Efficacy and safety of immune checkpoint inhibitors in patients with advanced non–small cell lung cancer (NSCLC): a systematic literature review

References

• GLOBOCAN. Global cancer observatory. GLOBOCAN; 2018 [accessed 2019 Mar 07]. https://gco.iarc.fr.
   Google Scholar
• Hammerschmidt S, Wirtz H. Lung cancer: current diagnosis and treatment. Dtsch Arztebl Int. 2009;106(49):809–16. quiz 819-820. doi:10.3238/arztebl.2009.0809.
   PubMed Web of Science ®Google Scholar
• Kashima J, Kitadai R, Okuma Y. Molecular and morphological profiling of lung cancer: a foundation for “Next-Generation” pathologists and oncologists. Cancers (Basel). 2019;11(5):599. doi:10.3390/cancers11050599.
   PubMed Web of Science ®Google Scholar
• Goldstraw P, Chansky K, Crowley J, Rami-Porta R, Asamura H, Eberhardt WEE, Nicholson AG, Groome P, Mitchell A, Bolejack V, et al. The IASLC lung cancer staging project: proposals for revision of the tnm stage groupings in the forthcoming (Eighth) edition of the TNM classification for lung cancer. J Thoracic Oncol. 2016;11(1):39–51. doi:10.1016/j.jtho.2015.09.009.
   PubMed Web of Science ®Google Scholar
• Ettinger DS, Aisner DL, Wood DE, Akerley W, Bauman J, Chang JY, Chirieac LR, D’Amico TA, Dilling TJ, Dobelbower M, et al. NCCN guidelines insights: non–small cell lung cancer, Version 5.2018. J Natl Compr Canc Netw. 2018;16(7):807–821. doi:10.6004/jnccn.2018.0062.
   PubMed Web of Science ®Google Scholar
• Russo A, Franchina T, Ricciardi GRR, Smiroldo V, Picciotto M, Zanghì M, Rolfo C, Adamo V. Third generation EGFR TKIs in EGFR-mutated NSCLC: where are we now and where are we going. Crit Rev Oncol Hematol. 2017;117:38–47. doi:10.1016/j.critrevonc.2017.07.003.
   PubMed Web of Science ®Google Scholar
• Vestergaard HH, Christensen MR, Lassen UN. A systematic review of targeted agents for non-small cell lung cancer. Acta Oncol. 2018;57(2):176–186. doi:10.1080/0284186X.2017.1404634.
   PubMed Web of Science ®Google Scholar
• Chin LP, Soo RA, Soong R, Ou SH. Targeting ROS1 with anaplastic lymphoma kinase inhibitors: a promising therapeutic strategy for a newly defined molecular subset of non-small-cell lung cancer. J Thoracic Oncol. 2012;7(11):1625–1630. doi:10.1097/JTO.0b013e31826baf83.
   PubMed Web of Science ®Google Scholar
• Rosas G, Ruiz R, Araujo JM, Pinto JA, Mas L. ALK rearrangements: biology, detection and opportunities of therapy in non-small cell lung cancer. Crit Rev Oncol Hematol. 2019;136:48–55. doi:10.1016/j.critrevonc.2019.02.006.
   PubMed Web of Science ®Google Scholar
• Gkolfinopoulos S, Mountzios G. Beyond EGFR and ALK: targeting rare mutations in advanced non-small cell lung cancer. Ann Transl Med. 2018;6(8):142. doi:10.21037/atm.2018.04.28.
   PubMed Web of Science ®Google Scholar
• Jardim DL, de Melo Gagliato D, Kurzrock R. Lessons from the development of the immune checkpoint inhibitors in oncology. Integr Cancer Ther. 2018;17(4):1012–1015. doi:10.1177/1534735418801524.
   PubMed Web of Science ®Google Scholar
• Weinstock C, Khozin S, Suzman D, Zhang L, Tang S, Wahby S, Goldberg KB, Kim G, Pazdur R. U.S. Food and drug administration approval summary: atezolizumab for metastatic non-small cell lung cancer. Clin Cancer Res. 2017;23(16):4534–4539. doi:10.1158/1078-0432.CCR-17-0540.
   PubMed Web of Science ®Google Scholar
• Mezquita L, Planchard D. Durvalumab for the treatment of non-small cell lung cancer. Expert Rev Respir Med. 2018;12(8):627–639. doi:10.1080/17476348.2018.1494575.
   PubMed Web of Science ®Google Scholar
• Kazandjian D, Suzman DL, Blumenthal G, Mushti S, He K, Libeg M, Keegan P, Pazdur R. FDA approval summary: nivolumab for the treatment of metastatic non-small cell lung cancer with progression on or after platinum-based chemotherapy. Oncologist. 2016;21(5):634–642. doi:10.1634/theoncologist.2015-0507.
   PubMed Web of Science ®Google Scholar
• Pai-Scherf L, Blumenthal GM, Li H, Subramaniam S, Mishra‐Kalyani PS, He K, Zhao H, Yu J, Paciga M, Goldberg KB. FDA approval summary: pembrolizumab for treatment of metastatic non-small cell lung cancer: first-line therapy and beyond. Oncologist. 2017;22(11):1392–1399. doi:10.1634/theoncologist.2017-0078.
   PubMed Web of Science ®Google Scholar
• Chen R, Hou X, Yang L, Zhao D. Comparative efficacy and safety of first-line treatments for advanced non-small cell lung cancer with immune checkpoint inhibitors: A systematic review and meta-analysis. Thorac Cancer. 2019;10(4):607–623. doi:10.1111/1759-7714.12971.
   PubMed Web of Science ®Google Scholar
• Tun AM, Thein KZ, Thein WL, Guevara E. Checkpoint inhibitors plus chemotherapy for first-line treatment of advanced non-small cell lung cancer: a systematic review and meta-analysis of randomized controlled trials. Future Sci OA. 2019;5(9):Fso421. doi:10.2144/fsoa-2019-0081.
   PubMed Web of Science ®Google Scholar
• Ramos-Esquivel A, van der Laat A, Rojas-Vigott R, Juarez M, Corrales-Rodriguez L. Anti-PD-1/anti-PD-L1 immunotherapy versus docetaxel for previously treated advanced non-small cell lung cancer: a systematic review and meta-analysis of randomised clinical trials. ESMO Open. 2017;2(3):e000236. doi:10.1136/esmoopen-2017-000236.
   PubMed Web of Science ®Google Scholar
• Liu J, Zhong Y, Peng S, Zhou X, Gan X. Efficacy and safety of PD1/PDL1 blockades versus docetaxel in patients with pretreated advanced non-small-cell lung cancer: a meta-analysis. Onco Targets Ther. 2018;11:8623–8632. doi:10.2147/OTT.S181413.
   PubMed Web of Science ®Google Scholar
• Hanna NH, Schneider BJ, Temin S, Baker Jr S, Brahmer J, Ellis PM, Gaspar LE, Haddad RY, Hesketh PJ, Jain D, et al. Therapy for Stage IV non-small-cell lung cancer without driver alterations: ASCO and OH (CCO) joint guideline update. J Clin Oncol. 2020;38(14):1608–1632.
   Web of Science ®Google Scholar
• Planchard D, Popat S, Kerr K, Novello S, Smit EF, Faivre-Finn C, Mok TS, Reck M, Van Schil PE, Hellmann MD, et al. Metastatic non-small cell lung cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2019;30(5):863–870. doi:10.1093/annonc/mdy474.
   PubMed Web of Science ®Google Scholar
• Antonia SJ, Villegas A, Daniel D, Vicente D, Murakami S, Hui R, Yokoi T, Chiappori A, Lee KH, de Wit M, et al. Durvalumab after chemoradiotherapy in Stage III non-small-cell lung cancer. N Engl J Med. 2017;377(20):1919–1929. doi:10.1056/NEJMoa1709937.
   PubMed Web of Science ®Google Scholar
• Hellmann MD, Paz-Ares L, Bernabe Caro R, Zurawski B, Kim S-W, Carcereny Costa E, Park K, Alexandru A, Lupinacci L, de la Mora Jimenez E, et al. Nivolumab plus Ipilimumab in advanced non-small-cell lung cancer. N Engl J Med. 2019;381(21):2020–2031. doi:10.1056/NEJMoa1910231.
   PubMed Web of Science ®Google Scholar
• Hellmann MD, Ciuleanu TE, Pluzanski A, Lee JS, Otterson GA, Audigier-Valette C, Minenza E, Linardou H, Burgers S, Salman P, et al. Nivolumab plus ipilimumab in lung cancer with a high tumor mutational burden. N Engl J Med. 2018;378(22):2093–2104. doi:10.1056/NEJMoa1801946.
   PubMed Web of Science ®Google Scholar
• Borghaei H, Langer CJ, Gadgeel S, Papadimitrakopoulou VA, Patnaik A, Powell SF, Gentzler RD, Martins RG, Stevenson JP, Jalal SI, et al. 24-month overall survival from KEYNOTE-021 Cohort G: pemetrexed and carboplatin with or without pembrolizumab as first-line therapy for advanced nonsquamous non-small cell lung cancer. J Thoracic Oncol. 2019;14(1):124–129. doi:10.1016/j.jtho.2018.08.004.
   PubMed Web of Science ®Google Scholar
• Gray JE, Villegas A, Daniel D, Vicente D, Murakami S, Hui R, Kurata T, Chiappori A, Lee KH, Cho BC, et al. Three-Year overall survival with durvalumab after chemoradiotherapy in Stage III NSCLC-update from PACIFIC. J Thoracic Oncol. 2019;15(2):288–293.
   PubMed Web of Science ®Google Scholar
• Reck M, Rodríguez-Abreu D, Robinson AG, Hui R, Csőszi T, Fülöp A, Gottfried M, Peled N, Tafreshi A, Cuffe S, et al. Updated analysis of KEYNOTE-024: pembrolizumab versus platinum-based chemotherapy for advanced non-small-cell lung cancer with PD-L1 tumor proportion score of 50% or greater. J Clin Oncol. 2019;37(7):537–546. doi:10.1200/JCO.18.00149.
   PubMed Web of Science ®Google Scholar
• York Uo. PROSPERO International prospective register of systeatic reviews. University of York; [accessed 2019 Apr 16]. https://www.crd.york.ac.uk/prospero/.
   Google Scholar
• Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097. doi:10.1371/journal.pmed.1000097.
   PubMed Web of Science ®Google Scholar
• Innovation VH. Covidence systematic review software. Veritas Health Innovation; [accessed Feb 06 2019]. www.covidence.org.
   Google Scholar
• Higgins JP, Altman DG, Gotzsche PC, Juni P, Moher D, Oxman AD, Savovic J, Schulz KF, Weeks L, Sterne JAC, et al. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ (Clinical Research Ed). 2011;343:d5928. doi:10.1136/bmj.d5928.
   PubMed Web of Science ®Google Scholar
• Guyatt GH, Oxman AD, Vist GE, Kunz R, Falck-Ytter Y, Alonso-Coello P, Schünemann HJ. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ (Clinical Research Ed). 2008;336(7650):924–926. doi:10.1136/bmj.39489.470347.AD.
   PubMed Web of Science ®Google Scholar
• Schünemann H, Brożek J, Guyatt G, Oxman A GRADE handbook for grading quality of evidence and strength of recommendations. Updated October 2013. The GRADE Working Group Web site. 2013 [accessed 2020 Feb 25]. www.guidelinedevelopment.org/handbook.
   Google Scholar
• DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–188. doi:10.1016/0197-2456(86)90046-2.
   PubMedGoogle Scholar
• Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ (Clinical Research Ed). 2003;327(7414):557–560. doi:10.1136/bmj.327.7414.557.
   PubMed Web of Science ®Google Scholar
• Antonia SJ, Villegas A, Daniel D, Vicente D, Murakami S, Hui R, Kurata T, Chiappori A, Lee KH, de Wit M. Overall survival with durvalumab after chemoradiotherapy in Stage III NSCLC. N Engl J Med. 2018;379(24):2342–2350. doi:10.1056/NEJMoa1809697.
   PubMed Web of Science ®Google Scholar
• Borghaei H, Paz-Ares L, Horn L, Spigel DR, Steins M, Ready NE, Chow LQ, Vokes EE, Felip E, Holgado E, et al. Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer. N Engl J Med. 2015;373(17):1627–1639. doi:10.1056/NEJMoa1507643.
   PubMed Web of Science ®Google Scholar
• Brahmer J, Reckamp KL, Baas P, Crinò L, Eberhardt WEE, Poddubskaya E, Antonia S, Pluzanski A, Vokes EE, Holgado E, et al. Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med. 2015;373(2):123–135. doi:10.1056/NEJMoa1504627.
   PubMed Web of Science ®Google Scholar
• Carbone DP, Reck M, Paz-Ares L, Creelan B, Horn L, Steins M, Felip E, van den Heuvel MM, Ciuleanu T-E, Badin F, et al. First-line nivolumab in Stage IV or recurrent non-small-cell lung cancer. N Engl J Med. 2017;376(25):2415–2426. doi:10.1056/NEJMoa1613493.
   PubMed Web of Science ®Google Scholar
• Fehrenbacher L, Spira A, Ballinger M, Kowanetz M, Vansteenkiste J, Mazieres J, Park K, Smith D, Artal-Cortes A, Lewanski C, et al. Atezolizumab versus docetaxel for patients with previously treated non-small-cell lung cancer (POPLAR): a multicentre, open-label, phase 2 randomised controlled trial. Lancet (London, England). 2016;387(10030):1837–1846. doi:10.1016/S0140-6736(16)00587-0.
   PubMed Web of Science ®Google Scholar
• Fehrenbacher L, von Pawel J, Park K, Rittmeyer A, Gandara DR, Ponce Aix S, Han J-Y, Gadgeel SM, Hida T, Cortinovis DL, et al. Updated efficacy analysis including secondary population results for OAK: a randomized Phase III study of atezolizumab versus docetaxel in patients with previously treated advanced non–small cell lung cancer. J Thoracic Oncol. 2018;13(8):1156–1170. doi:10.1016/j.jtho.2018.04.039.
   PubMed Web of Science ®Google Scholar
• Gandhi L, Rodriguez-Abreu D, Gadgeel S, Esteban E, Felip E, De Angelis F, Domine M, Clingan P, Hochmair MJ, Powell SF, et al. Pembrolizumab plus chemotherapy in metastatic non-small-cell lung cancer. N Engl J Med. 2018;378(22):2078–2092. doi:10.1056/NEJMoa1801005.
   PubMed Web of Science ®Google Scholar
• Herbst RS, Baas P, Kim D-W, Felip E, Pérez-Gracia JL, Han J-Y, Molina J, Kim J-H, Arvis CD, Ahn M-J, et al. Pembrolizumab versus docetaxel for previously treated, PD-L1-positive, advanced non-small-cell lung cancer (KEYNOTE-010): a randomised controlled trial. Lancet (London, England). 2016;387(10027):1540–1550. doi:10.1016/S0140-6736(15)01281-7.
   PubMed Web of Science ®Google Scholar
• Langer CJ, Gadgeel SM, Borghaei H, Papadimitrakopoulou VA, Patnaik A, Powell SF, Gentzler RD, Martins RG, Stevenson JP, Jalal SI, et al. Carboplatin and pemetrexed with or without pembrolizumab for advanced, non-squamous non-small-cell lung cancer: a randomised, phase 2 cohort of the open-label KEYNOTE-021 study. Lancet Oncol. 2016;17(11):1497–1508. doi:10.1016/S1470-2045(16)30498-3.
   PubMed Web of Science ®Google Scholar
• Mok TSK, Wu Y-L, Kudaba I, Kowalski DM, Cho BC, Turna HZ, Castro G, Srimuninnimit V, Laktionov KK, Bondarenko I, et al. Pembrolizumab versus chemotherapy for previously untreated, PD-L1-expressing, locally advanced or metastatic non-small-cell lung cancer (KEYNOTE-042): a randomised, open-label, controlled, phase 3 trial. Lancet (London, England). 2019;393(10183):1819–1830. doi:10.1016/S0140-6736(18)32409-7.
   PubMed Web of Science ®Google Scholar
• Paz-Ares L, Luft A, Vicente D, Tafreshi A, Gümüş M, Mazières J, Hermes B, Çay Şenler F, Csőszi T, Fülöp A, et al. Pembrolizumab plus chemotherapy for squamous non-small-cell lung cancer. N Engl J Med. 2018;379(21):2040–2051. doi:10.1056/NEJMoa1810865.
   PubMed Web of Science ®Google Scholar
• Reck M, Rodriguez-Abreu D, Robinson AG, Hui R, Csőszi T, Fülöp A, Gottfried M, Peled N, Tafreshi A, Cuffe S, et al. Pembrolizumab versus chemotherapy for PD-L1-positive non-small-cell lung cancer. N Engl J Med. 2016;375(19):1823–1833. doi:10.1056/NEJMoa1606774.
   PubMed Web of Science ®Google Scholar
• Rittmeyer A, Barlesi F, Waterkamp D, Park K, Ciardiello F, von Pawel J, Gadgeel SM, Hida T, Kowalski DM, Dols MC, et al. Atezolizumab versus docetaxel in patients with previously treated non-small-cell lung cancer (OAK): a phase 3, open-label, multicentre randomised controlled trial. Lancet (London, England). 2017;389(10066):255–265. doi:10.1016/S0140-6736(16)32517-X.
   PubMed Web of Science ®Google Scholar
• Socinski MA, Jotte RM, Cappuzzo F, Orlandi F, Stroyakovskiy D, Nogami N, Rodríguez-Abreu D, Moro-Sibilot D, Thomas CA, Barlesi F, et al. Atezolizumab for first-line treatment of metastatic nonsquamous NSCLC. N Engl J Med. 2018;378(24):2288–2301. doi:10.1056/NEJMoa1716948.
   PubMed Web of Science ®Google Scholar
• West H, McCleod M, Hussein M, Morabito A, Rittmeyer A, Conter HJ, Kopp H-G, Daniel D, McCune S, Mekhail T, et al. Atezolizumab in combination with carboplatin plus nab-paclitaxel chemotherapy compared with chemotherapy alone as first-line treatment for metastatic non-squamous non-small-cell lung cancer (IMpower130): a multicentre, randomised, open-label, phase 3 trial. Lancet Oncol. 2019;20(7):924–937. doi:10.1016/S1470-2045(19)30167-6.
   PubMed Web of Science ®Google Scholar
• Wu Y-L, Lu S, Cheng Y, Zhou C, Wang J, Mok T, Zhang L, Tu H-Y, Wu L, Feng J, et al. nivolumab versus docetaxel in a predominantly chinese patient population with previously treated advanced NSCLC: checkMate 078 randomized Phase III clinical trial. J Thoracic Oncol. 2019;14(5):867–875. doi:10.1016/j.jtho.2019.01.006.
   PubMed Web of Science ®Google Scholar
• Greillier L, Tomasini P, Barlesi F. The clinical utility of tumor mutational burden in non-small cell lung cancer. Transl Lung Cancer Res. 2018;7(6):639–646. doi:10.21037/tlcr.2018.10.08.
   PubMed Web of Science ®Google Scholar
• Crequit P, Chaimani A, Yavchitz A, Attiche N, Cadranel J, Trinquart L, Ravaud P. Comparative efficacy and safety of second-line treatments for advanced non-small cell lung cancer with wild-type or unknown status for epidermal growth factor receptor: a systematic review and network meta-analysis. BMC Med. 2017;15(1):193. doi:10.1186/s12916-017-0954-x.
   PubMed Web of Science ®Google Scholar
• Barnfield PC, Ellis PM. Second-line treatment of non-small cell lung cancer: new developments for tumours not harbouring targetable oncogenic driver mutations. Drugs. 2016;76(14):1321–1336. doi:10.1007/s40265-016-0628-6.
   PubMed Web of Science ®Google Scholar
• Kim ES. Avelumab: first Global Approval. Drugs. 2017;77(8):929–937. doi:10.1007/s40265-017-0749-6.
   PubMed Web of Science ®Google Scholar
• Motzer RJ, Penkov K, Haanen J, Rini B, Albiges L, Campbell MT, Venugopal B, Kollmannsberger C, Negrier S, Uemura M. Avelumab plus axitinib versus sunitinib for advanced renal-cell carcinoma. N Engl J Med. 2019;380(12):1103–1115. doi:10.1056/NEJMoa1816047.
   PubMed Web of Science ®Google Scholar
• Zarrabi K, Paroya A, Wu S. Emerging therapeutic agents for genitourinary cancers. J Hematol Oncol. 2019;12(1):89. doi:10.1186/s13045-019-0780-z.
   PubMed Web of Science ®Google Scholar
• Barlesi F, Vansteenkiste J, Spigel D, Ishii H, Garassino M, de Marinis F, Özgüroğlu M, Szczesna A, Polychronis A, Uslu R, et al. Avelumab versus docetaxel in patients with platinum-treated advanced non-small-cell lung cancer (JAVELIN Lung 200): an open-label, randomised, phase 3 study. Lancet Oncol. 2018;19(11):1468–1479. doi:10.1016/S1470-2045(18)30673-9.
   PubMed Web of Science ®Google Scholar