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Original article

Vol. 153 No. 9 (2023)

Prognostic implication of PD-L1 in early-stage non-small cell lung cancer: a retrospective single-centre study

  • Elona Cekani
  • Carolina Martorell
  • Francesco Martucci
  • Miriam Patella
  • Stefano Cafarotti
  • Antonio Valenti
  • Stefania Freguia
  • Francesca Molinari
  • Patrizia Froesch
  • Milo Frattini
  • Anastasios Stathis
  • Luciano Wannesson
DOI
https://doi.org/10.57187/smw.2023.40110
Cite this as:
Swiss Med Wkly. 2023;153:40110
Published
01.09.2023

Summary

BACKGROUND: The prognostic role of programmed death-ligand 1 (PD-L1) expression in patients with localised and locally advanced non-small cell lung cancer has not been fully elucidated. This information could help to better interpret recent and upcoming results of phase III adjuvant or neoadjuvant anti-PD-1/PD-L1 immunotherapy studies.

METHODS: In a cohort of 146 patients with early or locally advanced non-small cell lung cancer treated with curative intent (by surgery or radiotherapy), we investigated the prognostic value of PD-L1 expression and its correlation with other biological and clinical features. PD-L1 expression was stratified by quartiles. Primary endpoints were overall and disease-free survival. We also analysed the prognostic impact of the presence of actionable mutations, implemented treatment modality and completion of the treatment plan. Neither type of patient received neoadjuvant or adjuvant immunotherapy or target therapy.

RESULTS: Of the 146 selected patients, 32 (21.9%) presented disease progression and 15 died (10.3%) at a median follow-up of 20 months. In a univariable analysis, PD-L1 expression ≥25% was associated with significantly lower disease-free survival (hazard ratio [HR]) 1.9, 95% confidence interval [CI] 1.0–3.9, p = 0.049). PD-L1 expression ≥50% did not lead to disease-free survival or overall survival benefits (HR 1.2 and 1.1, respectively; 95% CI 0.6–2.6 and 0.3–3.4, respectively; pnot significant). In a multivariate analysis, a stage >I (HR 2.7, 95% CI 1.2–6, p = 0.012) and having an inoperable tumour (HR 3.2, 95% CI 1.4–7.4, p = 0.005) were associated with lower disease-free survival.

CONCLUSION: The population of patients with early-stage non-small cell lung cancer and PD-L1 expression ≥25% who were treated with curative intent during the pre-immunotherapy era exhibited a worse prognosis. This finding provides justification for the utilisation of adjuvant immunotherapy in this subgroup of patients, based on the current evidence derived from disease-free survival outcomes. However, for patients with PD-L1 expression <25%, opting to wait for the availability of the overall survival results may be a prudent choice.

References

  1. Califano R, Kerr K, Morgan RD, Lo Russo G, Garassino M, Morgillo F, et al. Immune Checkpoint Blockade: A New Era for Non-Small Cell Lung Cancer. Curr Oncol Rep. 2016 Sep;18(9):59. 10.1007/s11912-016-0544-7 DOI: https://doi.org/10.1007/s11912-016-0544-7
  2. Marrone KA, Brahmer JR. Immune Checkpoint Therapy in Non-Small Cell Lung Cancer. Cancer J. 2016;22(2):81–91. 10.1097/PPO.0000000000000178 DOI: https://doi.org/10.1097/PPO.0000000000000178
  3. Reck M, Rodríguez-Abreu D, Robinson AG, Hui R, Csőszi T, Fülöp A, et al.; KEYNOTE-024 Investigators. Pembrolizumab versus Chemotherapy for PD-L1-Positive Non-Small-Cell Lung Cancer. N Engl J Med. 2016 Nov;375(19):1823–33. 10.1056/NEJMoa1606774 DOI: https://doi.org/10.1056/NEJMoa1606774
  4. Herbst RS, Baas P, Kim DW, Felip E, Pérez-Gracia JL, Han JY, et al. Pembrolizumab versus docetaxel for previously treated, PD-L1-positive, advanced non-small-cell lung cancer (KEYNOTE-010): a randomised controlled trial. Lancet. 2016 Apr;387(10027):1540–50. 10.1016/S0140-6736(15)01281-7 DOI: https://doi.org/10.1016/S0140-6736(15)01281-7
  5. Velcheti V, Schalper KA, Carvajal DE, Anagnostou VK, Syrigos KN, Sznol M, et al. Programmed death ligand-1 expression in non-small cell lung cancer. Lab Invest. 2014;94(1):107-16. Epub 2013/11/13. doi: 10.1038/labinvest.2013.130. PubMed PMID: 24217091; PubMed Central PMCID: PMCPMC6125250. DOI: https://doi.org/10.1038/labinvest.2013.130
  6. Yang CY, Lin MW, Chang YL, Wu CT, Yang PC. Programmed cell death-ligand 1 expression in surgically resected stage I pulmonary adenocarcinoma and its correlation with driver mutations and clinical outcomes. Eur J Cancer. 2014 May;50(7):1361–9. 10.1016/j.ejca.2014.01.018 DOI: https://doi.org/10.1016/j.ejca.2014.01.018
  7. Wu S, Shi X, Sun J, Liu Y, Luo Y, Liang Z, et al. The significance of programmed cell death ligand 1 expression in resected lung adenocarcinoma. Oncotarget. 2017;8(10):16421-9. Epub 2017/02/02. doi: 10.18632/oncotarget.14851. PubMed PMID: 28145884; PubMed Central PMCID: PMCPMC5369973. DOI: https://doi.org/10.18632/oncotarget.14851
  8. Okita R, Maeda A, Shimizu K, Nojima Y, Saisho S, Nakata M. PD-L1 overexpression is partially regulated by EGFR/HER2 signaling and associated with poor prognosis in patients with non-small-cell lung cancer. Cancer Immunol Immunother. 2017 Jul;66(7):865–76. 10.1007/s00262-017-1986-y DOI: https://doi.org/10.1007/s00262-017-1986-y
  9. Takada K, Okamoto T, Toyokawa G, Kozuma Y, Matsubara T, Haratake N, et al. The expression of PD-L1 protein as a prognostic factor in lung squamous cell carcinoma. Lung Cancer. 2017 Feb;104:7–15. 10.1016/j.lungcan.2016.12.006 DOI: https://doi.org/10.1016/j.lungcan.2016.12.006
  10. Guo Q, Sun Y, Yu S, Bai H, Zhao J, Zhuo M, et al. Programmed cell death-ligand 1 (PD-L1) expression and fibroblast growth factor receptor 1 (FGFR1) amplification in stage III/IV lung squamous cell carcinoma (SQC). Thorac Cancer. 2017;8(2):73-9. Epub 2016/12/23. doi: 10.1111/1759-7714.12399. PubMed PMID: 28008744; PubMed Central PMCID: PMCPMC5334288. DOI: https://doi.org/10.1111/1759-7714.12399
  11. Sterlacci W, Fiegl M, Droeser RA, Tzankov A. Expression of PD-L1 Identifies a Subgroup of More Aggressive Non-Small Cell Carcinomas of the Lung. Pathobiology. 2016;83(5):267–75. 10.1159/000444804 DOI: https://doi.org/10.1159/000444804
  12. Ameratunga M, Asadi K, Lin X, Walkiewicz M, Murone C, Knight S, et al. PD-L1 and Tumor Infiltrating Lymphocytes as Prognostic Markers in Resected NSCLC. PLoS One. 2016;11(4):e0153954. Epub 2016/04/23. doi: 10.1371/journal.pone.0153954. PubMed PMID: 27104612; PubMed Central PMCID: PMCPMC4841565. DOI: https://doi.org/10.1371/journal.pone.0153954
  13. Sorensen SF, Zhou W, Dolled-Filhart M, Georgsen JB, Wang Z, Emancipator K, et al. PD-L1 Expression and Survival among Patients with Advanced Non-Small Cell Lung Cancer Treated with Chemotherapy. Transl Oncol. 2016;9(1):64-9. Epub 2016/03/08. doi: 10.1016/j.tranon.2016.01.003. PubMed PMID: 26947883; PubMed Central PMCID: PMCPMC4800057. DOI: https://doi.org/10.1016/j.tranon.2016.01.003
  14. Cooper WA, Tran T, Vilain RE, Madore J, Selinger CI, Kohonen-Corish M, et al. PD-L1 expression is a favorable prognostic factor in early stage non-small cell carcinoma. Lung Cancer. 2015 Aug;89(2):181–8. 10.1016/j.lungcan.2015.05.007 DOI: https://doi.org/10.1016/j.lungcan.2015.05.007
  15. Zhang Y, Wang L, Li Y, Pan Y, Wang R, Hu H, et al. Protein expression of programmed death 1 ligand 1 and ligand 2 independently predict poor prognosis in surgically resected lung adenocarcinoma. Onco Targets Ther. 2014;7:567-73. Epub 2014/04/22. doi: 10.2147/OTT.S59959. PubMed PMID: 24748806; PubMed Central PMCID: PMCPMC3990506. DOI: https://doi.org/10.2147/OTT.S59959
  16. Azuma K, Ota K, Kawahara A, Hattori S, Iwama E, Harada T, et al. Association of PD-L1 overexpression with activating EGFR mutations in surgically resected nonsmall-cell lung cancer. Ann Oncol. 2014 Oct;25(10):1935–40. 10.1093/annonc/mdu242 DOI: https://doi.org/10.1093/annonc/mdu242
  17. Chen YB, Mu CY, Huang JA. Clinical significance of programmed death-1 ligand-1 expression in patients with non-small cell lung cancer: a 5-year-follow-up study. Tumori. 2012 Nov;98(6):751–5. 10.1700/1217.13499 10.1177/030089161209800612 DOI: https://doi.org/10.1177/030089161209800612
  18. Mu CY, Huang JA, Chen Y, Chen C, Zhang XG. High expression of PD-L1 in lung cancer may contribute to poor prognosis and tumor cells immune escape through suppressing tumor infiltrating dendritic cells maturation. Med Oncol. 2011 Sep;28(3):682–8. 10.1007/s12032-010-9515-2 DOI: https://doi.org/10.1007/s12032-010-9515-2
  19. Felip E, Altorki N, Zhou C, Csőszi T, Vynnychenko I, Goloborodko O, et al.; IMpower010 Investigators. Adjuvant atezolizumab after adjuvant chemotherapy in resected stage IB-IIIA non-small-cell lung cancer (IMpower010): a randomised, multicentre, open-label, phase 3 trial. Lancet. 2021 Oct;398(10308):1344–57. 10.1016/S0140-6736(21)02098-5 DOI: https://doi.org/10.1016/S0140-6736(21)02098-5
  20. Forde PM, Spicer J, Lu S, Provencio M, Mitsudomi T, Awad MM, et al.; CheckMate 816 Investigators. Neoadjuvant Nivolumab plus Chemotherapy in Resectable Lung Cancer. N Engl J Med. 2022 May;386(21):1973–85. 10.1056/NEJMoa2202170
  21. D'Arcangelo M, D'Incecco A, Ligorio C, Damiani S, Puccetti M, Bravaccini S, et al. Programmed death ligand 1 expression in early stage, resectable non-small cell lung cancer. Oncotarget. 2019;10(5):561-72. Epub 2019/02/08. doi: 10.18632/oncotarget.26529. PubMed PMID: 30728907; PubMed Central PMCID: PMCPMC6355175. DOI: https://doi.org/10.18632/oncotarget.26529
  22. Ma J, Chi D, Wang Y, Yan Y, Zhao S, Liu H, et al. Prognostic value of PD-L1 expression in resected lung adenocarcinoma and potential molecular mechanisms. J Cancer. 2018;9(19):3489-99. Epub 2018/10/13. doi: 10.7150/jca.26155. PubMed PMID: 30310505; PubMed Central PMCID: PMCPMC6171018. DOI: https://doi.org/10.7150/jca.26155
  23. Chen YY, Wang LB, Zhu HL, Li XY, Zhu YP, Yin YL, et al. Relationship between programmed death-ligand 1 and clinicopathological characteristics in non-small cell lung cancer patients. Chin Med Sci J. 2013 Sep;28(3):147–51. 10.1016/s1001-9294(13)60040-1 10.1016/S1001-9294(13)60040-1 DOI: https://doi.org/10.1016/S1001-9294(13)60040-1
  24. Zhang M, Wang D, Sun Q, Pu H, Wang Y, Zhao S, et al. Prognostic significance of PD-L1 expression and (18)F-FDG PET/CT in surgical pulmonary squamous cell carcinoma. Oncotarget. 2017;8(31):51630-40. Epub 2017/09/09. doi: 10.18632/oncotarget.18257. PubMed PMID: 28881674; PubMed Central PMCID: PMCPMC5584275. DOI: https://doi.org/10.18632/oncotarget.18257
  25. Inamura K, Yokouchi Y, Sakakibara R, Kobayashi M, Subat S, Ninomiya H, et al. Relationship of tumor PD-L1 expression with EGFR wild-type status and poor prognosis in lung adenocarcinoma. Jpn J Clin Oncol. 2016 Oct;46(10):935–41. 10.1093/jjco/hyw087 DOI: https://doi.org/10.1093/jjco/hyw087
  26. Sun JM, Zhou W, Choi YL, Choi SJ, Kim SE, Wang Z, et al. Prognostic Significance of PD-L1 in Patients with Non-Small Cell Lung Cancer: A Large Cohort Study of Surgically Resected Cases. J Thorac Oncol. 2016 Jul;11(7):1003–11. 10.1016/j.jtho.2016.04.007 DOI: https://doi.org/10.1016/j.jtho.2016.04.007
  27. Tang Y, Fang W, Zhang Y, Hong S, Kang S, Yan Y, et al. The association between PD-L1 and EGFR status and the prognostic value of PD-L1 in advanced non-small cell lung cancer patients treated with EGFR-TKIs. Oncotarget. 2015;6(16):14209-19. Epub 2015/04/22. doi: 10.18632/oncotarget.3694. PubMed PMID: 25895031; PubMed Central PMCID: PMCPMC4546461. DOI: https://doi.org/10.18632/oncotarget.3694
  28. Postmus PE, Kerr KM, Oudkerk M, Senan S, Waller DA, Vansteenkiste J, et al.; ESMO Guidelines Committee. Early and locally advanced non-small-cell lung cancer (NSCLC): ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2017 Jul;28 suppl_4:iv1–21. 10.1093/annonc/mdx222 DOI: https://doi.org/10.1093/annonc/mdx222
  29. Ettinger DS, Wood DE, Aisner DL, Akerley W, Bauman JR, Bharat A, et al. NCCN Guidelines Insights: Non-Small Cell Lung Cancer, Version 2.2021. J Natl Compr Canc Netw. 2021 Mar;19(3):254–66. 10.6004/jnccn.2021.0013
  30. von Elm E, Altman DG, Egger M, Pocock SJ, Gotzsche PC, Vandenbroucke JP, et al. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet. 2007;370(9596):1453-7. doi: Doi 10.1016/S0140-6736(07)61602-X. PubMed PMID: WOS:000250386000022. DOI: https://doi.org/10.1016/S0140-6736(07)61602-X
  31. Vansteenkiste J, Crinò L, Dooms C, Douillard JY, Faivre-Finn C, Lim E, et al.; Panel Members. 2nd ESMO Consensus Conference on Lung Cancer: early-stage non-small-cell lung cancer consensus on diagnosis, treatment and follow-up. Ann Oncol. 2014 Aug;25(8):1462–74. 10.1093/annonc/mdu089 DOI: https://doi.org/10.1093/annonc/mdu089
  32. Garon EB, Rizvi NA, Hui R, Leighl N, Balmanoukian AS, Eder JP, et al.; KEYNOTE-001 Investigators. Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl J Med. 2015 May;372(21):2018–28. 10.1056/NEJMoa1501824
  33. Thunnissen E, Bubendorf L, Dietel M, Elmberger G, Kerr K, Lopez-Rios F, et al. EML4-ALK testing in non-small cell carcinomas of the lung: a review with recommendations. Virchows Arch. 2012;461(3):245-57. Epub 2012/07/25. doi: 10.1007/s00428-012-1281-4. PubMed PMID: 22825000; PubMed Central PMCID: PMCPMC3432214. DOI: https://doi.org/10.1007/s00428-012-1281-4
  34. Tsuta K, Kawago M, Yoshida A, Sekine S, Asamura H, Furuta K, et al. Primary lung adenocarcinoma with morule-like components: a unique histologic hallmark of aggressive behavior and EGFR mutation. Lung Cancer. 2014 Jul;85(1):12–8. 10.1016/j.lungcan.2014.03.022 DOI: https://doi.org/10.1016/j.lungcan.2014.03.022
  35. Bubendorf L, Buttner R, Al-Dayel F, Dietel M, Elmberger G, Kerr K, et al. Testing for ROS1 in non-small cell lung cancer: a review with recommendations. Virchows Archiv. 2016;469(5):489-503. doi: 10.1007/s00428-016-2000-3. PubMed PMID: WOS:000387226000002. DOI: https://doi.org/10.1007/s00428-016-2000-3
  36. Fatti e cifre sul cancro 2023 2023. Available from: https://www.cancer.org/research/cancer-facts-statistics/all-cancer-facts-figures/2023-cancer-facts-figures.html
  37. Schemper M, Smith TL. A note on quantifying follow-up in studies of failure time. Control Clin Trials. 1996 Aug;17(4):343–6. 10.1016/0197-2456(96)00075-x 10.1016/0197-2456(96)00075-X DOI: https://doi.org/10.1016/0197-2456(96)00075-X
  38. Zou W, Wolchok JD, Chen L. PD-L1 (B7-H1) and PD-1 pathway blockade for cancer therapy: Mechanisms, response biomarkers, and combinations. Sci Transl Med. 2016;8(328):328rv4. Epub 2016/03/05. doi: 10.1126/scitranslmed.aad7118. PubMed PMID: 26936508; PubMed Central PMCID: PMCPMC4859220. DOI: https://doi.org/10.1126/scitranslmed.aad7118
  39. Gatalica Z, Snyder C, Maney T, Ghazalpour A, Holterman DA, Xiao N, et al. Programmed cell death 1 (PD-1) and its ligand (PD-L1) in common cancers and their correlation with molecular cancer type. Cancer Epidemiol Biomarkers Prev. 2014 Dec;23(12):2965–70. 10.1158/1055-9965.EPI-14-0654 DOI: https://doi.org/10.1158/1055-9965.EPI-14-0654
  40. Patsoukis N, Brown J, Petkova V, Liu F, Li L, Boussiotis VA. Selective effects of PD-1 on Akt and Ras pathways regulate molecular components of the cell cycle and inhibit T cell proliferation. Sci Signal. 2012;5(230):ra46. Epub 2012/06/29. doi: 10.1126/scisignal.2002796. PubMed PMID: 22740686; PubMed Central PMCID: PMCPMC5498435. DOI: https://doi.org/10.1126/scisignal.2002796
  41. Duraiswamy J, Freeman GJ, Coukos G. Therapeutic PD-1 pathway blockade augments with other modalities of immunotherapy T-cell function to prevent immune decline in ovarian cancer. Cancer Res. 2013;73(23):6900-12. Epub 2013/08/27. doi: 10.1158/0008-5472.CAN-13-1550. PubMed PMID: 23975756; PubMed Central PMCID: PMCPMC3851914. DOI: https://doi.org/10.1158/0008-5472.CAN-13-1550
  42. Park HJ, Kusnadi A, Lee EJ, Kim WW, Cho BC, Lee IJ, et al. Tumor-infiltrating regulatory T cells delineated by upregulation of PD-1 and inhibitory receptors. Cell Immunol. 2012;278(1-2):76–83. 10.1016/j.cellimm.2012.07.001 DOI: https://doi.org/10.1016/j.cellimm.2012.07.001
  43. Shimoji M, Shimizu S, Sato K, Suda K, Kobayashi Y, Tomizawa K, et al. Clinical and pathologic features of lung cancer expressing programmed cell death ligand 1 (PD-L1). Lung Cancer. 2016 Aug;98:69–75. 10.1016/j.lungcan.2016.04.021 DOI: https://doi.org/10.1016/j.lungcan.2016.04.021
  44. Topalian SL, Taube JM, Anders RA, Pardoll DM. Mechanism-driven biomarkers to guide immune checkpoint blockade in cancer therapy. Nat Rev Cancer. 2016;16(5):275-87. Epub 2016/04/16. doi: 10.1038/nrc.2016.36. PubMed PMID: 27079802; PubMed Central PMCID: PMCPMC5381938. DOI: https://doi.org/10.1038/nrc.2016.36
  45. Ma W, Gilligan BM, Yuan J, Li T. Current status and perspectives in translational biomarker research for PD-1/PD-L1 immune checkpoint blockade therapy. J Hematol Oncol. 2016;9(1):47. Epub 2016/05/29. doi: 10.1186/s13045-016-0277-y. PubMed PMID: 27234522; PubMed Central PMCID: PMCPMC4884396. DOI: https://doi.org/10.1186/s13045-016-0277-y
  46. Zhang M, Li G, Wang Y, Wang Y, Zhao S, Haihong P, et al. PD-L1 expression in lung cancer and its correlation with driver mutations: a meta-analysis. Sci Rep. 2017;7(1):10255. Epub 2017/09/02. doi: 10.1038/s41598-017-10925-7. PubMed PMID: 28860576; PubMed Central PMCID: PMCPMC5578960. DOI: https://doi.org/10.1038/s41598-017-10925-7
  47. Li H, Xu Y, Wan B, Song Y, Zhan P, Hu Y, et al. The clinicopathological and prognostic significance of PD-L1 expression assessed by immunohistochemistry in lung cancer: a meta-analysis of 50 studies with 11,383 patients. Transl Lung Cancer Res. 2019;8(4):429-49. Epub 2019/09/27. doi: 10.21037/tlcr.2019.08.04. PubMed PMID: 31555517; PubMed Central PMCID: PMCPMC6749117. DOI: https://doi.org/10.21037/tlcr.2019.08.04
  48. Schmidt LH, Kummel A, Gorlich D, Mohr M, Brockling S, Mikesch JH, et al. PD-1 and PD-L1 Expression in NSCLC Indicate a Favorable Prognosis in Defined Subgroups. PLoS One. 2015;10(8):e0136023. Epub 2015/08/28. doi: 10.1371/journal.pone.0136023. PubMed PMID: 26313362; PubMed Central PMCID: PMCPMC4552388. DOI: https://doi.org/10.1371/journal.pone.0136023
  49. Hirsch FR, McElhinny A, Stanforth D, Ranger-Moore J, Jansson M, Kulangara K, et al. PD-L1 Immunohistochemistry Assays for Lung Cancer: Results from Phase 1 of the Blueprint PD-L1 IHC Assay Comparison Project. J Thorac Oncol. 2017 Feb;12(2):208–22. 10.1016/j.jtho.2016.11.2228 DOI: https://doi.org/10.1016/j.jtho.2016.11.2228
  50. Jain P, Gutierrez Bugarin J, Guha A, Jain C, Patil N, Shen T, et al. Cardiovascular adverse events are associated with usage of immune checkpoint inhibitors in real-world clinical data across the United States. ESMO Open. 2021;6(5):100252. Epub 2021/08/31. doi: 10.1016/j.esmoop.2021.100252. PubMed PMID: 34461483; PubMed Central PMCID: PMCPMC8403739. DOI: https://doi.org/10.1016/j.esmoop.2021.100252
  51. Matsuo Y, Chen F, Hamaji M, Kawaguchi A, Ueki N, Nagata Y, et al. Comparison of long-term survival outcomes between stereotactic body radiotherapy and sublobar resection for stage I non-small-cell lung cancer in patients at high risk for lobectomy: A propensity score matching analysis. Eur J Cancer. 2014 Nov;50(17):2932–8. 10.1016/j.ejca.2014.09.006 DOI: https://doi.org/10.1016/j.ejca.2014.09.006
  52. Varlotto J, Fakiris A, Flickinger J, Medford-Davis L, Liss A, Shelkey J, et al. Matched-pair and propensity score comparisons of outcomes of patients with clinical stage I non-small cell lung cancer treated with resection or stereotactic radiosurgery. Cancer. 2013 Aug;119(15):2683–91. 10.1002/cncr.28100 DOI: https://doi.org/10.1002/cncr.28100
  53. Verstegen NE, Oosterhuis JW, Palma DA, Rodrigues G, Lagerwaard FJ, van der Elst A, et al. Stage I-II non-small-cell lung cancer treated using either stereotactic ablative radiotherapy (SABR) or lobectomy by video-assisted thoracoscopic surgery (VATS): outcomes of a propensity score-matched analysis. Ann Oncol. 2013 Jun;24(6):1543–8. 10.1093/annonc/mdt026 DOI: https://doi.org/10.1093/annonc/mdt026
  54. Bryant AK, Mundt RC, Sandhu AP, Urbanic JJ, Sharabi AB, Gupta S, et al. Stereotactic Body Radiation Therapy Versus Surgery for Early Lung Cancer Among US Veterans. Ann Thorac Surg. 2018 Feb;105(2):425–31. 10.1016/j.athoracsur.2017.07.048 DOI: https://doi.org/10.1016/j.athoracsur.2017.07.048
  55. Crabtree TD, Denlinger CE, Meyers BF, El Naqa I, Zoole J, Krupnick AS, et al. Stereotactic body radiation therapy versus surgical resection for stage I non-small cell lung cancer. J Thorac Cardiovasc Surg. 2010 Aug;140(2):377–86. 10.1016/j.jtcvs.2009.12.054 DOI: https://doi.org/10.1016/j.jtcvs.2009.12.054
  56. Grills IS, Mangona VS, Welsh R, Chmielewski G, McInerney E, Martin S, et al. Outcomes after stereotactic lung radiotherapy or wedge resection for stage I non-small-cell lung cancer. J Clin Oncol. 2010 Feb;28(6):928–35. 10.1200/JCO.2009.25.0928 DOI: https://doi.org/10.1200/JCO.2009.25.0928
  57. Shirvani SM, Jiang J, Chang JY, Welsh JW, Gomez DR, Swisher S, et al. Comparative effectiveness of 5 treatment strategies for early-stage non-small cell lung cancer in the elderly. Int J Radiat Oncol Biol Phys. 2012;84(5):1060-70. Epub 2012/09/15. doi: 10.1016/j.ijrobp.2012.07.2354. PubMed PMID: 22975611; PubMed Central PMCID: PMCPMC3776428. DOI: https://doi.org/10.1016/j.ijrobp.2012.07.2354
  58. Yu JB, Soulos PR, Cramer LD, Decker RH, Kim AW, Gross CP. Comparative effectiveness of surgery and radiosurgery for stage I non-small cell lung cancer. Cancer. 2015;121(14):2341-9. Epub 2015/04/08. doi: 10.1002/cncr.29359. PubMed PMID: 25847699; PubMed Central PMCID: PMCPMC4490059. DOI: https://doi.org/10.1002/cncr.29359
  59. Zheng X, Schipper M, Kidwell K, Lin J, Reddy R, Ren Y, et al. Survival outcome after stereotactic body radiation therapy and surgery for stage I non-small cell lung cancer: a meta-analysis. Int J Radiat Oncol Biol Phys. 2014 Nov;90(3):603–11. 10.1016/j.ijrobp.2014.05.055 DOI: https://doi.org/10.1016/j.ijrobp.2014.05.055

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