EGFR mutation testing in lung cancer: a review of available methods and their use for analysis of tumour tissue and cytology samples

Ellison, Gillian; Zhu, Guanshan; Moulis, Alexandros; Dearden, Simon; Speake, Georgina; McCormack, Rose

doi:10.1136/jclinpath-2012-201194

Cited by 301Lung Cancer Treatments and MutationsHER2/EGFR in Cancer ResearchCancer Genomics and Diagnostics

EGFR mutation testing in lung cancer: a review of available methods and their use for analysis of tumour tissue and cytology samples

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Ellison, Gillian, Zhu, Guanshan, Moulis, Alexandros, Dearden, Simon, Speake, Georgina, McCormack, Rose·2013·Journal of Clinical Pathology

DOI 10.1136/jclinpath-2012-201194PMC PMC3582044

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Abstract

AIMS: Activating mutations in the gene encoding epidermal growth factor receptor (EGFR) can confer sensitivity to EGFR tyrosine kinase inhibitors such as gefitinib in patients with advanced non-small-cell lung cancer. Testing for mutations in EGFR is therefore an important step in the treatment-decision pathway. We reviewed reported methods for EGFR mutation testing in patients with lung cancer, initially focusing on studies involving standard tumour tissue samples. We also evaluated data on the use of cytology samples in order to determine their suitability for EGFR mutation analysis. METHODS: We searched the MEDLINE database for studies reporting on EGFR mutation testing methods in patients with lung cancer. RESULTS: Various methods have been investigated as potential alternatives to the historical standard for EGFR mutation testing, direct DNA sequencing. Many of these are targeted methods that specifically detect the most common EGFR mutations. The development of targeted mutation testing methods and commercially available test kits has enabled sensitive, rapid and robust analysis of clinical samples. The use of screening methods, subsequent to sample micro dissection, has also ensured that identification of more rare, uncommon mutations is now feasible. Cytology samples including fine needle aspirate and pleural effusion can be used successfully to determine EGFR mutation status provided that sensitive testing methods are employed. CONCLUSIONS: Several different testing methods offer a more sensitive alternative to direct sequencing for the detection of common EGFR mutations. Evidence published to date suggests cytology samples are viable alternatives for mutation testing when tumour tissue samples are not available.

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Molecular testing of biopsy and cytologic samples with adequate material yields similar failure rates.
“molecular studies of biopsy and cytologic samples with adequate material have yielded similar failure rates.40,43,44”
From The International Association for the Study of Lung Cancer Consensus Statement on Optimizing Management of EGFR Mutation–Positive Non–Small Cell Lung Cancer: Status in 2016 (2016) · cites this paper as [44]

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Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008
Ferlay, J., Shin, H., Bray, F., Forman, D., Mathers, C. D., & Parkin, D. M. (2010) · International Journal of Cancer · doi:10.1002/ijc.25516 · Cited by 21,271 · see citing works
Activating Mutations in the Epidermal Growth Factor Receptor Underlying Responsiveness of Non–Small-Cell Lung Cancer to Gefitinib
Lynch, T. J., Bell, D. W., Sordella, R., Gurubhagavatula, S., Okimoto, R. A., Brannigan, B. W., Harris, P. L., Haserlat, S. M., Supko, J. G., Haluska, F. G., et al. (2004) · New England Journal of Medicine · doi:10.1056/nejmoa040938 · Cited by 11,486 · see citing works
EGFR Mutations in Lung Cancer: Correlation with Clinical Response to Gefitinib Therapy
Paez, J. G., Jänne, P. A., Lee, J. C., Tracy, S., Greulich, H., Gabriel, S., Herman, P., Kaye, F. J., Lindeman, N., Boggon, T. J., et al. (2004) · Science · doi:10.1126/science.1099314 · Cited by 9,368 · see citing works
Gefitinib or Carboplatin–Paclitaxel in Pulmonary Adenocarcinoma
Mok, T. S., Wu, Y.-L., Thongprasert, S., Yang, C.-H., Chu, D.-T., Saijo, N., Sunpaweravong, P., Han, B., Margono, B., Ichinose, Y., et al. (2009) · New England Journal of Medicine · doi:10.1056/nejmoa0810699 · Cited by 8,261 · see citing works
Gefitinib or Chemotherapy for Non–Small-Cell Lung Cancer with Mutated EGFR
Maemondo, M., Inoue, A., Kobayashi, K., Sugawara, S., Oizumi, S., Isobe, H., Gemma, A., Harada, M., Yoshizawa, H., Kinoshita, I., et al. (2010) · New England Journal of Medicine · doi:10.1056/nejmoa0909530 · Cited by 5,525 · see citing works
Erlotinib versus standard chemotherapy as first-line treatment for European patients with advanced EGFR mutation-positive non-small-cell lung cancer (EURTAC): a multicentre, open-label, randomised phase 3 trial
Rosell, R., Carcereny, E., Gervais, R., Vergnenegre, A., Massuti, B., Felip, E., Palmero, R., Garcia-Gomez, R., Pallares, C., Sanchez, J. M., et al. (2012) · The Lancet Oncology · doi:10.1016/s1470-2045(11)70393-x · Cited by 5,489 · see citing works
EGF receptor gene mutations are common in lung cancers from “never smokers” and are associated with sensitivity of tumors to gefitinib and erlotinib
Pao, W., Miller, V., Zakowski, M., Doherty, J., Politi, K., Sarkaria, I., Singh, B., Heelan, R., Rusch, V., Fulton, L., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0405220101 · Cited by 4,338 · see citing works
Gefitinib versus cisplatin plus docetaxel in patients with non-small-cell lung cancer harbouring mutations of the epidermal growth factor receptor (WJTOG3405): an open label, randomised phase 3 trial
Mitsudomi, T., Morita, S., Yatabe, Y., Negoro, S., Okamoto, I., Tsurutani, J., Seto, T., Satouchi, M., Tada, H., Hirashima, T., et al. (2010) · The Lancet Oncology · doi:10.1016/s1470-2045(09)70364-x · Cited by 4,090 · see citing works
Erlotinib versus chemotherapy as first-line treatment for patients with advanced EGFR mutation-positive non-small-cell lung cancer (OPTIMAL, CTONG-0802): a multicentre, open-label, randomised, phase 3 study
Zhou, C., Wu, Y.-L., Chen, G., Feng, J., Liu, X.-Q., Wang, C., Zhang, S., Wang, J., Zhou, S., Ren, S., et al. (2011) · The Lancet Oncology · doi:10.1016/s1470-2045(11)70184-x · Cited by 4,081 · see citing works
Epidermal growth factor receptor mutations in lung cancer
Sharma, S. V., Bell, D. W., Settleman, J., & Haber, D. A. (2007) · Nature Reviews Cancer · doi:10.1038/nrc2088 · Cited by 3,170 · see citing works
American Society of Clinical Oncology Clinical Practice Guideline Update on Chemotherapy for Stage IV Non–Small-Cell Lung Cancer
Azzoli, C. G., Baker, S., Temin, S., Pao, W., Aliff, T., Brahmer, J., Johnson, D. H., Laskin, J. L., Masters, G., Milton, D., et al. (2009) · Journal of Clinical Oncology · doi:10.1200/jco.2009.23.5622 · Cited by 915 · see citing works
The BATTLE Trial: Personalizing Therapy for Lung Cancer
Kim, E. S., Herbst, R. S., Wistuba, I. I., Lee, J. J., Blumenschein, G. R., Tsao, A. S., Stewart, D. J., Hicks, M. E., Erasmus, J. J., Gupta, S. K., et al. (2011) · Cancer Discovery · doi:10.1158/2159-8274.cd-10-0010 · Cited by 888 · see citing works
First-SIGNAL: First-Line Single-Agent Iressa Versus Gemcitabine and Cisplatin Trial in Never-Smokers With Adenocarcinoma of the Lung
Han, J.-Y., Park, K., Kim, S.-W., Lee, D. H., Kim, H. Y., Kim, H. T., Ahn, M. J., Yun, T., Ahn, J. S., Suh, C., et al. (2012) · Journal of Clinical Oncology · doi:10.1200/jco.2011.36.8456 · Cited by 736 · see citing works
The Relationship between Epidermal Growth Factor Receptor Mutations and Clinicopathologic Features in Non–Small Cell Lung Cancers
Tokumo, M., Toyooka, S., Kiura, K., Shigematsu, H., Tomii, K., Aoe, M., Ichimura, K., Tsuda, T., Yano, M., Tsukuda, K., et al. (2005) · Clinical Cancer Research · doi:10.1158/1078-0432.1167.11.3 · Cited by 489 · see citing works
Sensitive Sequencing Method for KRAS Mutation Detection by Pyrosequencing
Ogino, S., Kawasaki, T., Brahmandam, M., Yan, L., Cantor, M., Namgyal, C., Mino-Kenudson, M. A., Lauwers, G. Y., Loda, M. F., & Fuchs, C. S. (2005) · Journal of Molecular Diagnostics · doi:10.1016/s1525-1578(10)60571-5 · Cited by 488 · see citing works
American Society of Clinical Oncology Provisional Clinical Opinion: Epidermal Growth Factor Receptor (EGFR) Mutation Testing for Patients With Advanced Non–Small-Cell Lung Cancer Considering First-Line EGFR Tyrosine Kinase Inhibitor Therapy
Keedy, V. L., Temin, S., Somerfield, M. R., Beasley, M. B., Johnson, D. H., McShane, L. M., Milton, D. T., Strawn, J. R., Wakelee, H. A., & Giaccone, G. (2011) · Journal of Clinical Oncology · doi:10.1200/jco.2010.31.8923 · Cited by 486 · see citing works
Profiling Critical Cancer Gene Mutations in Clinical Tumor Samples
MacConaill, L. E., Campbell, C. D., Kehoe, S. M., Bass, A. J., Hatton, C., Niu, L., Davis, M., Yao, K., Hanna, M., Mondal, C., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007887 · Cited by 434 · see citing works
Rapid targeted mutational analysis of human tumours: a clinical platform to guide personalized cancer medicine
Dias-Santagata, D. C., Akhavanfard, S., David, S. S., Vernovsky, K., Kuhlmann, G., Boisvert, S. L., Stubbs, H., McDermott, U., Settleman, J. E., Kwak, E. L., et al. (2010) · EMBO Molecular Medicine · doi:10.1002/emmm.201000070 · Cited by 392 · see citing works
Implementing multiplexed genotyping of non-small-cell lung cancers into routine clinical practice
Sequist, L. V., Heist, R. S., Shaw, A. T., Fidias, P., Rosovsky, R., Temel, J. S., Lennes, I. T., Digumarthy, S., Waltman, B. A., Bast, E., et al. (2011) · Annals of Oncology · doi:10.1093/annonc/mdr489 · Cited by 370 · see citing works
Replacing PCR with COLD-PCR enriches variant DNA sequences and redefines the sensitivity of genetic testing
Li, J., Wang, L., Mamon, H. J., Kulke, M. H., Berbeco, R. I., & Makrigiorgos, G. M. (2008) · Nature Medicine · doi:10.1038/nm1708 · Cited by 368 · see citing works
Biomarkers of Response to Epidermal Growth Factor Receptor Inhibitors in Non–Small-Cell Lung Cancer Working Group: Standardization for Use in the Clinical Trial Setting
Eberhard, D. A., Giaccone, G., & Johnson, B. E. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2007.12.9858 · Cited by 300 · see citing works
Rapid Polymerase Chain Reaction-Based Detection of Epidermal Growth Factor Receptor Gene Mutations in Lung Adenocarcinomas
Pan, Q., Pao, W. J., & Ladanyi, M. (2005) · Journal of Molecular Diagnostics · doi:10.1016/s1525-1578(10)60569-7 · Cited by 245 · see citing works
Suitability of Endobronchial Ultrasound-guided Transbronchial Needle Aspiration Specimens for Subtyping and Genotyping of Non–Small Cell Lung Cancer: A Multicenter Study of 774 Patients
Navani, N., Brown, J., Nankivell, M. G., Woolhouse, I., Harrison, R. N., Jeebun, V., Munavvar, M., Ng, B., Rassl, D. M., Falzon, M., et al. (2012) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201202-0294oc · Cited by 240 · see citing works
Suitability of Thoracic Cytology for New Therapeutic Paradigms in Non-small Cell Lung Carcinoma: High Accuracy of Tumor Subtyping and Feasibility of EGFR and KRAS Molecular Testing
Rekhtman, N., Brandt, S. M., Sigel, C., Friedlander, M. A., Riely, G. J., Travis, W. D., Zakowski, M. F., & Moreira, A. L. (2011) · Journal of Thoracic Oncology · doi:10.1097/jto.0b013e31820517a3 · Cited by 236 · see citing works
Epidermal growth factor receptor activating mutations in Spanish gefitinib-treated non-small-cell lung cancer patients
Cortés-Funes, H., Gómez, C. G., Rosell, R., Valero, P. M., Girón, C. G., Velasco, A., Izquierdo, Á., Díz, P., Camps, C., Castellanos, D., et al. (2005) · Annals of Oncology · doi:10.1093/annonc/mdi221 · Cited by 229 · see citing works
A rapid and sensitive enzymatic method for epidermal growth factor receptor mutation screening
Jänne, P. A., Borras, A. M., Kuang, Y., Rogers, A. M., Joshi, V. A., Liyanage, H., Lindeman, N., Lee, J. C., Halmos, B., Maher, E. A., et al. (2006) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-05-2047 · Cited by 214 · see citing works
High resolution melting analysis for rapid and sensitive EGFR and KRAS mutation detection in formalin fixed paraffin embedded biopsies
Do, H., Krypuy, M., Mitchell, P. L. R., Fox, S. B., & Dobrovic, A. (2008) · BMC Cancer · doi:10.1186/1471-2407-8-142 · Cited by 206 · see citing works
Assessment of EGFR Mutation Status in Lung Adenocarcinoma by Immunohistochemistry Using Antibodies Specific to the Two Major Forms of Mutant EGFR
Brevet, M., Arcila, M. E., & Ladanyi, M. (2010) · Journal of Molecular Diagnostics · doi:10.2353/jmoldx.2010.090140 · Cited by 205 · see citing works
Assessment of Epidermal Growth Factor Receptor Mutation by Endobronchial Ultrasound-Guided Transbronchial Needle Aspiration
Nakajima, T., Yasufuku, K., Suzuki, M., Hiroshima, K., Kubo, R., Mohammed, S., Miyagi, Y., Matsukuma, S., Sekine, Y., & Fujisawa, T. (2007) · CHEST Journal · doi:10.1378/chest.07-0095 · Cited by 198 · see citing works
Detection ofEGFRGene Mutation in Lung Cancer by Mutant-Enriched Polymerase Chain Reaction Assay
Asano, H., Toyooka, S., Tokumo, M., Ichimura, K., Aoe, K., Ito, S., Tsukuda, K., Ouchida, M., Aoe, M., Katayama, H., et al. (2006) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-05-0934 · Cited by 188 · see citing works
A Rapid, Sensitive Assay to Detect EGFR Mutation in Small Biopsy Specimens from Lung Cancer
Yatabe, Y., Hida, T., Horio, Y., Kosaka, T., Takahashi, T., & Mitsudomi, T. (2006) · Journal of Molecular Diagnostics · doi:10.2353/jmoldx.2006.050104 · Cited by 186 · see citing works
Rapid KRAS, EGFR, BRAF and PIK3CA Mutation Analysis of Fine Needle Aspirates from Non-Small-Cell Lung Cancer Using Allele-Specific qPCR
van Eijk, R., Licht, J., Schrumpf, M., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017791 · Cited by 181 · see citing works
A platform for rapid detection of multiple oncogenic mutations with relevance to targeted therapy in non-small-cell lung cancer.
Su, Z., Dias-Santagata, D., Duke, M., Hutchinson, K., Lin, Y.-L., Borger, D. R., Chung, C. H., Massion, P. P., Vnencak-Jones, C. L., Iafrate, A. J., et al. (2011) · The Journal of Molecular Diagnostics · doi:10.1016/j.jmoldx.2010.11.010 · Cited by 176 · see citing works
Prospective Validation for Prediction of Gefitinib Sensitivity by Epidermal Growth Factor Receptor Gene Mutation in Patients with Non-Small Cell Lung Cancer
Yoshida, K., Yatabe, Y., Park, J. Y., Shimizu, J., Horio, Y., Matsuo, K., Kosaka, T., Mitsudomi, T., & Hida, T. (2007) · Journal of Thoracic Oncology · doi:10.1016/s1556-0864(15)30013-7 · Cited by 165 · see citing works
A comparison of ARMS and DNA sequencing for mutation analysis in clinical biopsy samples
Ellison, G., Donald, E. L., McWalter, G., et al. (2010) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/1756-9966-29-132 · Cited by 153 · see citing works
Self-citation
Epidermal growth factor receptor gene mutation in non-small cell lung cancer using highly sensitive and fast TaqMan PCR assay
Endo, K., Konishi, A., Sasaki, H., et al. (2005) · Lung Cancer · doi:10.1016/j.lungcan.2005.08.009 · Cited by 152 · see citing works
EGFR mutation status in tumour-derived DNA from pleural effusion fluid is a practical basis for predicting the response to gefitinib
Kimura, H., Fujiwara, Y., Sone, T., et al. (2006) · British Journal of Cancer · doi:10.1038/sj.bjc.6603428 · Cited by 126 · see citing works
High sensitivity detection of epidermal growth factor receptor mutations in the pleural effusion of non‐small cell lung cancer patients
Kimura, H., Fujiwara, Y., Sone, T., Kunitoh, H., Tamura, T., Kasahara, K., & Nishio, K. (2006) · Cancer Science · doi:10.1111/j.1349-7006.2006.00216.x · Cited by 125 · see citing works
EGFR and KRAS mutations in lung carcinomas in the Dutch population: increased EGFR mutation frequency in malignant pleural effusion of lung adenocarcinoma
Smits, A. J. J., Kummer, J. A., Hinrichs, J. W. J., et al. (2012) · Cellular Oncology · doi:10.1007/s13402-012-0078-4 · Cited by 119 · see citing works
Novel Epidermal Growth Factor Receptor Mutation-Specific Antibodies for Non-small Cell Lung Cancer: Immunohistochemistry as a Possible Screening Method for Epidermal Growth Factor Receptor Mutations
Kato, Y., Peled, N., Wynes, M. W., Yoshida, K., Pardo, M., Mascaux, C., Ohira, T., Tsuboi, M., Matsubayashi, J., Nagao, T., et al. (2010) · Journal of Thoracic Oncology · doi:10.1097/jto.0b013e3181e9da60 · Cited by 118 · see citing works
Multigene Mutation Analysis of Metastatic Lymph Nodes in Non-small Cell Lung Cancer Diagnosed by Endobronchial Ultrasound-Guided Transbronchial Needle Aspiration
Nakajima, T., Yasufuku, K., Nakagawara, A., Kimura, H., & Yoshino, I. (2011) · CHEST Journal · doi:10.1378/chest.10-3186 · Cited by 117 · see citing works
Benchmarking of Mutation Diagnostics in Clinical Lung Cancer Specimens
Querings, S., Altmüller, J., Ansén, S., Zander, T., Seidel, D., Gabler, F., Peifer, M., Markert, E., STEMSHORN, K. C., Timmermann, B., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019601 · Cited by 115 · see citing works
EGFR gene status in cytological samples of nonsmall cell lung carcinoma
Santos, G. D. C., Saieg, M. A., Geddie, W. R., & Leighl, N. B. (2011) · Cancer Cytopathology · doi:10.1002/cncy.20150 · Cited by 114 · see citing works
A Multicenter Blinded Study to Evaluate KRAS Mutation Testing Methodologies in the Clinical Setting
Whitehall, V., Tran, K. L., Umapathy, A., Grieu, F., Hewitt, C., Evans, T., Ismail, T., Li, W. Q., Collins, P., Ravetto, P. F., et al. (2009) · Journal of Molecular Diagnostics · doi:10.2353/jmoldx.2009.090057 · Cited by 113 · see citing works
A Sensitive Method for Detecting EGFR Mutations in Non-small Cell Lung Cancer Samples with Few Tumor Cells
Molina‐Vila, M. Á., Bertrán-Alamillo, J., Reguart, N., Tarón, M., Castellà, E., Llatjós, M., Costa, C., Mayo, C., Pradas, A., Queralt, C., et al. (2008) · Journal of Thoracic Oncology · doi:10.1097/jto.0b013e318189f579 · Cited by 112 · see citing works
A Brief Retrospective Report on the Feasibility of Epidermal Growth Factor Receptor and KRAS Mutation Analysis in Transesophageal Ultrasound- and Endobronchial Ultrasound-Guided Fine Needle Cytological Aspirates
Schuurbiers, O. C. J., Looijen-Salamon, M. G., Ligtenberg, M. J. L., & van der Heijden, E. H. F. M. (2010) · Journal of Thoracic Oncology · doi:10.1097/jto.0b013e3181f0bd93 · Cited by 111 · see citing works
Prospective Validation for Prediction of Gefitinib Sensitivity by Epidermal Growth Factor Receptor Gene Mutation in Patients with Non-Small Cell Lung Cancer
Yoshida, K., Yatabe, Y., Park, J. Y., et al. (2007) · Journal of Thoracic Oncology · doi:10.1097/01243894-200701000-00006 · Cited by 109 · see citing works
Usefulness of EGFR mutation screening in pleural fluid to predict the clinical outcome of gefitinib treated patients with lung cancer
Soh, J., Toyooka, S., Aoe, K., Asano, H., Ichihara, S., Katayama, H., Hiraki, A., Kiura, K., Aoe, M., Sano, Y., et al. (2006) · International Journal of Cancer · doi:10.1002/ijc.22190 · Cited by 105 · see citing works
An evaluation study of EGFR mutation tests utilized for non-small-cell lung cancer in the diagnostic setting
Goto, K., Satouchi, M., Ishii, G., Nishio, K., Hagiwara, K., Mitsudomi, T., Whiteley, J. L., Donald, E. L., McCormack, R., & Todo, T. (2012) · Annals of Oncology · doi:10.1093/annonc/mds121 · Cited by 103 · see citing works
Self-citation
Epidermal Growth Factor Receptor Mutation Detection Using High-Resolution Melting Analysis Predicts Outcomes in Patients with Advanced Non–Small Cell Lung Cancer Treated with Gefitinib
Takano, T., Ohe, Y., Tsuta, K., Fukui, T., Sakamoto, H., Yoshida, T., Tateishi, U., Nokihara, H., Yamamoto, N., Sekine, I., et al. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-0627 · Cited by 103 · see citing works
Quantitative Analysis of Tumor in Bronchial Biopsy Specimens
Coghlin, C., Smith, L. J., Bakar, S., et al. (2010) · Journal of Thoracic Oncology · doi:10.1097/jto.0b013e3181ca12c4 · Cited by 100 · see citing works
Detection of Epidermal Growth Factor Receptor Mutation in Transbronchial Needle Aspirates of Non-Small Cell Lung Cancer
Horiike, A., Kimura, H., Nishio, K., et al. (2007) · CHEST Journal · doi:10.1378/chest.06-1673 · Cited by 99 · see citing works
Comprehensive epidermal growth factor receptor gene analysis from cytological specimens of non-small-cell lung cancers
Savić, S., Tapia, C., Grilli, B., et al. (2007) · British Journal of Cancer · doi:10.1038/sj.bjc.6604142 · Cited by 99 · see citing works
Screening for EGFR and KRAS Mutations in Endobronchial Ultrasound Derived Transbronchial Needle Aspirates in Non-Small Cell Lung Cancer Using COLD-PCR
Santis, G., Angell, R., Nickless, G., Quinn, A., Herbert, A., Cane, P., Spicer, J. F., Breen, R. A. M., McLean, E., & Tobal, K. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025191 · Cited by 98 · see citing works
Detection of EGFR mutations with mutation-specific antibodies in stage IV non-small-cell lung cancer
Simonetti, S., Molina‐Vila, M. Á., Queralt, C., de Aguirre, I., Mayo, C., Bertrán-Alamillo, J., Sánchez, J. J., González-Larriba, J. L., Jiménez, U., Isla, D., et al. (2010) · Journal of Translational Medicine · doi:10.1186/1479-5876-8-135 · Cited by 95 · see citing works
Rapid Detection of Epidermal Growth Factor Receptor Mutations in Lung Cancer by the SMart-Amplification Process
Hoshi, K., Takakura, H., Mitani, Y., Tatsumi, K., Momiyama, N., Ichikawa, Y., Togo, S., Miyagi, T., Kawai, Y., Kogo, Y., et al. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-0509 · Cited by 90 · see citing works
Clinical pharmacogenomic testing of KRAS, BRAF and EGFRmutations by high resolution melting analysis and ultra-deep pyrosequencing
Borràs, E., Jurado, I., Hernán, I., Gamundi, M. J., Dias, M. M. D. S., Martí, I., Mañé, B., Arcusa, À., Agúndez, J. A. G., Blanca, M., et al. (2011) · BMC Cancer · doi:10.1186/1471-2407-11-406 · Cited by 88 · see citing works
The Application of Molecular Diagnostic Studies Interrogating EGFR and KRAS Mutations to Stained Cytologic Smears of Lung Carcinoma
Betz, B. L., Roh, M. H., Weigelin, H. C., Placido, J. B., Schmidt, L. A., Farmen, S., Arenberg, D. A., Kalemkerian, G. P., & Knoepp, S. M. (2011) · American Journal of Clinical Pathology · doi:10.1309/ajcp84tutqosuong · Cited by 85 · see citing works
EGFR mutation detection in NSCLC—assessment of diagnostic application and recommendations of the German Panel for Mutation Testing in NSCLC
Penzel, R., Sers, C., Chen, Y., Lehmann-Mühlenhoff, U., Merkelbach‐Bruse, S., Jung, A., Kirchner, T., Büttner, R., Kreipe, H. H., Petersen, I., et al. (2010) · Archiv für Pathologische Anatomie und Physiologie und für Klinische Medicin · doi:10.1007/s00428-010-1000-y · Cited by 85 · see citing works
Pyrosequencing, a method approved to detect the two major EGFR mutations for anti EGFR therapy in NSCLC
Dufort, S., Richard, M., Lantuéjoul, S., & de Fraipont, F. (2011) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/1756-9966-30-57 · Cited by 84 · see citing works
Detection of EGFR Mutation Status in Lung Adenocarcinoma Specimens with Different Proportions of Tumor Cells Using Two Methods of Differential Sensitivity
Han, H., Lim, S.-N., An, J. Y., et al. (2011) · Journal of Thoracic Oncology · doi:10.1097/jto.0b013e31823c4c1b · Cited by 78 · see citing works
Using Whole Genome Amplification (WGA) of Low-Volume Biopsies to Assess the Prognostic Role of EGFR, KRAS, p53, and CMET Mutations in Advanced-Stage Non-small Cell Lung Cancer (NSCLC)
Lim, E. H., Zhang, S.-L., Li, J., Yap, W. S., Howe, T.-C., Tan, B. P., Lee, Y.-S., Wong, D., Khoo, K., Seto, K., et al. (2009) · Journal of Thoracic Oncology · doi:10.1097/jto.0b013e3181913e28 · Cited by 76 · see citing works
EGFR and KRAS mutations detection on lung cancer liquid-based cytology: a pilot study
Malapelle, U., Rosa, N. D., Rocco, D., et al. (2011) · Journal of Clinical Pathology · doi:10.1136/jclinpath-2011-200296 · Cited by 76 · see citing works
EGFR and KRAS mutation analysis in cytologic samples of lung adenocarcinoma enabled by laser capture microdissection
Roy‐Chowdhuri, S., Xi, L., Pham, T. H.-T., Hanson, J. C., Rodriguez‐Canales, J., Berman, A. W., Rajan, A., Giaccone, G., Emmert‐Buck, M. R., Raffeld, M. A., et al. (2011) · Modern Pathology · doi:10.1038/modpathol.2011.184 · Cited by 74 · see citing works
Assessment of Epidermal Growth Factor Receptor and K-Ras Mutation Status in Cytological Stained Smears of Non-Small Cell Lung Cancer Patients: Correlation with Clinical Outcomes
Lozano, M. D., Zulueta, J. J., Echeveste, J. I., Gúrpide, A., Seijo, L. M., Martín‐Algarra, S., del Barrio, A., Pı́o, R., Idoate, M. A., Labiano, T., et al. (2011) · The Oncologist · doi:10.1634/theoncologist.2010-0155 · Cited by 74 · see citing works
Detection of EGFR and KRAS mutations on trans-thoracic needle aspiration of lung nodules by high resolution melting analysis
Fassina, A., Gazziero, A., Zardo, D., Corradin, M., Aldighieri, E., & Rossi, G. P. (2009) · Journal of Clinical Pathology · doi:10.1136/jcp.2009.067587 · Cited by 72 · see citing works
Mutations in the tyrosine kinase domain of the EGFR gene associated with gefitinib response in non-small-cell lung cancer
Rosell, R., Ichinose, Y., Tarón, M., Sarries, C., Queralt, C., Méndez, P., Sánchez, J. M., Nishiyama, K., Morán, T., Cirauqui, B., et al. (2005) · Lung Cancer · doi:10.1016/j.lungcan.2005.05.017 · Cited by 71 · see citing works
Identification of non-small-cell lung cancer with activating EGFR mutations in malignant effusion and cerebrospinal fluid: Rapid and sensitive detection of exon 19 deletion E746-A750 and exon 21 L858R mutation by immunocytochemistry
Kawahara, A., Azuma, K., Sumi, A., Taira, T., Nakashima, K., Aikawa, E., Abe, H., Yamaguchi, T., Takamori, S., Akiba, J., et al. (2011) · Lung Cancer · doi:10.1016/j.lungcan.2011.02.002 · Cited by 70 · see citing works
Detection and comparison of epidermal growth factor receptor mutations in cells and fluid of malignant pleural effusion in non-small cell lung cancer
Zhang, X., Zhao, Y., Wang, M., et al. (2007) · Lung Cancer · doi:10.1016/j.lungcan.2007.10.011 · Cited by 69 · see citing works
The usefulness of mutation-specific antibodies in detecting epidermal growth factor receptor mutations and in predicting response to tyrosine kinase inhibitor therapy in lung adenocarcinoma
Kozu, Y., Tsuta, K., Kohno, T., et al. (2010) · Lung Cancer · doi:10.1016/j.lungcan.2010.11.003 · Cited by 67 · see citing works
The usefulness of mutation-specific antibodies in detecting epidermal growth factor receptor mutations and in predicting response to tyrosine kinase inhibitor therapy in lung adenocarcinoma
吉基, 神. (2011) · Medical Entomology and Zoology · Cited by 63 · see citing works
Evaluation of EGFR mutation status in cytology specimens: An institutional experience
Aisner, D. L., Deshpande, C. G., Baloch, Z. W., et al. (2011) · Diagnostic Cytopathology · doi:10.1002/dc.21851 · Cited by 61 · see citing works
Cross-Validation Study for Epidermal Growth Factor Receptor and KRAS Mutation Detection in 74 Blinded Non-small Cell Lung Carcinoma Samples: A Total of 5550 Exons Sequenced by 15 Molecular French Laboratories (Evaluation of the EGFR Mutation Status for the Administration of EGFR-TKIs in Non-Small Cell Lung Carcinoma [ERMETIC] Project—Part 1)
Beau‐Faller, M., Degeorges, A., Rolland, E., Mounawar, M., Antoine, M., Poulot, V., Mauguen, A., Barbu, V. D., Coulet, F., Prétet, J., et al. (2011) · Journal of Thoracic Oncology · doi:10.1097/jto.0b013e318211dcee · Cited by 56 · see citing works
The PCR-invader method (structure-specific 5′ nuclease-based method), a sensitive method for detecting EGFR gene mutations in lung cancer specimens; comparison with direct sequencing
Naoki, K., Soejima, K., Okamoto, H., Hamamoto, J., Hida, N., Nakachi, I., Yasuda, H., Nakayama, S., Yoda, S., Satomi, R., et al. (2011) · International Journal of Clinical Oncology · doi:10.1007/s10147-011-0187-5 · Cited by 54 · see citing works
Novel heteroduplex method using small cytology specimens with a remarkably high success rate for analysing EGFR gene mutations with a significant correlation to gefitinib efficacy in non-small-cell lung cancer
Oshita, F., Matsukuma, S., Yoshihara, M., Sakuma, Y., Ohgane, N., Kameda, Y., Saito, H., Yamada, K., Tsuchiya, E., & Miyagi, Y. (2006) · British Journal of Cancer · doi:10.1038/sj.bjc.6603396 · Cited by 52 · see citing works
An Alternative Method for Screening EGFR Mutation Using RFLP in Non-small Cell Lung Cancer Patients
Kawada, I., Soejima, K., Watanabe, H., et al. (2008) · Journal of Thoracic Oncology · doi:10.1097/jto.0b013e318186fadd · Cited by 49 · see citing works
RNA is favourable for analysingEGFRmutations in malignant pleural effusion of lung cancer
Tsai, T.-H., Su, K., Wu, S., Chang, Y., Luo, S., Jan, I., Yu, C., Yu, S.-L., Shih, J.-Y., & Yang, P. (2011) · European Respiratory Journal · doi:10.1183/09031936.00043511 · Cited by 49 · see citing works
Usefulness of tissue microarrays for assessment of protein expression, gene copy number and mutational status of EGFR in lung adenocarcinoma
Ilié, M., Hofman, V., Bonnetaud, C., Havet, K., Lespinet‐Fabre, V., Coëlle, C., Tanga, V., Vénissac, N., Mouroux, J., & Hofman, P. M. (2010) · Archiv für Pathologische Anatomie und Physiologie und für Klinische Medicin · doi:10.1007/s00428-010-0963-z · Cited by 48 · see citing works
Detection of gene point mutation in paraffin sections using in situ loop‐mediated isothermal amplification
Ikeda, S., 高部, 和., Inagaki, M., et al. (2007) · Pathology International · doi:10.1111/j.1440-1827.2007.02144.x · Cited by 47 · see citing works
Mutation Detection of Epidermal Growth Factor Receptor and KRAS Genes Using the Smart Amplification Process Version 2 from Formalin-Fixed, Paraffin-Embedded Lung Cancer Tissue
Miyamae, Y., Shimizu, K., Mitani, Y., Araki, T., Kawai, Y., Baba, M., Kakegawa, S., Sugano, M., Kaira, K., Lezhava, A., et al. (2010) · Journal of Molecular Diagnostics · doi:10.2353/jmoldx.2010.090105 · Cited by 43 · see citing works
Detection of EGFR Gene Mutations Using the Wash Fluid of CT-Guided Biopsy Needle in NSCLC Patients
Otani, H., Toyooka, S., Soh, J., et al. (2008) · Journal of Thoracic Oncology · doi:10.1097/jto.0b013e31816de2cd · Cited by 41 · see citing works
Recommendations for mutational analysis of EGFR in lung carcinoma.
Marchetti, A., Normanno, N., Pinto, C., et al. (2010) · PubMed · Cited by 37 · see citing works
Effusion Immunocytochemistry as an Alternative Approach for the Selection of First-Line Targeted Therapy in Advanced Lung Adenocarcinoma
Tsai, T.-H., Wu, S., Chang, Y., et al. (2012) · Journal of Thoracic Oncology · doi:10.1097/jto.0b013e31824cc46b · Cited by 36 · see citing works
Immunohistochemical detection of mutated epidermal growth factor receptors in pulmonary adenocarcinoma.
Nakamura, H., Mochizuki, A., Shinmyo, T., et al. (2010) · PubMed · Cited by 34 · see citing works
A Simple and Sensitive Method for Detecting Major Mutations Within the Tyrosine Kinase Domain of the Epidermal Growth Factor Receptor Gene in Non???small-cell Lung Carcinoma
Ohnishi, H., Ohtsuka, K., Ooide, A., Matsushima, S., Goya, T., & Watanabe, T. (2006) · Diagnostic Molecular Pathology · doi:10.1097/00019606-200606000-00007 · Cited by 29 · see citing works
Simple and Sensitive Method for Detecting Point Mutations of Epidermal Growth Factor Receptor Using Cationic Conjugated Polymers
Yang, Q., Qiu, T., Wu, W., et al. (2011) · ACS Applied Materials & Interfaces · doi:10.1021/am201248y · Cited by 25 · see citing works
Mutation profile of EGFR gene detected by denaturing high-performance liquid chromatography in Japanese lung cancer patients
Sueoka, N., Sato, A., Eguchi, H., Komiya, K., Sakuragi, T., Mitsuoka, M., Satoh, T., Hayashi, S., Nakachi, K., & Sueoka, E. (2006) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-006-0144-2 · Cited by 24 · see citing works
Use of CT-guided fine needle aspiration biopsy in epidermal growth factor receptor mutation analysis in patients with advanced lung cancer
Zhuang, Y., Wang, H., Shi, M., et al. (2011) · Acta Radiologica · doi:10.1258/ar.2011.110150 · Cited by 19 · see citing works
Bronchoscopic Microsampling is a Useful Complementary Diagnostic Tool for Detecting Lung Cancer
Yasuda, H., Soejima, K., Nakayama, S., et al. (2010) · Lung Cancer · doi:10.1016/j.lungcan.2010.07.016 · Cited by 18 · see citing works
A novel method for detection of mutation in epidermal growth factor receptor
Zhao, J., Zhao, J., Huang, J., et al. (2011) · Lung Cancer · doi:10.1016/j.lungcan.2011.02.015 · Cited by 16 · see citing works
Rapid and Efficient Detection of EGFR Mutations in Problematic Cytologic Specimens by High-Resolution Melting Analysis
Hlinkova, K., Babál, P., Berzinec, P., Majer, I., & Ilenčíková, D. (2011) · Molecular Diagnosis & Therapy · doi:10.1007/bf03257190 · Cited by 15 · see citing works
Clinical screening assay for EGFR exon 19 mutations using PNA-clamp smart amplification process version 2 in lung adenocarcinoma
Araki, T. (2011) · Oncology Reports · doi:10.3892/or.2011.1391 · Cited by 14 · see citing works
Direct sequencing in cytological specimens as a useful strategy for detecting EGFR mutations in non-small cell lung cancer patients
Cho, M.-C., Choi, C., Kim, S., et al. (2011) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm.2011.704 · Cited by 8 · see citing works

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[57]Navani N Brown JM Nankivell M Suitability of EBUS-TBNA specimens for subtyping and genotyping of NSCLC: a multi-centre study of 774 patients. Am J Respir Crit Care Med 2012; 185: 1316– 22 22505743 PMC3378660

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Endo, K., Sasaki, H., Yano, M., Kobayashi, Y., Yukiue, H., Haneda, H., Suzuki, E., Kawano, O., & Fujii, Y. (2006) · Oncology Reports · doi:10.3892/or.16.3.533 · Cited by 37 · see citing works
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Authors: Ellison, G., Zhu, G., Moulis, A., Dearden, S., Speake, G., & McCormack, R.
Affiliations: AstraZeneca (United Kingdom) (GB)
AstraZeneca R&D, Shanghai, China
AstraZeneca SA Hellas, Athens, Greece
Corresponding author: Ellison, Gillian
ORCID: Dearden, Simon
Venue: Journal of Clinical Pathology
Publisher: BMJ
Published: 2012-11-21
Volume: 66
Issue: 2
Pages: 79-89
ISSN: 0021-9746 (ISSN-L)
1472-4146
DOI: 10.1136/jclinpath-2012-201194
PMC: PMC3582044
OpenAlex: W2158667695
Cited by: 301
References: 93
Citations by year: 2026: 6 · 2025: 11 · 2024: 8 · 2023: 9 · 2022: 17 · 2021: 19 · 2020: 26 · 2019: 22 · 2018: 25 · 2017: 38 · 2016: 26 · 2015: 39 · 2014: 29 · 2013: 26
FWCI: 24.25
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc
Locations: Journal of Clinical Pathology (publishedVersion, cc-by-nc)
Europe PMC (PubMed Central) (publishedVersion, other-oa)
PubMed Central (publishedVersion, cc-by-nc)
PubMed (publishedVersion)
Funders: AstraZeneca
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: EGFR mutation testing, non-small cell lung cancer, EGFR tyrosine kinase inhibitors, gefitinib, fine needle aspirate, pleural effusion, uncommon EGFR mutations, direct DNA sequencing
MeSH terms: Antineoplastic Agents, Biopsy, Needle, Carcinoma, Non-Small-Cell Lung, Cytodiagnosis, DNA Mutational Analysis, Humans, Lung Neoplasms, Mutation, Pleural Effusion, Predictive Value of Tests, Reagent Kits, Diagnostic, Sensitivity and Specificity, Specimen Handling, Patient Selection, Microdissection, Protein Kinase Inhibitors, Precision Medicine, ErbB Receptors

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EGFR mutation testing in lung cancer: a review of available methods and their use for analysis of tumour tissue and cytology samples

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