Clinical efficacy and safety of afatinib in the treatment of non-small-cell lung cancer in Chinese patients

References

• EttingerDSWoodDEAisnerDLNon-small cell lung cancer, version 5.2017, NCCN clinical practice guidelines in oncologyJ Natl Compr Canc Netw201715450453528404761
   PubMed Web of Science ®Google Scholar
• SiegelRLMillerKDJemalACancer statistics, 2017CA Cancer J Clin201767173028055103
   PubMed Web of Science ®Google Scholar
• TravisWDBrambillaENicholsonAGWHO PanelThe 2015 World Health Organization classification of lung tumors: impact of genetic, clinical and radiologic advances since the 2004 classificationJ Thorac Oncol20151091243126026291008
   PubMed Web of Science ®Google Scholar
• ChenWZhengRBaadePDCancer statistics in China, 2015CA Cancer J Clin201666211513226808342
   PubMed Web of Science ®Google Scholar
• DattaDLahiriBPreoperative evaluation of patients undergoing lung resection surgeryChest200312362096210312796194
   PubMed Web of Science ®Google Scholar
• SchillerJHHarringtonDBelaniCPEastern Cooperative Oncology GroupComparison of four chemotherapy regimens for advanced non-small-cell lung cancerN Engl J Med20023462929811784875
   PubMed Web of Science ®Google Scholar
• ThomasALiuSVSubramaniamDSGiacconeGRefining the treatment of NSCLC according to histological and molecular subtypesNat Rev Clin Oncol201512951152625963091
   PubMed Web of Science ®Google Scholar
• AnagnostouVKBrahmerJRCancer immunotherapy: a future paradigm shift in the treatment of non-small cell lung cancerClin Cancer Res201521597698425733707
   PubMed Web of Science ®Google Scholar
• KazandjianDBlumenthalGMYuanWHeKKeeganPPazdurRFDA approval of gefitinib for the treatment of patients with metastatic EGFR mutation-positive non-small cell lung cancerClin Cancer Res20162261307131226980062
   PubMed Web of Science ®Google Scholar
• GeLShiRProgress of EGFR-TKI and ALK/ROS1 inhibitors in advanced non-small cell lung cancerInt J Clin Exp Med201587103301033926379824
   PubMed Web of Science ®Google Scholar
• DaviesRLGrosseVAKucherlapatiRBothwellMGenetic analysis of epidermal growth factor action: assignment of human epidermal growth factor receptor gene to chromosome 7Proc Natl Acad Sci U S A1980777418841926254014
   PubMed Web of Science ®Google Scholar
• KlapperLNGlatheSVaismanNThe ErbB-2/HER2 oncoprotein of human carcinomas may function solely as a shared coreceptor for multiple stroma-derived growth factorsProc Natl Acad Sci U S A19999694995500010220407
   PubMed Web of Science ®Google Scholar
• SandersJMWampoleMEThakurMLWickstromEMolecular determinants of epidermal growth factor binding: a molecular dynamics studyPLoS One201381e5413623382875
   PubMed Web of Science ®Google Scholar
• BowersGReardonDHewittTThe relative role of ErbB1–4 receptor tyrosine kinases in radiation signal transduction responses of human carcinoma cellsOncogene200120111388139711313882
   PubMed Web of Science ®Google Scholar
• GustersonBCowleyGMcIlhinneyJOzanneBFisherCReevesBEvidence for increased epidermal growth factor receptors in human sarcomasInt J Cancer19853666896932999006
   PubMed Web of Science ®Google Scholar
• ChernevaRGeorgievODimovaIRukovaBPetrovDTonchevaDEGFR and hTERT expression as a diagnostic approach for non-small cell lung cancer in high risk groupsBiomark Cancer20102576324179385
   PubMedGoogle Scholar
• RicciardiGRRussoAFranchinaTNSCLC and HER2: between lights and shadowsJ Thorac Oncol20149121750176225247338
   PubMed Web of Science ®Google Scholar
• ShigematsuHTakahashiTNomuraMSomatic mutations of the HER2 kinase domain in lung adenocarcinomasCancer Res20056551642164615753357
   PubMed Web of Science ®Google Scholar
• StephensPHunterCBignellGLung cancer: intragenic ERBB2 kinase mutations in tumoursNature20044317008525526
   PubMed Web of Science ®Google Scholar
• GatelyKFordeLCuffeSHigh coexpression of both EGFR and IGF1R correlates with poor patient prognosis in resected non-small-cell lung cancerClin Lung Cancer2014151586624210543
   PubMed Web of Science ®Google Scholar
• DouillardJYPirkerRO’ByrneKJRelationship between EGFR expression, EGFR mutation status, and the efficacy of chemotherapy plus cetuximab in FLEX study patients with advanced non-small-cell lung cancerJ Thorac Oncol20149571772424662454
   PubMed Web of Science ®Google Scholar
• LuYWangYZhangMHER2-siRNA delivered by EGFR-specific single chain antibody inhibits NSCLC cell proliferation and tumor growthOncotarget2016717235942360726988752
   PubMedGoogle Scholar
• KitanoHChungJYYlayaKProfiling of phospho-AKT, phospho-mTOR, phospho-MAPK and EGFR in non-small cell lung cancerJ Histochem Cytochem201462533534624487999
   PubMed Web of Science ®Google Scholar
• HynesNEMacDonaldGErbB receptors and signaling pathways in cancerCurr Opin Cell Biol200921217718419208461
   PubMed Web of Science ®Google Scholar
• GomezNCohenPDissection of the protein kinase cascade by which nerve growth factor activates MAP kinasesNature199135363401701731716348
   PubMed Web of Science ®Google Scholar
• BreindelJLHaskinsJWCowellEPZhaoMNguyenDXSternDFEGF receptor activates MET through MAPK to enhance non-small cell lung carcinoma invasion and brain metastasisCancer Res201373165053506523794705
   PubMed Web of Science ®Google Scholar
• NishimuraYTakiguchiSItoSItohKEGFstimulated AKT activation is mediated by EGFR recycling via an early endocytic pathway in a gefitinibresistant human lung cancer cell lineInt J Oncol20154641721172925653196
   PubMed Web of Science ®Google Scholar
• FrumanDARommelCPI3K and cancer: lessons, challenges and opportunitiesNat Rev Drug Discov201413214015624481312
   PubMed Web of Science ®Google Scholar
• HensonEChenYGibsonSEGFR family members’ regulation of autophagy is at a crossroads of cell survival and death in cancerCancers (Basel)201794E2728338617
   PubMed Web of Science ®Google Scholar
• JonesRBGordusAKrallJAMacBeathGA quantitative protein interaction network for the ErbB receptors using protein microarraysNature2006439707316817416273093
   PubMed Web of Science ®Google Scholar
• LynchTJBellDWSordellaRActivating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinibN Engl J Med2004350212129213915118073
   PubMed Web of Science ®Google Scholar
• ShepherdFARodrigues PereiraJCiuleanuTNational Cancer Institute of Canada Clinical Trials GroupErlotinib in previously treated non-small-cell lung cancerN Engl J Med2005353212313216014882
   PubMed Web of Science ®Google Scholar
• YunCHMengwasserKETomsAVThe T790M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATPProc Natl Acad Sci U S A200810562070207518227510
   PubMed Web of Science ®Google Scholar
• YoshidaTZhangGSmithMATyrosine phosphoproteomics identifies both codrivers and cotargeting strategies for T790M-related EGFR-TKI resistance in non-small cell lung cancerClin Cancer Res201420154059407424919575
   PubMed Web of Science ®Google Scholar
• SolcaFDahlGZoephelATarget binding properties and cellular activity of afatinib (BIBW 2992), an irreversible ErbB family blockerJ Pharmacol Exp Ther2012343234235022888144
   PubMed Web of Science ®Google Scholar
• HeigenerDFSchumannCSebastianMAfatinib Compassionate Use Consortium (ACUC)Afatinib in non-small cell lung cancer harboring uncommon EGFR mutations pretreated with reversible EGFR inhibitorsOncologist201520101167117426354527
   PubMed Web of Science ®Google Scholar
• SosMLRodeHBHeynckSChemogenomic profiling provides insights into the limited activity of irreversible EGFR Inhibitors in tumor cells expressing the T790M EGFR resistance mutationCancer Res201070386887420103621
   PubMed Web of Science ®Google Scholar
• OxnardGRThressKSAldenRSAssociation between plasma genotyping and outcomes of treatment with osimertinib (AZD9291) in advanced non-small-cell lung cancerJ Clin Oncol201634283375338227354477
   PubMed Web of Science ®Google Scholar
• KimESOlmutinib: first global approvalDrugs201676111153115727357069
   PubMed Web of Science ®Google Scholar
• SequistLVSoriaJCGoldmanJWRociletinib in EGFR-mutated non-small-cell lung cancerN Engl J Med2015372181700170925923550
   PubMed Web of Science ®Google Scholar
• TranPNKlempnerSJProfile of rociletinib and its potential in the treatment of non-small-cell lung cancerLung Cancer (Auckl)20167919728210165
   PubMedGoogle Scholar
• LiDAmbrogioLShimamuraTBIBW2992, an irreversible EGFR/HER2 inhibitor highly effective in preclinical lung cancer modelsOncogene200827344702471118408761
   PubMed Web of Science ®Google Scholar
• WongCHMaBBHuiCWTaoQChanATPreclinical evaluation of afatinib (BIBW2992) in esophageal squamous cell carcinoma (ESCC)Am J Cancer Res20155123588359926885448
   PubMed Web of Science ®Google Scholar
• JanjigianYYSmitEFGroenHJDual inhibition of EGFR with afatinib and cetuximab in kinase inhibitor-resistant EGFR-mutant lung cancer with and without T790M mutationsCancer Discov2014491036104525074459
   PubMed Web of Science ®Google Scholar
• ShigematsuHLinLTakahashiTClinical and biological features associated with epidermal growth factor receptor gene mutations in lung cancersJ Natl Cancer Inst200597533934615741570
   PubMed Web of Science ®Google Scholar
• LeeSYKimMJJinGSomatic mutations in epidermal growth factor receptor signaling pathway genes in non-small cell lung cancersJ Thorac Oncol20105111734174020881644
   PubMed Web of Science ®Google Scholar
• ShigematsuHGazdarAFSomatic mutations of epidermal growth factor receptor signaling pathway in lung cancersInt J Cancer2006118225726216231326
   PubMed Web of Science ®Google Scholar
• GirardNSimaCSJackmanDMNomogram to predict the presence of EGFR activating mutation in lung adenocarcinomaEur Respir J201239236637221778168
   PubMed Web of Science ®Google Scholar
• SharmaSVBellDWSettlemanJHaberDAEpidermal growth factor receptor mutations in lung cancerNat Rev Cancer20077316918117318210
   PubMed Web of Science ®Google Scholar
• LuRLHuCPYangHPLiYYGuQHWuLBiological characteristics and epidermal growth factor receptor tyrosine kinase inhibitors efficacy of EGFR mutation and its subtypes in lung adenocarcinomaPathol Oncol Res201420244545124297623
   PubMed Web of Science ®Google Scholar
• RosellRMoranTQueraltCSpanish Lung Cancer GroupScreening for epidermal growth factor receptor mutations in lung cancerN Engl J Med20093611095896719692684
   PubMed Web of Science ®Google Scholar
• ShiYAuJSThongprasertSA prospective, molecular epidemiology study of EGFR mutations in Asian patients with advanced non-small-cell lung cancer of adenocarcinoma histology (PIONEER)J Thorac Oncol20149215416224419411
   PubMed Web of Science ®Google Scholar
• HongSFangWHuZA large-scale cross-sectional study of ALK rearrangements and EGFR mutations in non-small-cell lung cancer in Chinese Han populationSci Rep20144726825434695
   PubMed Web of Science ®Google Scholar
• XieGXieFWuPThe mutation rates of EGFR in non-small cell lung cancer and KRAS in colorectal cancer of Chinese patients as detected by pyrosequencing using a novel dispensation orderJ Exp Clin Cancer Res2015346326081767
   PubMed Web of Science ®Google Scholar
• LiamCKLeowHRHowSHEpidermal growth factor receptor mutations in non-small cell lung cancers in a multiethnic Malaysian patient populationAsian Pac J Cancer Prev201415132132624528049
   PubMedGoogle Scholar
• TomitaMAyabeTChosaEKawagoeKNakamuraKEpidermal growth factor receptor mutations in Japanese men with lung adenocarcinomasAsian Pac J Cancer Prev20141524106271063025605150
   PubMedGoogle Scholar
• ArrietaOCardonaAFFederico BramugliaGCLICaPGenotyping non-small cell lung cancer (NSCLC) in Latin AmericaJ Thorac Oncol20116111955195922005474
   PubMed Web of Science ®Google Scholar
• ShiauCJBabwahJPda Cunha SantosGSample features associated with success rates in population-based EGFR mutation testingJ Thorac Oncol20149794795624922009
   PubMed Web of Science ®Google Scholar
• ZaricBStojsicVKovacevicTClinical characteristics, tumor, node, metastasis status, and mutation rate in domain of epidermal growth factor receptor gene in Serbian patients with lung adenocarcinomaJ Thorac Oncol2014991406141025122436
   PubMed Web of Science ®Google Scholar
• Maki-NevalaSRontyMMorelMEpidermal growth factor receptor mutations in 510 Finnish non-small-cell lung cancer patientsJ Thorac Oncol20149688689124828666
   PubMed Web of Science ®Google Scholar
• RamlauRCuferTBerzinecPINSIGHT study TeamEpidermal growth factor receptor mutation-positive non-small-cell lung cancer in the real-world setting in central Europe: the INSIGHT studyJ Thorac Oncol20151091370137426291014
   PubMed Web of Science ®Google Scholar
• SuzawaKToyookaSSakaguchiMAntitumor effect of afatinib, as a human epidermal growth factor receptor 2-targeted therapy, in lung cancers harboring HER2 oncogene alterationsCancer Sci20161071455226545934
   PubMed Web of Science ®Google Scholar
• MazieresJBarlesiFFilleronTLung cancer patients with HER2 mutations treated with chemotherapy and HER2-targeted drugs: results from the European EUHER2 cohortAnn Oncol201627228128626598547
   PubMed Web of Science ®Google Scholar
• MarNVredenburghJJWasserJSTargeting HER2 in the treatment of non-small cell lung cancerLung Cancer201587322022525601485
   PubMed Web of Science ®Google Scholar
• ZhangYSunYPanYFrequency of driver mutations in lung adenocarcinoma from female never-smokers varies with histologic subtypes and age at diagnosisClin Cancer Res20121871947195322317764
   PubMed Web of Science ®Google Scholar
• National Comprehensive Cancer NetworkNon-Small Cell Lung Cancer (Version 9, 2017) Available from: https://www.nccn.org/professionals/physician_gls/default.aspxAccessed January 3, 2018
   Google Scholar
• WangRZhangYPanYComprehensive investigation of oncogenic driver mutations in Chinese non-small cell lung cancer patientsOncotarget2015633343003430826486077
   PubMedGoogle Scholar
• SongZYuXShiZZhaoJZhangYHER2 mutations in Chinese patients with non-small cell lung cancerOncotarget2016747781527815827825109
   PubMedGoogle Scholar
• MazieresJPetersSLepageBLung cancer that harbors an HER2 mutation: epidemiologic characteristics and therapeutic perspectivesJ Clin Oncol201331161997200323610105
   PubMed Web of Science ®Google Scholar
• YangJCShihJYSuWCAfatinib for patients with lung adenocarcinoma and epidermal growth factor receptor mutations (LUX-Lung 2): a phase 2 trialLancet Oncol201213553954822452895
   PubMed Web of Science ®Google Scholar
• SequistLVYangJCYamamotoNPhase III study of afatinib or cisplatin plus pemetrexed in patients with metastatic lung adenocarcinoma with EGFR mutationsJ Clin Oncol201331273327333423816960
   PubMed Web of Science ®Google Scholar
• KatakamiNAtagiSGotoKLUX-Lung 4: a phase II trial of afatinib in patients with advanced non-small-cell lung cancer who progressed during prior treatment with erlotinib, gefitinib, or bothJ Clin Oncol201331273335334123816963
   PubMed Web of Science ®Google Scholar
• SchulerMYangJCParkKLUX-Lung 5 InvestigatorsAfatinib beyond progression in patients with non-small-cell lung cancer following chemotherapy, erlotinib/gefitinib and afatinib: phase III randomized LUX-lung 5 trialAnn Oncol201627341742326646759
   PubMed Web of Science ®Google Scholar
• WuYLZhouCHuCPAfatinib versus cisplatin plus gemcitabine for first-line treatment of Asian patients with advanced non-small-cell lung cancer harbouring EGFR mutations (LUX-Lung 6): an open-label, randomised phase 3 trialLancet Oncol201415221322224439929
   PubMed Web of Science ®Google Scholar
• ParkKTanEHO’ByrneKAfatinib versus gefitinib as first-line treatment of patients with EGFR mutation-positive non-small-cell lung cancer (LUX-Lung 7): a phase 2B, open-label, randomised controlled trialLancet Oncol201617557758927083334
   PubMed Web of Science ®Google Scholar
• SoriaJCFelipECoboMLUX-Lung 8 InvestigatorsAfatinib versus erlotinib as second-line treatment of patients with advanced squamous cell carcinoma of the lung (LUX-Lung 8): an open-label randomised controlled phase 3 trialLancet Oncol201516889790726156651
   PubMed Web of Science ®Google Scholar
• LeeVHLeungDKChoyTSEfficacy and safety of afatinib in Chinese patients with EGFR-mutated metastatic non-small-cell lung cancer (NSCLC) previously responsive to first-generation tyrosine-kinase inhibitors (TKI) and chemotherapy: comparison with historical cohort using erlotinibBMC Cancer20161614726911310
   PubMed Web of Science ®Google Scholar
• HirshVCadranelJCongXJSymptom and quality of life benefit of afatinib in advanced non-small-cell lung cancer patients previously treated with erlotinib or gefitinib: results of a randomized phase IIb/III trial (LUX-Lung 1)J Thorac Oncol20138222923723328549
   PubMed Web of Science ®Google Scholar
• KuanFCLiSHWangCLLinMHTsaiYHYangCTAnalysis of progression-free survival of first-line tyrosine kinase inhibitors in patients with non-small cell lung cancer harboring leu858Arg or exon 19 deletionsOncotarget2017811343135327935868
   PubMedGoogle Scholar
• De GreveJTeugelsEGeersCClinical activity of afatinib (BIBW 2992) in patients with lung adenocarcinoma with mutations in the kinase domain of HER2/neuLung Cancer201276112312722325357
   PubMed Web of Science ®Google Scholar
• ZhangLJCaiLLiZRelationship between epidermal growth factor receptor gene mutation and copy number in Chinese patients with non-small cell lung cancerChin J Cancer2012311049149922572014
   PubMedGoogle Scholar
• JiangBLiuFYangLSerum detection of epidermal growth factor receptor gene mutations using mutant-enriched sequencing in Chinese patients with advanced non-small cell lung cancerJ Int Med Res20113941392140121986139
   PubMed Web of Science ®Google Scholar
• WeiFLinCCJoonANoninvasive saliva-based EGFR gene mutation detection in patients with lung cancerAm J Respir Crit Care Med2014190101117112625317990
   PubMed Web of Science ®Google Scholar
• ChenSZhaoJCuiLLiuYUrinary circulating DNA detection for dynamic tracking of EGFR mutations for NSCLC patients treated with EGFR-TKIsClin Transl Oncol201719333234027468867
   PubMed Web of Science ®Google Scholar
• TakanoTOheYTsutaKEpidermal growth factor receptor mutation detection using high-resolution melting analysis predicts outcomes in patients with advanced non small cell lung cancer treated with gefitinibClin Cancer Res20071318 pt 15385539017875767
   PubMed Web of Science ®Google Scholar
• JannePABorrasAMKuangYA rapid and sensitive enzymatic method for epidermal growth factor receptor mutation screeningClin Cancer Res2006123 pt 175175816467085
   PubMed Web of Science ®Google Scholar
• HuYCZhangQHuangYHLiuYFChenHLComparison of two methods to extract DNA from formalin-fixed, paraffin-embedded tissues and their impact on EGFR mutation detection in non-small cell lung carcinomaAsian Pac J Cancer Prev20141562733273724761893
   PubMedGoogle Scholar
• VanderlaanPAYamaguchiNFolchESuccess and failure rates of tumor genotyping techniques in routine pathological samples with non-small-cell lung cancerLung Cancer2014841394424513263
   PubMed Web of Science ®Google Scholar
• VogelsteinBPapadopoulosNVelculescuVEZhouSDiazLAJrKinzlerKWCancer genome landscapesScience201333961271546155823539594
   PubMed Web of Science ®Google Scholar
• SacherAGPaweletzCDahlbergSEProspective validation of rapid plasma genotyping for the detection of EGFR and KRAS mutations in advanced lung cancerJAMA Oncol2016281014102227055085
   PubMed Web of Science ®Google Scholar
• SeoANParkTIJinYNovel EGFR mutation-specific antibodies for lung adenocarcinoma: highly specific but not sensitive detection of an E746_A750 deletion in exon 19 and an L858R mutation in exon 21 by immunohistochemistryLung Cancer201483331632324412618
   PubMed Web of Science ®Google Scholar
• AsanoHToyookaSTokumoMDetection of EGFR gene mutation in lung cancer by mutant-enriched polymerase chain reaction assayClin Cancer Res2006121434816397022
   PubMed Web of Science ®Google Scholar
• MaMShiCQianJTengJZhongHHanBComparison of plasma and tissue samples in epidermal growth factor receptor mutation by ARMS in advanced non-small cell lung cancerGene20165911586427370697
   PubMed Web of Science ®Google Scholar
• van DijkELAugerHJaszczyszynYThermesCTen years of next-generation sequencing technologyTrends Genet201430941842625108476
   PubMed Web of Science ®Google Scholar
• GoodwinSMcPhersonJDMcCombieWRComing of age: ten years of next-generation sequencing technologiesNat Rev Genet201617633335127184599
   PubMed Web of Science ®Google Scholar
• EllisonGDonaldEMcWalterGA comparison of ARMS and DNA sequencing for mutation analysis in clinical biopsy samplesJ Exp Clin Cancer Res20102913220925915
   PubMed Web of Science ®Google Scholar
• KozuYTsutaKKohnoTThe usefulness of mutation-specific antibodies in detecting epidermal growth factor receptor mutations and in predicting response to tyrosine kinase inhibitor therapy in lung adenocarcinomaLung Cancer2011731455021129809
   PubMed Web of Science ®Google Scholar
• WonJKKeamBKohJConcomitant ALK translocation and EGFR mutation in lung cancer: a comparison of direct sequencing and sensitive assays and the impact on responsiveness to tyrosine kinase inhibitorAnn Oncol201526234835425403583
   PubMed Web of Science ®Google Scholar
• ThompsonJCYeeSSTroxelABDetection of therapeutically targetable driver and resistance mutations in lung cancer patients by next-generation sequencing of cell-free circulating tumor DNAClin Cancer Res201622235772578227601595
   PubMed Web of Science ®Google Scholar
• KobayashiYAzumaKNagaiHCharacterization of EGFR T790M, L792F, and C797S mutations as mechanisms of acquired resistance to afatinib in lung cancerMol Cancer Ther201716235736427913578
   PubMed Web of Science ®Google Scholar
• HashidaSYamamotoHShienKAcquisition of cancer stem cell-like properties in non-small cell lung cancer with acquired resistance to afatinibCancer Sci2015106101377138426202045
   PubMed Web of Science ®Google Scholar
• LeeYWangYJamesMJeongJHYouMInhibition of IGF1R sig-naling abrogates resistance to afatinib (BIBW2992) in EGFR T790M mutant lung cancer cellsMol Carcinog2016555991100126052929
   PubMed Web of Science ®Google Scholar