Using Multiplexed Assays of Oncogenic Drivers in Lung Cancers to Select Targeted Drugs
Open accessAbstract
IMPORTANCE: Targeting oncogenic drivers (genomic alterations critical to cancer development and maintenance) has transformed the care of patients with lung adenocarcinomas. The Lung Cancer Mutation Consortium was formed to perform multiplexed assays testing adenocarcinomas of the lung for drivers in 10 genes to enable clinicians to select targeted treatments and enroll patients into clinical trials. OBJECTIVES: To determine the frequency of oncogenic drivers in patients with lung adenocarcinomas and to use the data to select treatments targeting the identified driver(s) and measure survival. DESIGN, SETTING, AND PARTICIPANTS: From 2009 through 2012, 14 sites in the United States enrolled patients with metastatic lung adenocarcinomas and a performance status of 0 through 2 and tested their tumors for 10 drivers. Information was collected on patients, therapies, and survival. INTERVENTIONS: Tumors were tested for 10 oncogenic drivers, and results were used to select matched targeted therapies. MAIN OUTCOMES AND MEASURES: Determination of the frequency of oncogenic drivers, the proportion of patients treated with genotype-directed therapy, and survival. RESULTS: From 2009 through 2012, tumors from 1007 patients were tested for at least 1 gene and 733 for 10 genes (patients with full genotyping). An oncogenic driver was found in 466 of 733 patients (64%). Among these 733 tumors, 182 tumors (25%) had the KRAS driver; sensitizing EGFR, 122 (17%); ALK rearrangements, 57 (8%); other EGFR, 29 (4%); 2 or more genes, 24 (3%); ERBB2 (formerly HER2), 19 (3%); BRAF, 16 (2%); PIK3CA, 6 (<1%); MET amplification, 5 (<1%); NRAS, 5 (<1%); MEK1, 1 (<1%); AKT1, 0. Results were used to select a targeted therapy or trial in 275 of 1007 patients (28%). The median survival was 3.5 years (interquartile range [IQR], 1.96-7.70) for the 260 patients with an oncogenic driver and genotype-directed therapy compared with 2.4 years (IQR, 0.88-6.20) for the 318 patients with any oncogenic driver(s) who did not receive genotype-directed therapy (propensity score-adjusted hazard ratio, 0.69 [95% CI, 0.53-0.9], P = .006). CONCLUSIONS AND RELEVANCE: Actionable drivers were detected in 64% of lung adenocarcinomas. Multiplexed testing aided physicians in selecting therapies. Although individuals with drivers receiving a matched targeted agent lived longer, randomized trials are required to determine if targeting therapy based on oncogenic drivers improves survival. TRIAL REGISTRATION: clinicaltrials.gov Identifier: NCT01014286.
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Claims the paper makes
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- Findingown data
Drivers in two genes were found in 3% (24 of 733) of fully genotyped tumors.
“2 or more genes, 24 (3%)”
- Also stated in: § Results · plain
“we found drivers in 2 genes in 24 tumors (3%).”
Quote in the paperNot a substantial claim - Also stated in: § Results · plain
- Findingown data
In the full genotype set, patients with a driver and targeted therapy had a median survival of 3.5 years, versus 2.5 years for those with a driver and no targeted therapy (P<.001).
“The 190 patients with an oncogenic driver and treatment with a targeted agent had a median survival of 3.5 years (IQR, 1.96-7.70); the 248 with a driver and no targeted therapy, 2.5 years (P < .001”
Quote in the paperSubstantial claim - Findingown data
ERBB2 mutations occurred in 3% (19 of 733) of fully genotyped tumors.
“ERBB2 (formerly HER2), 19 (3%)”
- Also stated in: § Results · plain
“The frequencies of ERBB2 (all exon 20 insertions) were 3% (19 of 733 specimens)”
Quote in the paperNot a substantial claim - Also stated in: § Results · plain
- Findingown data
Among patients with an oncogenic driver, those given genotype-directed therapy had a median survival of 3.5 years, compared with 2.4 years for those who did not receive such therapy.
“The median survival was 3.5 years (interquartile range [IQR], 1.96-7.70) for the 260 patients with an oncogenic driver and genotype-directed therapy compared with 2.4 years (IQR, 0.88-6.20) for the 318 patients with any oncogenic driver(s) who did not receive genotype-directed therapy”
- Also stated in: § Results · plain
“The 260 patients with an oncogenic driver and treatment with a targeted agent had a median survival of 3.5 years; the 318 patients with a driver and no targeted therapy, 2.4 years”
Quote in the paperSubstantial claim - Also stated in: § Results · plain
- Findingown data
ALK rearrangements were found in 8% (57 of 733) of fully genotyped tumors.
“ALK rearrangements, 57 (8%)”
- Also stated in: § Results · plain
“ALK rearrangements occurred in 57 of 733 specimens (8%).”
Quote in the paperNot a substantial claim - Also stated in: § Results · plain
- Findingown data
Among lung adenocarcinoma patients whose tumors were tested for all 10 drivers, an oncogenic driver was found in 64% (466 of 733).
“An oncogenic driver was found in 466 of 733 patients (64%).”
- Also stated in: § Results · plain
“Among the 733 specimens tested for all 10 genes, 466 (64% [95% CI, 60%-67%) had an oncogenic driver”
Quote in the paperSubstantial claim - Also stated in: § Results · plain
- Findingown data
In the fully genotyped group, KRAS mutations were the most common driver, present in 25% (182 of 733) of tumors.
“Among these 733 tumors, 182 tumors (25%) had the KRAS driver”
- Also stated in: § Results · plain
“KRAS mutations were the most frequent, found in 182 of 733 specimens (25%)”
Quote in the paperNot a substantial claim - Also stated in: § Results · plain
- Findingown data
Overall, 44% of individuals with a detected driver received a targeted therapy.
“Overall, 28% (95% CI, 24%-30%) of eligible patients and 44% of individuals with drivers detected received a targeted therapy.”
Quote in the paperSubstantial claim - Findingown data
Driver frequencies in the 1007 specimens with at least one gene assessed mirrored those in the fully genotyped group.
“The frequencies of drivers in the 1007 specimens in which at least 1 gene was assessed are presented in Table 2 and mirror the results with the patients’ tumors with full genotyping.”
Quote in the paperSubstantial claim - Findingown data
BRAF mutations occurred in 2% (16 of 733) of fully genotyped tumors.
“BRAF, 16 (2%)”
- Also stated in: § Results · plain
“BRAF mutations were 2% (16 of 733 specimens)”
Quote in the paperNot a substantial claim - Also stated in: § Results · plain
- Findingown data
In a propensity score-adjusted Cox model, genotype-directed therapy among patients with an oncogenic driver was associated with a lower risk of death (HR 0.69, 95% CI 0.53-0.9, P=.006).
“propensity score–adjusted hazard ratio, 0.69 [95% CI, 0.53-0.9], P = .006”
- Also stated in: § Results · plain
“showed a decreased risk of death (HR, 0.69 [95% CI, 0.53-0.9], P = .006).”
Quote in the paperSubstantial claim - Also stated in: § Results · plain
- Findingown data
Genotyping results were used to choose a targeted therapy or trial for 28% (275 of 1007) of patients.
“Results were used to select a targeted therapy or trial in 275 of 1007 patients (28%).”
Quote in the paperSubstantial claim - Findingown data
Among 1007 patients tested for at least one driver, 93% had sufficient information for survival analysis.
“Among the 1007 patients tested for at least 1 driver, 93% had sufficient information to be included in the survival analysis”
Quote in the paperNot a substantial claim - Findingown data
Sensitizing EGFR mutations occurred in 17% (122 of 733) of fully genotyped tumors.
“sensitizing EGFR, 122 (17%)”
- Also stated in: § Results · plain
“sensitizing EGFR (EGFR[s]) mutations (exon 19 deletions, L858R, L861Q, and G719X) in 122 of 733 specimens (17%)”
Quote in the paperNot a substantial claim - Also stated in: § Results · plain
- Findingown data
Of 80 patients with ALK rearrangements, 52 were treated with crizotinib.
“We treated 52 of the 80 patients (65%) with ALK rearrangements with crizotinib.”
Quote in the paperNot a substantial claim - Findingnone given
Patients with ERBB2 or MET alterations were placed on targeted trials.
“Patients with ERBB2 or MET were placed on targeted trials.”
Quote in the paperSubstantial claim - Findingown data
The LCMC identified 18 patients with BRAF mutations who were candidates for BRAF inhibitor trials.
“We identified 18 patients with BRAF mutations who were candidates for trials with BRAF inhibitors.”
Quote in the paperSubstantial claim - Study design and conductreasoning
Because treatment was not randomly assigned and was left to the treating physician's discretion, bias could have been introduced.
“Because treatment was not randomly assigned and was at the discretion of the treating physician, there is the potential to introduce bias.”
Quote in the paperSubstantial claim - Premisecitation
A listing of 11 oncology drugs approved for other indications that target 7 drivers found in lung cancers is now included in NCCN guidelines.
“A listing of 11 oncological drugs approved for other indications that target 7 oncological drivers found in lung cancers is now included in the National Comprehensive Cancer Network guidelines.8”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [8] National Comprehensive Cancer Network NCCN clinical practice guidelines in oncology 2014 http://www.nccn.org/professionals/physician_gls/f_guidelines.asp. Accessed April 21
Not checked in the free run.
- Premisecitation
As more oncogenic drivers are detected, testing for targets sequentially reduces efficiency.
“With additional oncogenic drivers being detected, testing for targets sequentially lessens the efficiency of the process.9”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [9] Atherly AJ Camidge DR The cost-effectiveness of screening lung cancer patients for targeted drug sensitivity markers Br J Cancer 2012 106 6 1100 1106 22374459 PMC3304427
Not checked in the free run.
- Study design and conductreasoning
Because the study was not randomized to compare survival by receipt of targeted therapy, its observations should be considered proof of concept rather than definitive.
“As this was not a randomized study designed to compare survival in patients with a tumor with an oncogenic driver based on whether or not they received a targeted therapy, our observations should be considered a proof of concept rather than a definitive result.”
Quote in the paperSubstantial claim - Study design and conductreasoning
The propensity score analysis may not have adequately ruled out confounding from known or unknown factors not included in the model.
“The propensity score analysis (including sex, age at enrollment, performance status, smoking history, stage at diagnosis, prior therapy, and elapsed time from metastatic disease diagnosis to study enrollment) may not have adequately ruled out confounding, due to other confounding factors—known or unknown—not included in the model.”
Quote in the paperSubstantial claim - Premisecitation
Lung adenocarcinoma has an estimated frequency of actionable oncogenic drivers above 50%.
“It is also the type of lung cancer with a higher than 50% estimated frequency of actionable oncogenic drivers.2,3”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [2] Pao W Girard N New driver mutations in non-small cell lung cancer Lancet Oncol 2011 12 2 175 180 21277552
Not checked in the free run.
- cites [3] Clinical Lung Cancer Genome Project, Network Genomic Medicine A genomics-based classification of human lung tumors Sci Transl Med 2013 5 209 209ra153 PMC4006630 24174329
Not checked in the free run.
- Interpretationown data
The LCMC showed that routine multiplex genotyping information can be generated from patients with lung adenocarcinomas.
“The LCMC demonstrated that it is possible to routinely generate multiplex genotyping information from patients with lung adenocarcinomas.”
Quote in the paperSubstantial claim - Study design and conductreasoning
The study design cannot support definitive conclusions that survival differences are attributable to determining and using oncogenic drivers.
“The study design is not appropriate to reach definitive conclusions about survival differences being attributable to the determination and use of oncogenic drivers.”
Quote in the paperSubstantial claim - Interpretationnone given
Multiplexed testing facilitates rapid inclusion of new oncogenic drivers into existing panels.
“Multiplexed testing also facilitates the rapid inclusion of new oncogenic drivers to existing panels.”
Quote in the paperNot a substantial claim - Interpretationown data
Performing multiplex genomic characterization detected additional mutations with little need for additional resources.
“Performing multiplex genomic characterization detected additional mutations with little need for additional resources.”
Quote in the paperSubstantial claim
- The quote only partly states this claim. 1
- May combine two claims. 8
- Classified as probably not a substantial claim. 9
The quote only partly states this claim.
Findingown dataOther EGFR mutations not linked to kinase inhibitor sensitivity were identified in 4% (29 of 733) of fully genotyped tumors.
“other EGFR, 29 (4%)”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataThe LCMC characterized at least one gene in 91% (1007 of 1102) of eligible patients and all 10 genes in 66% (733 of 1102).
“The LCMC characterized at least 1 gene for 91% (1007 of 1102 patients) of eligible patients with genotyping of all 10 genes in 66% (733 of 1102 patients).”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataThe median potential follow-up was 2.0 years.
“The median potential follow-up was 2.0 years.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataExcluding EGFR- and ALK-positive cancers, patients with other drivers who received targeted therapy had a median survival of 4.9 years, compared with 2.4 years for those with a driver not receiving targeted therapy and 2.1 years for those without a driver (P=.14).
“The 49 patients with oncogenic drivers other than EGFR or ALK who received a targeted therapy had a median survival of 4.9 years compared with the 678 with (318 patients) or without (360 patients) a driver identified, but not receiving a targeted agent, whose median survivals were 2.4 years with a driver (IQR, 0.88-6.20) and 2.1 years without (P = .14”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataOf 175 patients with sensitizing EGFR mutations, 146 received targeted therapy: 130 erlotinib alone and 16 another EGFR inhibitor alone or in combination.
“Of the 175 patients (83%) with EGFR(s) mutations, 146 were treated with targeted therapy: 130 with erlotinib alone, and 16 with another EGFR inhibitor alone or in combination.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataPatients in the driver plus treatment group had better prognostic features: 5% better performance status, 3-year lower median age, and more likely to be never smokers.
“Patients in the driver + treatment group had a 5% better performance status, a 3-year lower median age, and were more likely to be never smokers (Table 1); factors that could lead to an improved prognosis.”
Quote in the paperNot a substantial claimMay combine two claims.
Interpretationown dataMultiplexed testing helped physicians select therapies and patients for targeted trials.
“Multiplexed testing aided physicians in selecting therapies.”
- Also stated in: § Conclusions · plain
“Multiplexed testing aided physicians in selecting therapies and patients for targeted trials.”
Quote in the paperSubstantial claim- Also stated in: § Conclusions · plain
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationTesting for somatic EGFR mutations and ALK rearrangements is now routine.
“Testing for somatic mutations in the epidermal growth factor receptor (EGFR) gene4-6 and rearrangements of the anaplastic lymphoma kinase (ALK) gene7 is now routine.8”
Quote in the paperNot a substantial claim0 of 5 sources checked- cites [4] Lynch TJ Bell DW Sordella R Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small cell lung cancer to gefitinib N Engl J Med 2004 350 21 2129 2139 15118073
Not checked in the free run.
- cites [5] Paez JG Jänne PA Lee JC EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy Science 2004 304 5676 1497 1500 15118125
Not checked in the free run.
- cites [6] Pao W Miller V Zakowski M EGF receptor gene mutations are common in lung cancers from “never smokers” and are associated with sensitivity of tumors to gefitinib and erlotinib Proc Natl Acad SciUS A 2004 101 36 13306 13311 PMC516528 15329413
Not checked in the free run.
- cites [7] Kwak EL Bang YJ Camidge DR Anaplastic lymphoma kinase inhibition in non-small cell lung cancer N Engl J Med 2010 363 18 1693 1703 20979469 PMC3014291
Not checked in the free run.
- cites [8] National Comprehensive Cancer Network NCCN clinical practice guidelines in oncology 2014 http://www.nccn.org/professionals/physician_gls/f_guidelines.asp. Accessed April 21
Not checked in the free run.
Classified as probably not a substantial claim.
Study design and conductnone givenAdenocarcinoma was centrally confirmed.
“Adenocarcinoma was centrally confirmed.”
Quote in the paperSubstantial claimClassified as probably not a substantial claim.
Study design and conductown dataThe LCMC clinical committee chairs reviewed records to verify that the treatment administered was directed against the driver detected in the patient's tumor.
“The LCMC clinical committee chairs reviewed the records of each patient with an oncogenic driver and the targeted agent administered to verify that the treatment was directed against that driver(s) detected in the patient’s tumor.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductreasoningWith a planned sample size of 1000, the half-width of the 95% CI would be less than 5% if the oncogenic driver rate were less than 40%.
“With the proposed sample size of 1000, the half-width of the 95% CI is less than 5% if the oncogenic driver rate is less than 40%.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenThe decision to recommend targeted therapy for a patient with a driver was left to the treating physician.
“The decision to recommend a targeted therapy to a patient with a tumor harboring an oncogenic driver was left to the treating physician.”
Quote in the paperNot a substantial claimClassified as probably not a substantial claim.
Study design and conductown dataThe propensity model adjusted for sex, age at enrollment, performance status, smoking history, stage at diagnosis, prior therapy, and elapsed time from metastatic diagnosis to enrollment.
“The knowledge-based confounding variables adjusted in the propensity model were sex, age at enrollment, performance status, smoking history, stage at diagnosis, prior therapy (surgery, chest radiotherapy, or chemotherapy), and elapsed time from metastatic disease diagnosis to study enrollment (years).”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenCriteria for specimen adequacy were not prespecified.
“Criteria for specimen adequacy were not prespecified.”
Quote in the paperNot a substantial claimMay combine two claims.
PremisecitationThe LCMC effort differs from other genomic characterization efforts such as TCGA, which studied localized disease and used resection specimens.
“The LCMC effort differs from other genomic characterization efforts, like the Cancer Genome Atlas that studied patients with localized disease and obtained tissues exclusively from resection specimens.35-40”
Quote in the paperNot a substantial claim0 of 6 sources checked- cites [35] Weir BA Woo MS Getz G Characterizing the cancer genome in lung adenocarcinoma Nature 2007 450 7171 893 898 17982442 PMC2538683
Not checked in the free run.
- cites [36] Barletta JA Perner S Iafrate AJ Clinical significance of TTF-1 protein expression and TTF-1 gene amplification in lung adenocarcinoma J Cell Mol Med 2009 13 8B 1977 1986 19040416 PMC2830395
Not checked in the free run.
- cites [37] Hammerman PS Sos ML Ramos AH Mutations in the DDR2 kinase gene identify a novel therapeutic target in squamous cell lung cancer Cancer Discov 2011 1 1 78 89 22328973 PMC3274752
Not checked in the free run.
- cites [38] Cancer Genome Atlas Research Network Comprehensive genomic characterization of squamous cell lung cancers Nature 2012 489 7417 519 525 [published online September 27, 2012] 22960745 PMC3466113
Not checked in the free run.
- cites [39] D’Angelo SP Janjigian YY Ahye N Distinct clinical course of EGFR-mutant resected lung cancers: results of testing of 1118 surgical specimens and effects of adjuvant gefitinib and erlotinib J Thorac Oncol 2012 7 12 1815 1822 23154553
Not checked in the free run.
- cites [40] Peifer M Fernández-Cuesta L Sos ML Integrative genome analyses identify key somatic driver mutations of small cell lung cancer Nat Genet 2012 44 10 1104 1110 22941188 PMC4915822
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Study design and conductnone givenLCMC pathologists shared blinded samples, with a positive sample included for all 10 drivers.
“The LCMC pathologists shared blinded samples, with a positive sample included for all 10 drivers.”
Quote in the paperNot a substantial claimMay combine two claims.
InterpretationreasoningThe multiplexed genotyping platforms made effective use of patient tissue and identified actionable drivers sooner, giving patients earlier access to therapies or trials.
“The multiplexed genotyping platforms made effective use of patient tissue and identified actionable drivers sooner, giving patient’s earlier access to therapies or trials.”
Quote in the paperSubstantial claim
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The presence of EGFR mutations defines a specific molecular subgroup of NSCLC (~15% of Caucasian patients with adenocarcinomas) that respond to an EGFR TKI in over 60% of patients.
“The presence of EGFR mutations defines a specific molecular subgroup of NSCLC (~15% of Caucasian patients with adenocarcinomas) [37, 38] that respond to an EGFR TKI in over 60% of patients (Table 1).”
From A decade of EGFR inhibition in EGFR-mutated non small cell lung cancer (NSCLC): Old successes and future perspectives (2015) · cites this paper as [38]
Somatic mutations in the kinase domain of EGFR are detected in approximately 40% of lung adenocarcinoma in Asians and 17% in Caucasians.
“Somatic mutations in the kinase domain of the epidermal growth factor receptor (EGFR) gene are detected in approximately 40% and 17% of lung adenocarcinoma in Asians1 and in Caucasians,2 respectively.”
From Not all epidermal growth factor receptor mutations in lung cancer are created equal: Perspectives for individualized treatment strategy (2016) · cites this paper as [2]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
MET amplification count differs within the full-genotyping results
MajorMET amplification is reported in 5 of the 733 fully genotyped tumors, but the later count assigns MET amplification to 8 double-driver tumors in that group.
“Amplification of MET (MET/ CEP7 >2.2) was found in 5 of 733 patients’ tumors (<1%).”
“In the full genotyping group, we found drivers in 2 genes in 24 tumors (3%). Of these 24 specimens, 20 (83%) included either a mutation in PIK3CA (n = 12) or MET amplification (n = 8).”
Targeted-therapy percentage is overstated
MinorThe reported 275 of 1007 patients is 27.3%, which rounds to 27%, not 28%.
Reported 28 · recomputed 27.308838
“Results were used to select a targeted therapy or trial in 275 of 1007 patients (28%).”
Supplementary figure number conflicts for the exclusion analysis
MinorThe Results attribute the analysis excluding EGFR- and ALK-positive cancers to eFigure 6, whereas the Discussion attributes that analysis to eFigure 4.
“We also recomputed the survival data excluding individuals with EGFR- and ALK-positive cancers. The 49 patients with oncogenic drivers other than EGFR or ALK who received a targeted therapy had a median survival of 4.9 years compared with the 678 with (318 patients) or without (360 patients) a driver identified, but not receiving a targeted agent, whose median survivals were 2.4 years with a driver (IQR, 0.88-6.20) and 2.1 years without (P = .14; eFigure 6 in the Supplement).”
“survival analyses excluding these patients revealed that individuals with other drivers treated with targeted therapies still had an observed 2.5-year improvement in median survival over those who did not receive targeted therapy (eFigure 4 in the Supplement).”
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KIF5B-RET fusions in lung adenocarcinoma
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Clinical Characteristics of Patients With Lung Adenocarcinomas Harboring BRAF Mutations
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Self-citationA Genomics-Based Classification of Human Lung Tumors
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Self-citationMutations in the DDR2 Kinase Gene Identify a Novel Therapeutic Target in Squamous Cell Lung Cancer
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Self-citationNatural History and Molecular Characteristics of Lung Cancers Harboring EGFR Exon 20 Insertions
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Self-citationErlotinib for Frontline Treatment of Advanced Non–Small Cell Lung Cancer: a Phase II Study
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“exon19 del 103 (10) [9-12] 68 (9) [7-12]”
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Characteristics of Lung Cancers Harboring NRAS Mutations
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Self-citationThe cost-effectiveness of screening lung cancer patients for targeted drug sensitivity markers
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Self-citationNCI-MATCH Launch Highlights New Trial Design in Precision-Medicine Era:
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ALK inhibitors and advanced non-small cell lung cancer (Review)
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The biology and management of non-small cell lung cancer
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Memorial Sloan Kettering-Integrated Mutation Profiling of Actionable Cancer Targets (MSK-IMPACT)
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Self-citationVemurafenib in Multiple Nonmelanoma Cancers with <i>BRAF</i> V600 Mutations
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The global burden of lung cancer: current status and future trends
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Self-citationTrastuzumab Deruxtecan in HER2 -Mutant Non–Small-Cell Lung Cancer
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Understanding and targeting resistance mechanisms in NSCLC
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Current Challenges in Cancer Treatment
Zugazagoitia, J., Guedes, C., Ponce, S., Ferrer, I., Molina‐Pinelo, S., & Paz-Ares, L. G. (2016) · Clinical Therapeutics · doi:10.1016/j.clinthera.2016.03.026 · Cited by 929 · see citing works
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Self-citationCell death-based treatment of lung adenocarcinoma
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Tumor biomarkers for diagnosis, prognosis and targeted therapy
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NCCN Guidelines Insights: Non–Small Cell Lung Cancer, Version 4.2016
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Self-citationPrecision Diagnosis and Treatment for Advanced Non–Small-Cell Lung Cancer
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“academic centers, one oncogenic driver mutation could be tested in 91% of tissue specimens but the ten desired target gene alterations could only be measured in 66% of them, a shortfall of 25% [8].”
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Self-citationNon‐small cell lung cancer in China
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Overcoming therapy resistance in EGFR-mutant lung cancer
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Self-citationPrecision medicine for cancer with next-generation functional diagnostics
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Self-citationThird-generation EGFR and ALK inhibitors: mechanisms of resistance and management
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Self-citation
- Authors
- Kris, M. G., Johnson, B. E., Berry, L. D., Kwiatkowski, D. J., Iafrate, A. J., Wistuba, I. I., Varella-Garcia, M., Franklin, W. A., Aronson, S. L., Su, P.-F., Shyr, Y., Camidge, D. R., Sequist, L. V., Glisson, B. S., Khuri, F. R., Garon, E. B., Pao, W., Rudin, C., Schiller, J., Haura, E. B., Socinski, M., Shirai, K., Chen, H., Giaccone, G., Ladanyi, M., Kugler, K., Minna, J. D., & Bunn, P. A.
- Affiliations
- Memorial Sloan Kettering Cancer Center (US)
- Dana-Farber Cancer Institute (US)
- Vanderbilt University (US)
- Brigham and Women's Hospital (US)
- Massachusetts General Hospital (US)
- The University of Texas MD Anderson Cancer Center (US)
- University of Colorado Cancer Center Denver, Aurora
- University of Colorado Cancer Center (US)
- The Partners HealthCare Center for Personalized Genetic Medicine, Boston, Massachusetts
- Winship Cancer Institute (US)
- University of California, Los Angeles (US)
- Johns Hopkins University (US)
- The University of Texas Southwestern Medical Center (US)
- Moffitt Cancer Center (US)
- UPMC Hillman Cancer Center (US)
- Medical University of South Carolina (US)
- National Institutes of Health (US)
- Corresponding author
- Kris, Mark G.
- ORCID
- Kris, Mark G.
- Johnson, Bruce E.
- Berry, Lynne D.
- Kwiatkowski, David J.
- Iafrate, A. John
- Wistuba, Ignacio I.
- Shyr, Yu
- Camidge, D. Ross
- Sequist, Lecia V.
- Glisson, Bonnie S.
- Khuri, Fadlo R.
- Garon, Edward B.
- Pao, William
- Rudin, Charles
- Schiller, Joan
- Haura, Eric B.
- Socinski, Mark
- Shirai, Keisuke
- Chen, Heidi
- Giaccone, Giuseppe
- Ladanyi, Marc
- Minna, John D.
- Bunn, Paul A.
- Venue
- JAMA
- Publisher
- American Medical Association (AMA)
- Published
- 2014-05-21
- Volume
- 311
- Issue
- 19
- Pages
- 1998
- ISSN
- 0002-9955 (ISSN-L)
- 0098-7484
- PMC
- PMC4163053
- OpenAlex
- W2065477010
- Semantic Scholar
- 07fff1c9d77fb2b8731d7d86b38c7ac05df654c7
- Cited by
- 1,724
- References
- 69
- Citations by year
- 2026: 55 · 2025: 99 · 2024: 101 · 2023: 116 · 2022: 164 · 2021: 171 · 2020: 173 · 2019: 137 · 2018: 186 · 2017: 162 · 2016: 173 · 2015: 146 · 2014: 37 · 2013: 2
- FWCI
- 138.25
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- JAMA (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (UL1TR000124)
- National Cancer Institute (RC2CA148394, K23CA149079, P01CA129243, 1RC2CA148394‐010, P50CA058187, P30CA008748, P30CA016672, P30CA046934)
- National Center for Advancing Translational Sciences
- Topics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Lung Cancer Treatments and Mutations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Lung Cancer Diagnosis and Treatment
- Keywords
- lung adenocarcinoma, oncogenic drivers, targeted therapy, multiplex genotyping, KRAS, EGFR, ALK rearrangement, BRAF, PIK3CA, ERBB2, MET amplification, NRAS, MEK1, AKT1, metastatic lung cancer, survival, genotype-directed therapy, clinical trial recruitment
- MeSH terms
- Adenocarcinoma of Lung, Adenocarcinoma, Aged, Female, Genotype, Humans, Lung Neoplasms, Male, Middle Aged, Proto-Oncogenes, Survival Analysis, Sequence Analysis, DNA, Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization, Molecular Targeted Therapy, Multiplex Polymerase Chain Reaction
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-06.
Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-06.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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