Rebiopsy of Lung Cancer Patients with Acquired Resistance to EGFR Inhibitors and Enhanced Detection of the T790M Mutation Using a Locked Nucleic Acid-Based Assay

Arcila, Maria E.; Oxnard, Geoffrey R.; Nafa, Khedoudja; Riely, Gregory J.; Solomon, Stephen B.; Zakowski, Maureen F.; Kris, Mark G.; Pao, William; Miller, Vincent A.; Ladanyi, Marc

doi:10.1158/1078-0432.ccr-10-2277

Cited by 574Lung Cancer Treatments and MutationsHER2/EGFR in Cancer ResearchCancer Genomics and Diagnostics

Rebiopsy of Lung Cancer Patients with Acquired Resistance to EGFR Inhibitors and Enhanced Detection of the T790M Mutation Using a Locked Nucleic Acid-Based Assay

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Arcila, Maria E., Oxnard, Geoffrey R., Nafa, Khedoudja, Riely, Gregory J., Solomon, Stephen B., Zakowski, Maureen F., Kris, Mark G., Pao, William +2 more·2011·Clinical Cancer Research

DOI 10.1158/1078-0432.ccr-10-2277PMC PMC3070951

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Abstract

Background: The epidermal growth factor receptor (EGFR) mutation T790M is reported in approximately 50% of lung cancers with acquired resistance to EGFR inhibitors and is a potential prognostic and predictive biomarker. Its assessment can be challenging due to limited tissue availability and underdetection at low mutant allele levels. Here, we sought to determine the feasibility of tumor rebiopsy and to more accurately assess the prevalence of the T790M using a highly sensitive locked nucleic acid (LNA) PCR/sequencing assay. MET amplification was also analyzed. Methods: Patients with acquired resistance were rebiopsied and samples were studied for sensitizing EGFR mutations. Positive cases were evaluated for T790M using standard PCR-based methods and a subset were re-evaluated with an LNA-PCR/sequencing method with an analytical sensitivity of approximately 0.1%. MET amplification was assessed by FISH. Results: Of 121 patients undergoing tissue sampling, 104 (86%) were successfully analyzed for sensitizing EGFR mutations. Most failures were related to low tumor content. All patients (61/61) with matched pretreatment and resistance specimens showed concordance for the original sensitizing EGFR mutation. Standard T790M mutation analysis on 99 patients detected 51(51%) mutants. Retesting of 30 negative patients by the LNA-based method detected 11 additional mutants for an estimated prevalence of 68%. MET was amplified in 11% of cases (4/37). Conclusions: The re-biopsy of lung cancer patients with acquired resistance is feasible and provides sufficient material for mutation analysis in most patients. Using high sensitivity methods, the T790M is detected in up to 68% of these patients. Clin Cancer Res; 17(5); 1169–80. ©2011 AACR.

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Approximately 10-25% of NSCLC cases are not eligible for a biopsy or do not have adequate tissue.
“as approximately 10-25% of NSCLC cases are not eligible for a biopsy or do not have adequate tissue68,69.”
From Selective KRAS G12C inhibitors in non-small cell lung cancer: chemistry, concurrent pathway alterations, and clinical outcomes (2021) · cites this paper as [69]
Acquired resistance to conventional EGFR-TKIs develops after a median of 10 to 12 months and is most commonly mediated by an acquired T790M mutation.
“Resistance to conventional EGFR-TKIs develops after a median of 10 to 12 months and is most commonly mediated by an acquired mutation, T790M1-5.”
From Association Between Plasma Genotyping and Outcomes of Treatment With Osimertinib (AZD9291) in Advanced Non–Small-Cell Lung Cancer (2016) · cites this paper as [1]
Primary EGFR sensitizing mutations are early truncal events, and prior work found little heterogeneity across multiple biopsies.
“each initial EGFR sensitizing mutation is an early “truncal” event in the pathogenesis of lung adenocarcinoma, and previous studies have not detected significant heterogeneity across multiple biopsies (5,37).”
From Detection of T790M, the Acquired Resistance EGFR Mutation, by Tumor Biopsy versus Noninvasive Blood-Based Analyses (2016) · cites this paper as [37]

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Lu, X., Yu, L., Zhang, Z., Ren, X., Smaill, J. B., & Ding, K. (2018) · Medicinal Research Reviews · doi:10.1002/med.21488 · Cited by 173 · see citing works
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He, M., Capelletti, M., Nafa, K., Yun, C.-H., Arcila, M. E., Miller, V. A., Ginsberg, M. S., Zhao, B., Kris, M. G., Eck, M. J., et al. (2012) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-11-2361 · Cited by 149 · see citing works
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Hochmair, M. J., Morabito, A., Hao, D., Yang, C.-T., Soo, R. A., Yang, J. C.-H., Gucalp, R., Halmos, B., Wang, L., Märten, A., et al. (2019) · Future Oncology · doi:10.2217/fon-2019-0346 · Cited by 85 · see citing works
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Jenkins, S., Chih-Hsin Yang, J., Jänne, P. A., Thress, K. S., Yu, K., Hodge, R., Weston, S., Dearden, S., Patel, S., Cantarini, M., et al. (2017) · Journal of Thoracic Oncology · doi:10.1016/j.jtho.2017.05.002 · Cited by 53 · see citing works
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Peng, L., Song, Z.-G., & Jiao, S.-C. (2014) · Scientific Reports · doi:10.1038/srep06104 · Cited by 48 · see citing works
Continuing EGFR inhibition beyond progression in advanced non-small cell lung cancer
Yap, T. A., Macklin-Doherty, A., & Popat, S. (2017) · European Journal of Cancer · doi:10.1016/j.ejca.2016.10.014 · Cited by 38 · see citing works
AZD9291 in EGFR -Mutant Advanced Non-Small-Cell Lung Cancer Patients
Remon, J., & Planchard, D. (2015) · Future Oncology · doi:10.2217/fon.15.250 · Cited by 33 · see citing works
Molecular determinants of drug-specific sensitivity for epidermal growth factor receptor (EGFR) exon 19 and 20 mutants in non-small cell lung cancer
Tsigelny, I. F., Wheler, J. J., Greenberg, J. P., Kouznetsova, V. L., Stewart, D. J., Bazhenova, L., & Kurzrock, R. (2015) · Oncotarget · doi:10.18632/oncotarget.3472 · Cited by 30 · see citing works
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Jia, J., Morse, M. A., Nagy, R. J., Lanman, R. B., & Strickler, J. H. (2018) · Frontiers in Oncology · doi:10.3389/fonc.2018.00305 · Cited by 17 · see citing works

EGFR T790M resistance mutation in NSCLC: Real-life data of patients treated with osimertinib.
Hochmair, M. J., Holzer, S., Filipits, M., Mohn-Staudner, A., Arns, M., Errhalt, P., Absenger, G., Koller-Herzog, U., Setinek, U., Haslbauer, F., et al. (2016) · Journal of Clinical Oncology · doi:10.1200/jco.2016.34.15_suppl.e20572 · Cited by 3 · see citing works
P3.02b-040 A Comparison of ddPCR and ARMS for Detecting EGFR T790M Status from Advanced NSCLC Patients with Acquired EGFR-TKI Resistance
Wang, W., Song, Z., Zhang, Y., et al. (2017) · Journal of Thoracic Oncology · doi:10.1016/j.jtho.2016.11.1707 · Cited by 2 · see citing works
P2.03-040 EGFR T790M Mutation Detection and Osimertinib Treatment Response Evaluation by Liquid Biopsy in Advanced NSCLC Patients
Li, C., Liu, H., Zhang, B., Zhang, Z., Su, Y., & Wang, C. (2017) · Journal of Thoracic Oncology · doi:10.1016/j.jtho.2017.09.1291 · Cited by 1 · see citing works
EGFR T790M detection and osimertinib treatment response evaluation by liquid biopsy in lung adenocarcinoma patients with acquired resistance to first generation EGFR tyrosine kinase inhibitors
Li, C., Jia, R., Liu, H., Zhang, B., & Wang, C. (2018) · Diagnostic Pathology · doi:10.1186/s13000-018-0728-6 · Cited by 20 · see citing works
EGFR T790M Mutation Detection in Patients With Non-Small Cell Lung Cancer After First Line EGFR TKI Therapy: Summary of Results in a Three-Year Period and a Comparison of Commercially Available Detection Kits
Bencze, E., Bogos, K., Kohánka, A., Báthory-Fülöp, L., Sárosi, V., Csernák, E., Bittner, N., Melegh, Z., & Tóth, E. (2022) · Pathology & Oncology Research · doi:10.3389/pore.2022.1610607 · Cited by 15 · see citing works

Authors: Arcila, M. E., Oxnard, G. R., Nafa, K., Riely, G. J., Solomon, S. B., Zakowski, M. F., Kris, M. G., Pao, W., Miller, V. A., & Ladanyi, M.
Affiliations: Memorial Sloan Kettering Cancer Center (US)
Authors' Affiliations: 1Molecular Diagnostics Service, Department of Pathology; 2Thoracic Oncology Service, Division of Solid Tumor Oncology, Department of Medicine; 3Interventional Radiology Service, Department of Radiology; and 4Human Oncology and Pathogenesis Program, Memorial Sloan-Kettering Cancer Center, New York, New York
Corresponding author: Ladanyi, Marc
ORCID: Arcila, Maria E.
Oxnard, Geoffrey R.
Riely, Gregory J.
Solomon, Stephen B.
Zakowski, Maureen F.
Kris, Mark G.
Pao, William
Miller, Vincent A.
Ladanyi, Marc
Venue: Clinical Cancer Research
Publisher: American Association for Cancer Research (AACR)
Published: 2011-03-01
Volume: 17
Issue: 5
Pages: 1169-1180
ISSN: 1078-0432 (ISSN-L)
1557-3265
DOI: 10.1158/1078-0432.ccr-10-2277
PMC: PMC3070951
OpenAlex: W2022670843
Cited by: 574
References: 48
Citations by year: 2026: 7 · 2025: 10 · 2024: 16 · 2023: 18 · 2022: 35 · 2021: 34 · 2020: 34 · 2019: 41 · 2018: 61 · 2017: 62 · 2016: 57 · 2015: 52 · 2014: 40 · 2013: 53 · 2012: 36
FWCI: 39.70
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Clinical Cancer Research (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
National Cancer Institute (R01CA121210, P01CA129243, R21CA115051)
Topics: Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Lung Cancer Treatments and Mutations
Health Sciences › Medicine › Oncology › HER2/EGFR in Cancer Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
Keywords: lung cancer, EGFR inhibitors, acquired drug resistance, T790M mutation, MET amplification, predictive biomarkers
MeSH terms: Adult, Aged, Aged, 80 and over, Alleles, Biopsy, DNA Mutational Analysis, Female, Humans, Lung Neoplasms, Male, Middle Aged, Mutation, Oligonucleotides, Prognosis, Biomarkers, Tumor, Polymerase Chain Reaction, In Situ Hybridization, Fluorescence, Drug Resistance, Neoplasm, ErbB Receptors

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Rebiopsy of Lung Cancer Patients with Acquired Resistance to EGFR Inhibitors and Enhanced Detection of the T790M Mutation Using a Locked Nucleic Acid-Based Assay

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