Zygouris,Eleftherios; Papalexis,Petros; Gkoufa,Aikaterini; Damaskos,Christos; Pierrakou,Aikaterini; Mantzouranis,Konstantinos; Chlapoutakis,Serafeim; Aravantinou-Fatorou,Aikaterini; Sklapani,Pagona; Trakas,Nikolaos; Janinis,Jim; Dahabreh,Jubrail; Spandidos,Demetrios A.

doi:10.3892/ol.2022.13433

Simultaneous pathological findings in biopsy specimens of patients with surgically resected lung carcinoids and their role in survival

Authors:
- Vasiliki Epameinondas Georgakopoulou
- Eleftherios Zygouris
- Petros Papalexis
- Aikaterini Gkoufa
- Christos Damaskos
- Aikaterini Pierrakou
- Konstantinos Mantzouranis
- Serafeim Chlapoutakis
- Aikaterini Aravantinou-Fatorou
- Pagona Sklapani
- Nikolaos Trakas
- Jim Janinis
- Jubrail Dahabreh
- Demetrios A. Spandidos
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Affiliations: Department of Pulmonology, Laiko General Hospital, 11527 Athens, Greece, Department Oncology, Athens Medical Group, 15125 Athens, Greece, First Department of Propedeutic Internal Medicine, Laiko General Hospital, Medical School, National and Kapodistrian University of Athens, 11527 Athens, Greece, First Department of Internal Medicine, Laiko General Hospital, 11527 Athens, Greece, Renal Transplantation Unit, Laiko General Hospital, 11527 Athens, Greece, Department of Pathology, Sismanogleio Hospital, 15126 Athens, Greece, First Department of Pulmonology, Sismanogleio Hospital, 15126 Athens, Greece, Department of Thoracic Surgery, Agios Savvas Hospital, 11522 Athens, Greece, First Department of Internal Medicine, Laiko General Hospital, 11527 Athens, Greece, Department of Cytology, Mitera Hospital, 15123 Athens, Greece, Department of Biochemistry, Sismanogleio Hospital, 15126 Athens, Greece, Laboratory of Clinical Virology, School of Medicine, University of Crete, 71003 Heraklion, Greece
Published online on: July 15, 2022 https://doi.org/10.3892/ol.2022.13433
Article Number: 313
Copyright: © Georgakopoulou et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Pulmonary carcinoid tumors are rare, low‑grade malignant tumors that constitute 1‑2% of all lung tumors. The present study aimed to describe the simultaneous pathological findings in biopsy specimens of patients with surgically resected lung carcinoids and determine their association with survival rates. For this purpose, 108 patients with resected carcinoid lung tumors were followed‑up for 96 months and analyzed for simultaneous pathological findings in biopsy specimens. Among these, simultaneous pathological findings were found in 82 patients. The association between these findings and patient survival rates was evaluated. Atelectasis was a simultaneous finding in 52.4% of the patients, desquamative interstitial pneumonia (DIP) in 13.4%, emphysema in 24.4% and bronchiectasis in 9.8%. The survival rate was 100% for the patients with atelectasis, 81.8% for the patients with DIP, 90% for the patients with emphysema and 75% for the patients with bronchiectasis (P<0.05). According to the univariate analysis, the type of carcinoid was associated with patient survival with better survival rates for patients with typical carcinoids, while age, sex, stage and simultaneous pathological findings were not associated with patient survival. On the whole, there was a statistically significant difference in the survival rates of patients with resected lung carcinoids with different simultaneous pathological findings. However, further studies are warranted to assess the role of these findings in the survival of these patients.

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1	Yang Z, Wang Z, Duan Y and Xu S: Clinicopathological characteristics and prognosis of resected cases of carcinoid tumors of the lung. Thorac Cancer. 7:633–638. 2016. View Article : Google Scholar : PubMed/NCBI
2	Kosmidis PA: Treatment of carcinoid of the lung. Curr Opin Oncol. 16:146–149. 2004. View Article : Google Scholar
3	Fink G, Krelbaum T, Yellin A, Bendayan D, Saute M, Glazer M and Kramer MR: Pulmonary carcinoid: Presentation, diagnosis, and outcome in 142 cases in Israel and review of 640 cases from the literature. Chest. 119:1647–1651. 2001. View Article : Google Scholar
4	Fraser RS, Muller NL, Colman N and Pare PD: Fraser and Pare's diagnosis of diseases of the chest. Neuroendocrine neoplasms. 4th edition. Philadelphia: WB Saunders Co; pp. 1229–1250. 1999
5	Colby TV, Koss M and Travis WD: Atlas of tumor pathology. Tumors of the lower respiratory tract. Armed Forces Institute of Pathology; Washington, DC: 1995
6	Soga J and 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. 5:211–219. 1999.PubMed/NCBI
7	Mark EJ, Quay SC and Dickersin GR: Papillary carcinoid tumor of the lung. Cancer. 48:316–324. 1981. View Article : Google Scholar : PubMed/NCBI
8	Travis WD, Linnoila RI, Tsokos MG, Hitchcock CL, Cutler GB Jr, Nieman L, Chrousos G, Pass H and Doppman J: Neuroendocrine tumors of the lung with proposed criteria for large-cell neuroendocrine carcinoma. An ultrastructural, immunohistochemical, and flow cytometric study of 35 cases. Am J Surg Pathol. 15:529–553. 1991. View Article : Google Scholar
9	Travis WD, Rush W, Flieder DB, Falk R, Fleming MV, Gal AA and Koss MN: Survival analysis of 200 pulmonary neuroendocrine tumors with clarification of criteria for atypical carcinoid and its separation from typical carcinoid. Am J Surg Pathol. 22:934–944. 1998. View Article : Google Scholar
10	Miller RR and Müller NL: Neuroendocrine cell hyperplasia and obliterative bronchiolitis in patients with peripheral carcinoid tumors. Am J Surg Pathol. 19:653–658. 1995. View Article : Google Scholar
11	Wang J, Ren S, Liu Y, Guo K, Chen X, Wang Z and Chen R: Carcinoid tumorlets co-existing with chronic pulmonary inflammatory processes: Imaging findings and histological appearances. Med Sci Monit. 26:e9260142020.
12	Huang Y, Yang X, Lu T, Li M, Zhao M, Yang X, Ma K, Wang S, Zhan C, Liu Y and Wang Q: Assessment of the prognostic factors in patients with pulmonary carcinoid tumor: A population-based study. Cancer Med. 7:2434–2441. 2018. View Article : Google Scholar : PubMed/NCBI
13	Georgakopoulou VE, Zygouris E, Nikokiris C, Damaskos C, Pierrakou A, Garmpis N, Garmpi A, Sklapani P, Aravantinou A, Trakas N, et al: Predictive indicators of survival in patients with surgically resected lung carcinoid tumors at a Greek medical center. Cureus. 12:e103002020.PubMed/NCBI
14	Georgakopoulou VE, Zygouris E, Damaskos C, Pierrakou A, Papalexis P, Garmpis N, Aravantinou-Fatorou A, Chlapoutakis S, Diamantis E, Nikokiris C, et al: Prognostic value of the immunohistochemistry markers CD56, TTF-1, synaptophysin, CEA, EMA and NSE in surgically resected lung carcinoid tumors. Mol Clin Oncol. 16:312022. View Article : Google Scholar
15	Papaxoinis G, Lamarca A, Quinn AM, Mansoor W and Nonaka D: Clinical and pathologic characteristics of pulmonary carcinoid tumors in central and peripheral locations. Endocr Pathol. 29:259–268. 2018. View Article : Google Scholar
16	Beasley MB, Thunnissen FB, Brambilla E, Hasleton P, Steele R, Hammar SP, Colby TV, Sheppard M, Shimosato Y, Koss MN, et al: Pulmonary atypical carcinoid: Predictors of survival in 106 cases. Hum Pathol. 31:1255–1265. 2000. View Article : Google Scholar
17	Halabi S and Owzar K: The importance of identifying and validating prognostic factors in oncology. Semin Oncol. 37:e9–e18. 2010. View Article : Google Scholar
18	Travis WD, Brambilla E, Nicholson AG, Yatabe Y, Austin JHM, Beasley MB, Chirieac LR, Dacic S, Duhig E, Flieder DB, 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. 10:1243–1260. 2015. View Article : Google Scholar
19	Feng SH and Yang ST: The new 8th TNM staging system of lung cancer and its potential imaging interpretation pitfalls and limitations with CT image demonstrations. Diagn Interv Radiol. 25:270–279. 2019. View Article : Google Scholar
20	Woodring JH and Reed JC: Types and mechanisms of pulmonary atelectasis. J Thorac Imaging. 11:92–108. 1996. View Article : Google Scholar : PubMed/NCBI
21	Müller NL, Fraser RS, Colman NC and Paré PD: Radiologic diagnosis of diseases of the chest. WB Saunders; Philadelphia, PA: 2001
22	Tepavac A, Secen N, Sazdanic Velikic D, Popovic G and Perin B: Atelectasis: Positive or negative prognostic factor on outcome of patients with non-small cell lung cancer? J BUON. 15:679–683. 2010.PubMed/NCBI
23	Gu K, Lee HY, Lee K, Choi JY, Woo SY, Sohn I, Kim HK, Choi YS, Kim J, Zo JI and Shim YM: Integrated evaluation of clinical, pathological and radiological prognostic factors in squamous cell carcinoma of the lung. PLoS One. 14:e02232982019. View Article : Google Scholar : PubMed/NCBI
24	Hasbek Z, Yucel B, Salk I, Turgut B, Erselcan T, Babacan NA and Kacan T: Potential impact of atelectasis and primary tumor glycolysis on F-18 FDG PET/CT on survival in lung cancer patients. Asian Pac J Cancer Prev. 15:4085–4089. 2014. View Article : Google Scholar : PubMed/NCBI
25	Bulbul Y, Eris B, Orem A, Gulsoy A, Oztuna F, Ozlu T and Ozsu S: Pulmonary atelectasis and survival in advanced non-small cell lung carcinoma. Ups J Med Sci. 115:176–180. 2010. View Article : Google Scholar
26	Dediu M, Crisan E, Radut M, Tarlea A, Median D, Alexandru A, Vremes G and Gal C: The favorable prognostic significance of atelectasis in patients with advanced non-small cell lung cancer: Results of a prospective observational study. Lung Cancer. 63:271–276. 2009. View Article : Google Scholar : PubMed/NCBI
27	Pang Z, Ding N, Dong W, Ni Y, Zhang T, Qu X, Du J and Liu Q: Prognostic effects of preoperative obstructive pneumonitis or atelectasis and comparison with tumor size in non-small cell lung cancer. J Thorac Dis. 9:768–778. 2017. View Article : Google Scholar : PubMed/NCBI
28	Standards for the diagnosis and care of patients with chronic obstructive pulmonary disease, . American thoracic society. Am J Respir Crit Care Med. 152:S77–S121. 1995.PubMed/NCBI
29	Liu S, Ko S and Chen W: Bronchial carcinoid tumor presenting with complete lobar collapse and unilateral lung emphysema. Clin Imaging. 24:159–161. 2000. View Article : Google Scholar : PubMed/NCBI
30	Sato S, Nakamura M, Shimizu Y, Goto T, Koike T, Ishikawa H and Tsuchida M: The impact of emphysema on surgical outcomes of early-stage lung cancer: A retrospective study. BMC Pulm Med. 19:732019. View Article : Google Scholar : PubMed/NCBI
31	Lee SJ, Yoo JW, Ju S, Cho YJ, Kim JD, Kim SH, Jang IS, Jeong BK, Lee GW, Jeong YY, et al: Quantitative severity of pulmonary emphysema as a prognostic factor for recurrence in patients with surgically resected non-small cell lung cancer. Thorac Cancer. 10:421–427. 2019. View Article : Google Scholar : PubMed/NCBI
32	Gao YH, Guan WJ, Liu Q, Wang HQ, Zhu YN, Chen RC and Zhang GJ: Impact of COPD and emphysema on survival of patients with lung cancer: A meta-analysis of observational studies. Respirology. 21:269–279. 2016. View Article : Google Scholar : PubMed/NCBI
33	Lee HY, Kim EY, Kim YS, Ahn HK and Kim YK: Prognostic significance of CT-determined emphysema in patients with small cell lung cancer. J Thorac Dis. 10:874–881. 2018. View Article : Google Scholar : PubMed/NCBI
34	Georgakopoulou VE, Trakas N, Damaskos C, Garmpis N, Karakou E, Chatzikyriakou R, Lambrou P and Tsiafaki X: Neutrophils to lymphocyte ratio as a biomarker in bronchiectasis exacerbation: A retrospective study. Cureus. 12:e97282020.PubMed/NCBI
35	Meng Z and Linian H: A typical carcinoid tumor of the lung presenting as diffuse cystic bronchiectasis. J Coll Physicians Surg Pak. 30:229–230. 2020. View Article : Google Scholar : PubMed/NCBI
36	Charokopos N, Tsiamita M, Karkoulias K, Koumoundourou D, Aletra C, Dougenis D and Spiropoulos K: Carcinoid tumour behind bronchiectasis. Monaldi Arch Chest Dis. 65:110–113. 2006.PubMed/NCBI
37	Janah H, Jabri H, Bopaka RG, Khattabi WE and Afif H: Localised bronchiectasis revealing carcinoid tumor. Pan Afr Med J. 24:2782016.(In French). View Article : Google Scholar : PubMed/NCBI
38	Ghobadi H, Farzaneh E and Darvishkhah H: Carcinoid tumor with localized bronchiectasis. Tanaffos. 12:56–60. 2013.PubMed/NCBI
39	Liu B, Pu Q, Liu L and Che G: Facial flushing due to multifocal tumorlets in the lung with bronchiectasis. Ann Thorac Surg. 88:641–642. 2009. View Article : Google Scholar : PubMed/NCBI
40	Klinke F, Bosse U and Höfler H: The tumorlet carcinoid in bronchiectasis-changed lungs. An example of a multifocal, endocrine tumor. Pneumologie. 44 (Suppl 1):S607–S609. 1990.(In German).
41	Canessa PA, Santini D, Zanelli M and Capecchi V: Pulmonary tumourlets and microcarcinoids in bronchiectasis. Monaldi Arch Chest Dis. 52:138–139. 1997.PubMed/NCBI
42	Chakraborty RK, Basit H and Sharma S: Desquamative Interstitial Pneumonia. StatPearls Treasure Island (FL): StatPearls Publishing; August 12–2020
43	Bischoff P, Trinks A, Wiederspahn J, Obermayer B, Pett JP, Jurmeister P, Elsner A, Dziodzio T, Rückert JC, Neudecker J, et al: The single-cell transcriptional landscape of lung carcinoid tumors. Int J Cancer. 150:2058–2071. 2022. View Article : Google Scholar : PubMed/NCBI