Circulating DNA in diagnosis and monitoring EGFR gene mutations in advanced non-small cell lung cancer

Translational Lung Cancer Research

Volumn 4, Issue 5, 2015, Pages 584-597

  Bordi, Paola ^a   Del Re, Marzia ^b   Danesi, Romano ^b   Tiseo, Marcello ^a  

^a UNIVERSITY HOSPITAL OF PARMA   (Italy)

^b UNIVERSITY OF PISA   (Italy)

Author keywords

Circulating DNA; Epidermal growth factor receptor (EGFR); Non small cell lung cancer (NSCLC); Tyrosine kinase inhibitor (TKI) resistance

Indexed keywords

CIRCULATING CELL FREE TUMOR DNA; CIRCULATING DNA; DNA; DNA FRAGMENT; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; TUMOR MARKER; UNCLASSIFIED DRUG;

ADVANCED CANCER; CLINICAL TRIAL (TOPIC); EGFR GENE; FEASIBILITY STUDY; GENE MUTATION; GENOTYPE; HUMAN; LUNG BIOPSY; MASS SPECTROMETRY; MUTATIONAL ANALYSIS; NEXT GENERATION SEQUENCING; NON INVASIVE PROCEDURE; NON SMALL CELL LUNG CANCER; ONCOGENE; POLYMERASE CHAIN REACTION; REAL TIME POLYMERASE CHAIN REACTION; REVIEW; SENSITIVITY AND SPECIFICITY;

EID: 84960119237     PISSN: 22186751     EISSN: 22264477     Source Type: Journal    
DOI: 10.3978/j.issn.2218-6751.2015.08.09     Document Type: Review

References (92)

1. Brahmer J, Reckamp KL, Baas P, et al. Nivolumab versus Docetaxel in Advanced Squamous-Cell Non-Small-Cell Lung Cancer. N Engl J Med 2015;373:123-35.
2. Reck M, Popat S, Reinmuth N, et al. Metastatic non-small-cell lung cancer (NSCLC): ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2014;25 Suppl 3:iii27-39.
3. Chan BA, Hughes BG. Targeted therapy for non-small cell lung cancer: current standards and the promise of the future. Transl Lung Cancer Res 2015;4:36-54.
4. Mok TS, Wu YL, Thongprasert S, et al. Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med 2009;361:947-57.
5. Rosell R, Carcereny E, Gervais R, et al. 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. Lancet Oncol 2012;13:239-46.
6. Solomon BJ, Mok T, Kim DW, et al. First-line crizotinib versus chemotherapy in ALK-positive lung cancer. N Engl J Med 2014;371:2167-77.
7. Salomon DS, Brandt R, Ciardiello F, et al. Epidermal growth factor-related peptides and their receptors in human malignancies. Crit Rev Oncol Hematol 1995;19:183-232.
8. Zhang X, Gureasko J, Shen K, et al. An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor. Cell 2006;125:1137-49.
9. Shigematsu H, Lin L, Takahashi T, et al. Clinical and biological features associated with epidermal growth factor receptor gene mutations in lung cancers. J Natl Cancer Inst 2005;97:339-46.
10. Yang JC, Wu YL, Schuler M, et al. Afatinib versus cisplatin-based chemotherapy for EGFR mutation-positive lung adenocarcinoma (LUX-Lung 3 and LUX-Lung 6): analysis of overall survival data from two randomised, phase 3 trials. Lancet Oncol 2015;16:141-51.
11. Vanderlaan PA, Yamaguchi N, Folch E, et al. Success and failure rates of tumor genotyping techniques in routine pathological samples with non-small-cell lung cancer. Lung Cancer 2014;84:39-44.
12. Singh VM, Salunga RC, Huang VJ, et al. Analysis of the effect of various decalcification agents on the quantity and quality of nucleic acid (DNA and RNA) recovered from bone biopsies. Ann Diagn Pathol 2013;17:322-6.
13. Diaz LA Jr, Bardelli A. Liquid biopsies: genotyping circulating tumor DNA. J Clin Oncol 2014;32:579-86.
14. Gerlinger M, Rowan AJ, Horswell S, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 2012;366:883-92.
15. Vogelstein B, Papadopoulos N, Velculescu VE, et al. Cancer genome landscapes. Science 2013;339:1546-58.
16. Overman MJ, Modak J, Kopetz S, et al. Use of research biopsies in clinical trials: are risks and benefits adequately discussed? J Clin Oncol 2013;31:17-22.
17. Jänne PA, Yang JC, Kim DW, et al. AZD9291 in EGFR inhibitor-resistant non-small-cell lung cancer. N Engl J Med 2015;372:1689-99.
18. Sequist LV, Soria JC, Goldman JW, et al. Rociletinib in EGFR-mutated non-small-cell lung cancer. N Engl J Med 2015;372:1700-9.
19. Ruibal Morell A. CEA serum levels in non-neoplastic disease. Int J Biol Markers 1992;7:160-6.
20. Ilie M, Hofman V, Long E, et al. Current challenges for detection of circulating tumor cells and cell-free circulating nucleic acids, and their characterization in non-small cell lung carcinoma patients. What is the best blood substrate for personalized medicine? Ann Transl Med 2014;2:107.
21. Bettegowda C, Sausen M, Leary RJ, et al. Detection of circulating tumor DNA in early- and late-stage human malignancies. Sci Transl Med 2014;6:224ra24.
22. Mandel P, Metais P. Les acides nucléiques du plasma sanguin chez l'homme. C R Seances Soc Biol Fil 1948;142:241-3.
23. Punnoose EA, Atwal S, Liu W, et al. Evaluation of circulating tumor cells and circulating tumor DNA in non-small cell lung cancer: association with clinical endpoints in a phase II clinical trial of pertuzumab and erlotinib. Clin Cancer Res 2012;18:2391-401.
24. Frattini M, Gallino G, Signoroni S, et al. Quantitative and qualitative characterization of plasma DNA identifies primary and recurrent colorectal cancer. Cancer Lett 2008;263:170-81.
25. Dawson SJ, Tsui DW, Murtaza M, et al. Analysis of circulating tumor DNA to monitor metastatic breast cancer. N Engl J Med 2013;368:1199-209.
26. Yung TK, Chan KC, Mok TS, et al. Single-molecule detection of epidermal growth factor receptor mutations in plasma by microfluidics digital PCR in non-small cell lung cancer patients. Clin Cancer Res 2009;15:2076-84.
27. Forshew T, Murtaza M, Parkinson C, et al. Noninvasive identification and monitoring of cancer mutations by targeted deep sequencing of plasma DNA. Sci Transl Med 2012;4:136ra68.
28. Lee YJ, Yoon KA, Han JY, et al. Circulating cell-free DNA in plasma of never smokers with advanced lung adenocarcinoma receiving gefitinib or standard chemotherapy as first-line therapy. Clin Cancer Res 2011;17:5179-87.
29. Misale S, Yaeger R, Hobor S, et al. Emergence of KRAS mutations and acquired resistance to anti-EGFR therapy in colorectal cancer. Nature 2012;486:532-6.
30. Liu P, Liang H, Xue L, et al. Potential clinical significance of plasma-based KRAS mutation analysis using the COLD-PCR/TaqMan(®) -MGB probe genotyping method. Exp Ther Med 2012;4:109-112.
31. Li J, Wang L, Mamon H, et al. Replacing PCR with COLD-PCR enriches variant DNA sequences and redefines the sensitivity of genetic testing. Nat Med 2008;14:579-84.
32. Wilkening S, Hemminki K, Thirumaran RK, et al. Determination of allele frequency in pooled DNA: comparison of three PCR-based methods. Biotechniques 2005;39:853-8.
33. Goto K, Ichinose Y, Ohe Y, et al. Epidermal growth factor receptor mutation status in circulating free DNA in serum: from IPASS, a phase III study of gefitinib or carboplatin/paclitaxel in non-small cell lung cancer. J Thorac Oncol 2012;7:115-21.
34. Hindson BJ, Ness KD, Masquelier DA, et al. High-throughput droplet digital PCR system for absolute quantitation of DNA copy number. Anal Chem 2011;83:8604-10.
35. Diehl F, Li M, Dressman D, et al. Detection and quantification of mutations in the plasma of patients with colorectal tumors. Proc Natl Acad Sci U S A 2005;102:16368-73.
36. Murtaza M, Dawson SJ, Tsui DW, et al. Non-invasive analysis of acquired resistance to cancer therapy by sequencing of plasma DNA. Nature 2013;497:108-12.
37. Kimura H, Kasahara K, Kawaishi M, et al. Detection of epidermal growth factor receptor mutations in serum as a predictor of the response to gefitinib in patients with non-small-cell lung cancer. Clin Cancer Res 2006;12:3915-21.
38. Kimura H, Suminoe M, Kasahara K, et al. Evaluation of epidermal growth factor receptor mutation status in serum DNA as a predictor of response to gefitinib (IRESSA). Br J Cancer 2007;97:778-84.
39. Zhao X, Han RB, Zhao J, et al. Comparison of epidermal growth factor receptor mutation statuses in tissue and plasma in stage I-IV non-small cell lung cancer patients. Respiration 2013;85:119-25.
40. Tseng JS, Yang TY, Tsai CR, et al. Dynamic plasma EGFR mutation status as a predictor of EGFR-TKI efficacy in patients with EGFR-mutant lung adenocarcinoma. J Thorac Oncol 2015;10:603-10.
41. Weber B, Meldgaard P, Hager H, et al. Detection of EGFR mutations in plasma and biopsies from non-small cell lung cancer patients by allele-specific PCR assays. BMC Cancer 2014;14:294.
42. Douillard JY, Ostoros G, Cobo M, et al. Gefitinib treatment in EGFR mutated caucasian NSCLC: circulating-free tumor DNA as a surrogate for determination of EGFR status. J Thorac Oncol 2014;9:1345-53.
43. Mok T, Wu YL, Lee JS, et al. Detection and Dynamic Changes of EGFR Mutations from Circulating Tumor DNA as a Predictor of Survival Outcomes in NSCLC Patients Treated with First-line Intercalated Erlotinib and Chemotherapy. Clin Cancer Res 2015;21:3196-203.
44. Luo J, Shen L, Zheng D. Diagnostic value of circulating free DNA for the detection of EGFR mutation status in NSCLC: a systematic review and meta-analysis. Sci Rep 2014;4:6269.
45. Qiu M, Wang J, Xu Y, et al. Circulating tumor DNA is effective for the detection of EGFR mutation in non-small cell lung cancer: a meta-analysis. Cancer Epidemiol Biomarkers Prev 2015;24:206-12.
46. He C, Liu M, Zhou C, et al. Detection of epidermal growth factor receptor mutations in plasma by mutant-enriched PCR assay for prediction of the response to gefitinib in patients with non-small-cell lung cancer. Int J Cancer 2009;125:2393-9.
47. Kuang Y, Rogers A, Yeap BY, et al. Noninvasive detection of EGFR T790M in gefitinib or erlotinib resistant non-small cell lung cancer. Clin Cancer Res 2009;15:2630-6.
48. Bai H, Mao L, Wang HS, et al. Epidermal growth factor receptor mutations in plasma DNA samples predict tumor response in Chinese patients with stages IIIB to IV non-small-cell lung cancer. J Clin Oncol 2009;27:2653-9.
49. Sriram KB, Tan ME, Savarimuthu SM, et al. Screening for activating EGFR mutations in surgically resected nonsmall cell lung cancer. Eur Respir J 2011;38:903-10.
50. Jiang B, Liu F, Yang L, et al. Serum detection of epidermal growth factor receptor gene mutations using mutant-enriched sequencing in Chinese patients with advanced non-small cell lung cancer. J Int Med Res 2011;39:1392-401.
51. Taniguchi K, Uchida J, Nishino K, et al. Quantitative detection of EGFR mutations in circulating tumor DNA derived from lung adenocarcinomas. Clin Cancer Res 2011;17:7808-15.
52. Brevet M, Johnson ML, Azzoli CG, et al. Detection of EGFR mutations in plasma DNA from lung cancer patients by mass spectrometry genotyping is predictive of tumor EGFR status and response to EGFR inhibitors. Lung Cancer 2011;73:96-102.
53. Nakamura T, Sueoka-Aragane N, Iwanaga K, et al. Application of a highly sensitive detection system for epidermal growth factor receptor mutations in plasma DNA. J Thorac Oncol 2012;7:1369-81.
54. Hu C, Liu X, Chen Y, et al. Direct serum and tissue assay for EGFR mutation in non-small cell lung cancer by high-resolution melting analysis. Oncol Rep 2012;28:1815-21.
55. Huang Z, Wang ZJ, Bai H, et al. The detection of EGFR mutation status in plasma is reproducible and can dynamically predict the efficacy of EGFR-TKI. Thorac Cancer 2012;3:334-40.
56. Xu F, Wu J, Xue C, et al. Comparison of different methods for detecting epidermal growth factor receptor mutations in peripheral blood and tumor tissue of non-small cell lung cancer as a predictor of response to gefitinib. Onco Targets Ther 2012;5:439-47.
57. Yam I, Lam DC, Chan K, et al. EGFR array: uses in the detection of plasma EGFR mutations in non-small cell lung cancer patients. J Thorac Oncol 2012;7:1131-40.
58. Jing CW, Wang Z, Cao HX, et al. High resolution melting analysis for epidermal growth factor receptor mutations in formalin-fixed paraffin-embedded tissue and plasma free DNA from non-small cell lung cancer patients. Asian Pac J Cancer Prev 2014;14:6619-23.
59. Liu X, Lu Y, Zhu G, et al. The diagnostic accuracy of pleural effusion and plasma samples versus tumour tissue for detection of EGFR mutation in patients with advanced non-small cell lung cancer: comparison of methodologies. J Clin Pathol 2013;66:1065-9.
60. Lv C, Ma Y, Feng Q, et al. A pilot study: sequential gemcitabine/cisplatin and icotinib as induction therapy for stage IIB to IIIA non-small-cell lung adenocarcinoma. World J Surg Oncol 2013;11:96.
61. Zhang H, Liu D, Li S, et al. Comparison of EGFR signaling pathway somatic DNA mutations derived from peripheral blood and corresponding tumor tissue of patients with advanced non-small-cell lung cancer using liquidchip technology. J Mol Diagn 2013;15:819-26.
62. Kim ST, Sung JS, Jo UH, et al. Can mutations of EGFR and KRAS in serum be predictive and prognostic markers in patients with advanced non-small cell lung cancer (NSCLC)? Med Oncol 2013;30:328.
63. Kim HR, Lee SY, Hyun DS, et al. Detection of EGFR mutations in circulating free DNA by PNA-mediated PCR clamping. J Exp Clin Cancer Res 2013;32:50.
64. Li X, Ren R, Ren S, et al. Peripheral blood for epidermal growth factor receptor mutation detection in non-small cell lung cancer patients. Transl Oncol 2014;7:341-8.
65. Wang S, Han X, Hu X, et al. Clinical significance of pretreatment plasma biomarkers in advanced non-small cell lung cancer patients. Clin Chim Acta 2014;430:63-70.
66. Bai H, Wang Z, Chen K, et al. Influence of chemotherapy on EGFR mutation status among patients with non-small-cell lung cancer. J Clin Oncol 2012;30:3077-83.
67. Reck M, Hagiwara K, Han B, et al. Investigating the utility of circulating-free tumour-derived DNA (ctDNA) in plasma for the detection of epidermal growth factor receptor (EGFR) mutation status in european and japanese patients (PTS) with advanced non-small-cell lung cancer (ANSCLC): ASSESS study. European Lung Cancer Conference, Geneva, Switzerland, 2015;abstr: 229.
68. Han B, Tjulandin S, Hagiwara K, et al. Determining the prevalence of EGFR mutations in Asian and Russian patients (pts) with advanced non-small-cell lung cancer (aNSCLC) of adenocarcinoma (ADC) and non-ADC histology: IGNITE study. European Lung Cancer Conference, Geneva, Switzerland, 2015;abstr: 233.
69. Benesova L, Minarik M, Jancarikova D, et al. Multiplicity of EGFR and KRAS mutations in non-small cell lung cancer (NSCLC) patients treated with tyrosine kinase inhibitors. Anticancer Res 2010;30:1667-71.
70. Wang S, An T, Wang J, et al. Potential clinical significance of a plasma-based KRAS mutation analysis in patients with advanced non-small cell lung cancer. Clin Cancer Res 2010;16:1324-30.
71. Del Re M, Landi L, Tiseo M, et al. Association of KRAS mutations in cell-free circulating tumor DNA with occurrence of resistance to TKIs in NSCLC. J Clin Oncol 2014;32:5 suppl: abstr 11056.
72. Sequist LV, Waltman BA, Dias-Santagata D, et al. Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors. Sci Transl Med 2011;3:75ra26.
73. Yu HA, Arcila ME, Rekhtman N, et al. Analysis of tumor specimens at the time of acquired resistance to EGFR-TKI therapy in 155 patients with EGFR-mutant lung cancers. Clin Cancer Res 2013;19:2240-7.
74. Sacher AG, Jänne PA, Oxnard GR. Management of acquired resistance to epidermal growth factor receptor kinase inhibitors in patients with advanced non-small cell lung cancer. Cancer 2014;120:2289-98.
75. Kobayashi S, Boggon TJ, Dayaram T, et al. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N Engl J Med 2005;352:786-92.
76. Pao W, Miller VA, Politi KA, et al. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med 2005;2:e73.
77. Yun CH, Mengwasser KE, Toms AV, et al. The T790M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATP. Proc Natl Acad Sci U S A 2008;105:2070-5.
78. Oxnard GR, Arcila ME, Sima CS, et al. Acquired resistance to EGFR tyrosine kinase inhibitors in EGFR-mutant lung cancer: distinct natural history of patients with tumors harboring the T790M mutation. Clin Cancer Res 2011;17:1616-22.
79. Oya Y, Yoshida T, Tanaka K, et al. Association between clinical outcome of first EGFR-TKIs and T790M mutation in NSCLC patients harboring EGFR mutation with acquired resistance to EGFR-TKIs. J Clin Oncol 2015;33:suppl; abstr e19123.
80. Zheng Di, Ye X, Zhang M, et al. Association of plasma EGFR T790M ctDNA status with clinical outcome in advanced NSCLC patients with acquired EGFR-TKI resistance. J Clin Oncol 2015;33:suppl; abstr 8080.
81. Oxnard GR, Paweletz CP, Kuang Y, et al. Noninvasive detection of response and resistance in EGFR-mutant lung cancer using quantitative next-generation genotyping of cell-free plasma DNA. Clin Cancer Res 2014;20:1698-705.
82. Sorensen BS, Wu L, Wei W, et al. Monitoring of epidermal growth factor receptor tyrosine kinase inhibitor-sensitizing and resistance mutations in the plasma DNA of patients with advanced non-small cell lung cancer during treatment with erlotinib. Cancer 2014;120:3896-901.
83. Marchetti A, Palma JF, Felicioni L, et al. Early prediction of response to tyrosine kinase inhibitors by quantification of EGFR mutations in plasma of non-small cell lung cancer patients. J Clin Oncol 2015;33:suppl; abstr 8079.
84. Ahn MJ, Lee JY, Lim SH, et al. Dynamic serial monitoring of EGFR mutations in plasma DNA samples in EGFR mutant NSCLC patients treated with EGFR TKI. J Clin Oncol 2015;33:suppl; abstr 8078.
85. Wang Z, Chen R, Wang S, et al. Quantification and dynamic monitoring of EGFR T790M in plasma cell-free DNA by digital PCR for prognosis of EGFR-TKI treatment in advanced NSCLC. PLoS One 2014;9:e110780.
86. Nakamura T, Sueoka-Aragane N, Iwanaga K, et al. A noninvasive system for monitoring resistance to epidermal growth factor receptor tyrosine kinase inhibitors with plasma DNA. J Thorac Oncol 2011;6:1639-48.
87. Marcq M, Vallée A, Bizieux A, et al. Detection of EGFR mutations in the plasma of patients with lung adenocarcinoma for real-time monitoring of therapeutic response to tyrosine kinase inhibitors? J Thorac Oncol 2014;9:e49-50.
88. Piotrowska Z, Niederst MJ, Karlovich CA, et al. Heterogeneity Underlies the Emergence of EGFRT790 Wild-Type Clones Following Treatment of T790M-Positive Cancers with a Third-Generation EGFR Inhibitor. Cancer Discov 2015;5:713-22.
89. Sequist LV, Goldman JW, Wakelee HA, et al. Efficacy of rociletinib (CO-1686) in plasma-genotyped T790M-positive non-small cell lung cancer (NSCLC) patients (pts). J Clin Oncol 2015;33:suppl; abstr 8001.
90. Thress KS, Paweletz CP, Felip E, et al. Acquired EGFR C797S mutation mediates resistance to AZD9291 in non-small cell lung cancer harboring EGFR T790M. Nat Med 2015;21:560-2.
91. Rosell R, Molina MA, Costa C, et al. Pretreatment EGFR T790M mutation and BRCA1 mRNA expression in erlotinib-treated advanced non-small-cell lung cancer patients with EGFR mutations. Clin Cancer Res 2011;17:1160-8.
92. Watanabe M, Kawaguchi T, Isa S, et al. Ultra-Sensitive Detection of the Pretreatment EGFR T790M Mutation in Non-Small Cell Lung Cancer Patients with an EGFR-Activating Mutation Using Droplet Digital PCR. Clin Cancer Res 2015;21:3552-60.