Emerging role of nivolumab in the management of patients with non-small-cell lung cancer: current data and future perspectives

References

• LeighlNBTreatment paradigms for patients with metastatic non-small-cell lung cancer: first-, second-, and third-lineCurr Oncol201219Suppl 1S52S5822787411
   PubMed Web of Science ®Google Scholar
• HannaNShepherdFAFossellaFVRandomized phase III trial of pemetrexed versus docetaxel in patients with non-small-cell lung cancer previously treated with chemotherapyJ Clin Oncol20042291589159715117980
   PubMed Web of Science ®Google Scholar
• ShepherdFAPereiraJRCiuleanuTErlotinib in previously treated non-small-cell lung cancerN Engl J Med2005353212313216014882
   PubMed Web of Science ®Google Scholar
• SchillerJHHarringtonDBelaniCPComparison of four chemotherapy regimens for advanced non-small-cell lung cancerN Engl J Med20023462929811784875
   PubMed Web of Science ®Google Scholar
• ScagliottiGVParikhPvon PawelJPhase III study comparing cisplatin plus gemcitabine with cisplatin plus pemetrexed in chemotherapy-naive patients with advanced-stage non-small-cell lung cancerJ Clin Oncol200826213543355118506025
   PubMed Web of Science ®Google Scholar
• DelbaldoCMichielsSSyzNSoriaJCLe ChevalierTPignonJPBenefits of adding a drug to a single-agent or a 2-agent chemotherapy regimen in advanced non-small-cell lung cancer: a meta-analysisJAMA2004292447048415280345
   PubMed Web of Science ®Google Scholar
• Opdivo (nivolumab) injection for intravenous use [prescribing information]New YorkBristol-Myers Squibb2015
   Google Scholar
• European Medicines AgencyOpdivo (nivolumab) [EU summary of product characteristics]2016 Available from: http://www.ema.europa.eu/docs/en_GB/document_library/EPAR_-_Product_Information/human/003985/WC500189765.pdfAccessed May 29, 2016
   Google Scholar
• RibasATumor immunotherapy directed at PD-1N Engl J Med2012366262517251922658126
   PubMed Web of Science ®Google Scholar
• TopalianSLDrakeCGPardollDMTargeting the PD-1/B7-H1 (PD-L1) pathway to activate anti-tumor immunityCurr Opin Immunol201224220721222236695
   PubMed Web of Science ®Google Scholar
• KonishiJYamazakiKAzumaMKinoshitaIDosaka-AkitaHNishimuraMB7-H1 expression on non-small cell lung cancer cells and its relationship with tumor-infiltrating lymphocytes and their PD-1 expressionClin Cancer Res200410155094510015297412
   PubMed Web of Science ®Google Scholar
• ChenYBMuCYHuangJAClinical significance of programmed death-1 ligand-1 expression in patients with non-small cell lung cancer: a 5-year-follow-up studyTumori201298675175523389362
   PubMed Web of Science ®Google Scholar
• BolandJMKwonEDHarringtonSMTumor B7-H1 and B7-H3 expression in squamous cell carcinoma of the lungClin Lung Cancer201314215716322868219
   PubMed Web of Science ®Google Scholar
• YangCYLinMWChangYLWuCTYangPCProgrammed cell death-ligand 1 expression in surgically resected stage I pulmonary adenocarcinoma and its correlation with driver mutations and clinical outcomesEur J Cancer20145071361136924548766
   PubMed Web of Science ®Google Scholar
• ZhangYWangLLiYProtein expression of programmed death 1 ligand 1 and ligand 2 independently predict poor prognosis in surgically resected lung adenocarcinomaOnco Targets Ther2014756757324748806
   PubMed Web of Science ®Google Scholar
• AzumaKOtaKKawaharaAAssociation of PD-L1 overexpression with activating EGFR mutations in surgically resected nonsmall-cell lung cancerAnn Oncol201425101935194025009014
   PubMed Web of Science ®Google Scholar
• VelchetiVSchalperKACarvajalDEProgrammed death ligand-1 expression in non-small cell lung cancerLab Invest201494110711624217091
   PubMed Web of Science ®Google Scholar
• RozaliENHatoSVRobinsonBWLakeRALesterhuisWJProgrammed death ligand 2 in cancer-induced immune suppressionClin Dev Immunol2012201265634022611421
   PubMedGoogle Scholar
• FreemanGJLongAJIwaiYEngagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activationJ Exp Med200019271027103411015443
   PubMed Web of Science ®Google Scholar
• ZouWChenLInhibitory B7-family molecules in the tumour microenvironmentNat Rev Immunol20088646747718500231
   PubMed Web of Science ®Google Scholar
• DongHStromeSESalomaoDRTumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasionNat Med20028879380012091876
   PubMed Web of Science ®Google Scholar
• BrahmerJRPardollDMImmune checkpoint inhibitors: making immunotherapy a reality for the treatment of lung cancerCancer Immunol Res201312859124777499
   PubMed Web of Science ®Google Scholar
• BrahmerJRDrakeCGWollnerIPhase I study of single-agent anti-programmed death-1 (MDX-1106) in refractory solid tumors: safety, clinical activity, pharmacodynamics, and immunologic correlatesJ Clin Oncol201028193167317520516446
   PubMed Web of Science ®Google Scholar
• TopalianSLHodiFSBrahmerJRSafety, activity, and immune correlates of anti-PD-1 antibody in cancerN Engl J Med2012366262443245422658127
   PubMed Web of Science ®Google Scholar
• PasseyCSimonJHongQRoyAAgrawalSAssessment of drug interaction potential by nivolumab using cytokine modulation dataClin Pharm Ther201597Suppl 1S96
   Google Scholar
• GettingerSNHornLGandhiLOverall survival and long-term safety of nivolumab (anti-programmed death 1 antibody, BMS-936558, ONO-4538) in patients with previously treated advanced non-small-cell lung cancerJ Clin Oncol201533182004201225897158
   PubMed Web of Science ®Google Scholar
• HornLRizviNMazieresDLonger-term follow-up of a phase 2 study (CheckMate 063) of nivolumab in patients with advanced, refractory squamous non-small cell lung cancerJ Thorac Oncol201510Suppl 2S175
   Google Scholar
• RizviNAMazièresJPlanchardDActivity and safety of nivolumab, an anti-PD-1 immune checkpoint inhibitor, for patients with advanced, refractory squamous non-small-cell lung cancer (Check-Mate 063): a phase 2, single-arm trialLancet Oncol201516325726525704439
   PubMed Web of Science ®Google Scholar
• ReckampKSpigelDRizviNPhase 3 randomized trial (CheckMate 017) of nivolumab vs docetaxel in advanced squamous cell non-small cell lung cancerPoster presented at: 16th World Conference on Lung CancerSeptember 6–9, 2015Denver, CO
   Google Scholar
• BrahmerJReckampKLBaasPNivolumab versus docetaxel in advanced squamous-cell non–small-cell lung cancerN Engl J Med2015373212313526028407
   PubMed Web of Science ®Google Scholar
• BorghaeiHBrahmerJRHornLNivolumab vs docetaxel in patients with advanced NSCLC: CheckMate 017/057 2-y update and exploratory cytokine profile analysesJ Clin Oncol201634Suppl9025
   Google Scholar
• BorghaeiHPaz-AresLHornLNivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancerN Engl J Med2015373171627163926412456
   PubMed Web of Science ®Google Scholar
• SchmidtLHKümmelAGörlichDPD-1 and PD-L1 expression in NSCLC indicate a favorable prognosis in defined subgroupsPLoS One2015108e013602326313362
   PubMed Web of Science ®Google Scholar
• TaubeJMKleinABrahmerJRAssociation of PD-1, PD-1 ligands, and other features of the tumor immune microenvironment with response to anti-PD-1 therapyClin Cancer Res201420195064507424714771
   PubMed Web of Science ®Google Scholar
• GettingerSHellmanMShepherdFFirst-line monotherapy with nivolumab (NIVO; anti-programmed death-1 [PD-1]) in advanced non-small cell lung cancer (NSCLC): safety, efficacy and correlation of outcomes with PD-1 ligand (PD-L1) expressionJ Clin Oncol201533Suppl8025
   Google Scholar
• HellmannMDGettingerSNGoldmanJWCheckMate 012: safety and efficacy of first-line nivolumab and ipilimumab in advanced NSCLCJ Clin Oncol201634Suppl3001
   Google Scholar
• SocinskiMCreelanBHornLNSCLC, metastatic CheckMate 026: a phase 3 trial of nivolumab vs investigator’s choice (IC) of platinum-based doublet chemotherapy (PT-DC) as first-line therapy for stage iv/recurrent programmed death ligand 1 (PD-L1)-positive NSCLCAnn Oncol201627Suppl 6LBA7
   Google Scholar
• PostowMAChesneyJPavlickACNivolumab and ipilimumab versus ipilimumab in untreated melanomaN Engl J Med2015372212006201725891304
   PubMed Web of Science ®Google Scholar
• RizviNGettingerSGoldmanJSafety and efficacy of first-line nivolumab and ipilimumab in non-small cell lung cancerJ Thoracic Oncol2015109 Suppl 2S176
   Web of Science ®Google Scholar
• GettingerSChowLQBorghaeiHSafety and response with nivolumab (anti-PD-1; BMS-936558, ONO-4538) plus erlotinib in patients (Pts) with epidermal growth factor receptor mutant (EGFR MT) advanced non-small cell lung cancer (NSCLC)Int J Radiat Oncol Biol Phys2014905S34S35
   Google Scholar
• KroemerGGalluzziLKeppOZitvogelLImmunogenic cell death in cancer therapyAnnu Rev Immunol201331517223157435
   PubMed Web of Science ®Google Scholar
• LiuWMFowlerDWSmithPDalgleishAGPre-treatment with chemotherapy can enhance the antigenicity and immunogenicity of tumours by promoting adaptive immune responsesBr J Cancer2010102111512319997099
   PubMed Web of Science ®Google Scholar
• GhiringhelliFMenardCPuigPEMetronomic cyclophosph-amide regimen selectively depletes CD4+CD25+ regulatory T cells and restores T and NK effector functions in end stage cancer patientsCancer Immunol Immunother200756564164816960692
   PubMed Web of Science ®Google Scholar
• ZhangLDermawanKJinMDifferential impairment of regulatory T cells rather than effector T cells by paclitaxel-based chemotherapyClin Immunol2008129221922918771959
   PubMed Web of Science ®Google Scholar
• AntoniaSJBrahmerJRGettingerSNivolumab (anti-PD-1; BMS-936558, ONO-4538) in combination with platinum-based doublet chemotherapy (PT-DC) in advanced non-small cell lung cancer (NSCLC)Int J Radiat Oncol Biol Phys2014905S2
   Web of Science ®Google Scholar
• LangerCJEmerging immunotherapies in the treatment of non-small cell lung cancer (NSCLC): the role of immune checkpoint inhibitorsAm J Clin Oncol201538442243024685885
   PubMed Web of Science ®Google Scholar
• WeberJSYangJCAtkinsMBDisisMLToxicities of immunotherapy for the practitionerJ Clin Oncol201533182092209925918278
   PubMed Web of Science ®Google Scholar
• AntoniaSBendellJTaylorMPhase I/II study of nivolumab with or without ipilimumab for treatment of recurrent small cell lung cancer (SCLC): CA209-032J Clin Oncol201533Suppl7503
   Google Scholar
• Martin-LiberalJFurnessAJJoshiKPeggsKSQuezadaSALarkinJAnti-programmed cell death-1 therapy and insulin-dependent diabetes: a case reportCancer Immunol Immunother201564676576725828465
   PubMed Web of Science ®Google Scholar
• HughesJVudattuNSznolMPrecipitation of autoimmune diabetes with anti-PD-1 immunotherapyDiabetes Care2015384e55e5725805871
   PubMed Web of Science ®Google Scholar
• OkamotoMGotohKMasakiTFulminant type 1 diabetes mellitus with anti-programmed cell death-1 therapyJ Diabetes Investig201676915918
   PubMed Web of Science ®Google Scholar
• WeberJSKudchadkarRRYuBSafety, efficacy, and biomarkers of nivolumab with vaccine in ipilimumab-refractory or -naive melanomaJ Clin Oncol201331344311431824145345
   PubMed Web of Science ®Google Scholar
• HusseinMMcCleodMChandlerJSafety and efficacy of nivolumab in an ongoing trial of a PD-L1 patient population with metastatic non-small cell lung cancerJ Thorac Oncol2015109 Suppl 2S175
   Web of Science ®Google Scholar
• BrahmerJRTykodiSSChowLQSafety and activity of anti-PD-L1 antibody in patients with advanced cancerN Engl J Med2012366262455246522658128
   PubMed Web of Science ®Google Scholar
• ScarpaceSLMetastatic squamous cell non-small-cell lung cancer (NSCLC): disrupting the drug treatment paradigm with immunotherapiesDrugs Context2015421228926576187
   PubMedGoogle Scholar
• WeberJSKahlerKCHauschildAManagement of immune-related adverse events and kinetics of response with ipilimumabJ Clin Oncol201230212691269722614989
   PubMed Web of Science ®Google Scholar
• PostowMACallahanMKWolchokJDImmune checkpoint blockade in cancer therapyJ Clin Oncol201533171974198225605845
   PubMed Web of Science ®Google Scholar
• ChowLQExploring novel immune-related toxicities and endpoints with immune-checkpoint inhibitors in non-small cell lung cancerAm Soc Clin Oncol Educ Book201333e280
   Google Scholar
• HodiFSO’DaySJMcDermottDFImproved survival with ipilimumab in patients with metastatic melanomaN Engl J Med2010363871172320525992
   PubMed Web of Science ®Google Scholar
• HamidORobertCDaudASafety and tumor responses with lambrolizumab (anti-PD-1) in melanomaN Engl J Med2013369213414423724846
   PubMed Web of Science ®Google Scholar
• National Comprehensive Cancer NetworkNCCN clinical practice guidelines in oncology (NCCN guidelines): non-small cell lung cancer (version 4. 2016)2016 Available from: http://www.vitromolecularlaboratories.com/wp-content/uploads/2016/07/NCCN-Clinical-Practice-Guidelines-in-Oncology-NCCN-Guidelines%C2%AE.pdfAccessed March 29, 2017
   Google Scholar
• GaronEBRizviNAHuiRPembrolizumab for the treatment of non-small-cell lung cancerN Engl J Med2015372212018202825891174
   PubMed Web of Science ®Google Scholar
• SoriaJCruzCBahledaRClinical activity, safety and biomarkers of PD-L1 blockade in non-small cell lung cancer (NSCLC): additional analyses from a clinical study of the engineered antibody MPDL3280A (anti-PDL1)Eur J Cancer201349Suppl3408
   Google Scholar
• RizviNBrahmerJOuSHSafety and clinical activity of MEDI4736, an anti-programmed cell death-ligand (PD-L1) antibody, in patients with non-small cell lung cancer (NSCLC)J Clin Oncol201533Suppl8032
   Google Scholar
• SpigelDChaftJGettingerSClinical activity and safety from a phase II study (FIR) of MPDL3280A (anti-PD-L1) in PD-L1-selected patients with non-small cell lung cancer (NSCLC)J Clin Oncol201533Suppl8028
   Google Scholar
• BesseBJohnsonMJannePPhase II, single-arm trial (BIRCH) of atezolizumab as first-line or subsequent therapy for locally advanced or metastatic PD-L1-selected non-small cell lung cancer (NSCLC)Eur J Cancer201551Suppl 3S717S718
   Google Scholar
• PassigliaFBronteGBazanVPD-L1 expression as predictive biomarker in patients with NSCLC: a pooled analysisOncotarget2016715197381974726918451
   PubMedGoogle Scholar
• IlieMLong-MiraEBenceCComparative study of the PD-L1 status between surgically resected specimens and matched biopsies of NSCLC patients reveal major discordances: a potential issue for anti-PD-L1 therapeutic strategiesAnn Oncol201627114715326483045
   PubMed Web of Science ®Google Scholar
• McLaughlinJHanGSchalperKAQuantitative assessment of the heterogeneity of PD-L1 expression in non-small-cell lung cancerJAMA Oncol201621465426562159
   PubMed Web of Science ®Google Scholar
• MansfieldASAubryMCMoserJCTemporal and spatial discordance of programmed cell death-ligand 1 expression and lymphocyte tumor infiltration between paired primary lesions and brain metastases in lung cancerAnn Oncol201627101953195827502709
   PubMed Web of Science ®Google Scholar
• IlieMHofmanVDietelMSoriaJCHofmanPAssessment of the PD-L1 status by immunohistochemistry: challenges and perspectives for therapeutic strategies in lung cancer patientsVirchows Arch2016468551152526915032
   PubMed Web of Science ®Google Scholar
• HirschFRMcElhinnyAStanforthDPD-L1 immunohistochemistry assays for lung cancer: results from phase 1 of the Blueprint PD-L1 IHC Assay Comparison ProjectJ Thorac Oncol201712220822227913228
   PubMed Web of Science ®Google Scholar
• RatcliffeMJSharpeAMidhaAAgreement between programmed cell death ligand-1 diagnostic assays across multiple protein expression cut-offs in non-small cell lung cancerClin Cancer Res Epub2017110
   PubMedGoogle Scholar
• KyiCCarvajalRDWolchokJDPostowMAIpilimumab in patients with melanoma and autoimmune diseaseJ Immunother Cancer2014213525349698
   PubMedGoogle Scholar
• PedersenMAndersenRNørgaardPSuccessful treatment with ipilimumab and interleukin-2 in two patients with metastatic melanoma and systemic autoimmune diseaseCancer Immunol Immunother201463121341134625227926
   PubMed Web of Science ®Google Scholar
• NaritaTOisoNTaketomoYSerological aggravation of autoimmune thyroid disease in two cases receiving nivolumabJ Dermatol201643221021426198822
   PubMed Web of Science ®Google Scholar
• GettingsEJHackettCTScottTFSevere relapse in a multiple sclerosis patient associated with ipilimumab treatment of melanomaMult Scler201521567025257614
   PubMed Web of Science ®Google Scholar
• HarveyRDImmunologic and clinical effects of targeting PD-1 in lung cancerClin Pharmacol Ther201496221422324690569
   PubMed Web of Science ®Google Scholar
• HarmankayaKErasimCKoelblingerCContinuous systemic corticosteroids do not affect the ongoing regression of metastatic melanoma for more than two years following ipilimumab therapyMed Oncol20112841140114420593249
   PubMed Web of Science ®Google Scholar
• EisenhauerEATherassePBogaertsJNew response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1)Eur J Cancer200945222824719097774
   PubMed Web of Science ®Google Scholar
• WolchokJDHoosAO’DaySGuidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteriaClin Cancer Res200915237412742019934295
   PubMed Web of Science ®Google Scholar
• HodiFRibasADaudAEvaluation of immune-related response criteria (irRC) in patients with advanced melanoma treated with the anti-PD-1 monoclonal antibody MK-3475J Clin Oncol20042214 Suppl3006
   Google Scholar
• MinorDRChinKKashani-SabetMInfliximab in the treatment of anti-CTLA4 antibody (ipilimumab) induced immune-related colitisCancer Biother Radiopharm200924332132519538054
   PubMed Web of Science ®Google Scholar
• AminAPlimackEInfanteJNivolumab (anti-PD-1; BMS-936558, ONO-4538) in combination with sunitinib or pazopanib in patients (pts) with metastatic renal cell carcinoma (mRCC)J Clin Oncol2014325 Suppl5010
   Google Scholar
• OttPHodiFSBuchbinderEIInhibition of immune checkpoints and vascular endothelial growth factor as combination therapy for metastatic melanoma: an overview of rationale, preclinical evidence, and initial clinical dataFront Oncol2015520226442214
   PubMed Web of Science ®Google Scholar
• HellmanMCreelanBWooKSmoking history and response to nivolumab in patients with advanced NSCLCsAnn Oncol2014254iv429
   Google Scholar
• RizviNAHellmannMDSnyderACancer immunology: mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancerScience2015348623012412825765070
   PubMed Web of Science ®Google Scholar
• WangCThudiumKBHanMIn vitro characterization of the anti-PD-1 antibody nivolumab, BMS-936558, and in vivo toxicology in non-human primatesCancer Immunol Res20142984685624872026
   PubMed Web of Science ®Google Scholar
• FengYBajajGWangXModel-based analysis of nivolumab to support clinical pharmacology profiling in subjects with solid tumorsClin Pharmacol Ther201597Suppl 1S41S42
   Google Scholar
• ScottLJNivolumab: a review in advanced melanomaDrugs201575121413142426220912
   PubMedGoogle Scholar