An update on liquid biopsy analysis for diagnostic and monitoring applications in non-small cell lung cancer

References

• Molina JR, Yang P, Cassivi SD, et al. Non-small cell lung cancer: epidemiology, risk factors, treatment, and survivorship. Mayo Clin Proc. 2008;83:584–594.
   PubMed Web of Science ®Google Scholar
• 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;373:123–135.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Mok TS, Wu YL, Thongprasert S, et al. Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med. 2009;361:947–957.
   PubMed Web of Science ®Google Scholar
• 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;13:239–246.
   PubMed Web of Science ®Google Scholar
• Solomon BJ, Mok T, Kim DW, et al. First-line crizotinib versus chemotherapy in ALK-positive lung cancer. N Engl J Med. 2014;371:2167–2177.
   PubMed Web of Science ®Google Scholar
• Diaz LA Jr., Bardelli A. Liquid biopsies: genotyping circulating tumor DNA. J Clin Oncol. 2014;32:579–586.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Tan DS, Camilleri-Broet S, Tan EH, et al. Intertumor heterogeneity of non-small-cell lung carcinomas revealed by multiplexed mutation profiling and integrative genomics. Int J Cancer. 2014;135:1092–1100.
   PubMed Web of Science ®Google Scholar
• Gerlinger M, Rowan AJ, Horswell S, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med. 2012;366:883–892.
   PubMed Web of Science ®Google Scholar
• Vogelstein B, Papadopoulos N, Velculescu VE, et al. Cancer genome landscapes. Science. 2013;339:1546–1558.
   PubMed Web of Science ®Google Scholar
• Molina-Vila MA, Mayo-de-Las-Casas C, Gimenez-Capitan A, et al. Liquid biopsy in non-small cell lung cancer. Front Med (Lausanne). 2016;3:69.
   PubMed Web of Science ®Google Scholar
• Luke JJ, Oxnard GR, Paweletz CP, et al. Realizing the potential of plasma genotyping in an age of genotype-directed therapies. J Natl Cancer Inst. 2014;106:dju214
   PubMedGoogle Scholar
• 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;18:2391–2401.
   PubMed Web of Science ®Google Scholar
• Fleischhacker M, Schmidt B. Circulating nucleic acids (CNAs) and cancer–a survey. Biochim Biophys Acta. 2007;1775:181–232.
   PubMed Web of Science ®Google Scholar
• Leary RJ, Kinde I, Diehl F, et al. Development of personalized tumor biomarkers using massively parallel sequencing. Sci Transl Med. 2010;2:20ra14.
   PubMed Web of Science ®Google Scholar
• Leary RJ, Sausen M, Kinde I, et al. Detection of chromosomal alterations in the circulation of cancer patients with whole-genome sequencing. Sci Transl Med. 2012;4:162ra154.
   PubMed Web of Science ®Google Scholar
• Dawson SJ, Tsui DW, Murtaza M, et al. Analysis of circulating tumor DNA to monitor metastatic breast cancer. N Engl J Med. 2013;368:1199–1209.
   PubMed Web of Science ®Google Scholar
• Bettegowda C, Sausen M, Leary RJ, et al. Detection of circulating tumor DNA in early- and late-stage human malignancies. Sci Transl Med. 2014;6:224ra224.
   Web of Science ®Google Scholar
• 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;102:16368–16373.
   PubMed Web of Science ®Google Scholar
• Diehl F, Schmidt K, Choti MA, et al. Circulating mutant DNA to assess tumor dynamics. Nat Med. 2008;14:985–990.
   PubMed Web of Science ®Google Scholar
• Schwarzenbach H, Hoon DS, Pantel K. Cell-free nucleic acids as biomarkers in cancer patients. Nat Rev Cancer. 2011;11:426–437.
   PubMed Web of Science ®Google Scholar
• Stroun M, Lyautey J, Lederrey C, et al. About the possible origin and mechanism of circulating DNA apoptosis and active DNA release. Clin Chim Acta. 2001;313:139–142.
   PubMed Web of Science ®Google Scholar
• Choi JJ, Reich CF 3rd, Pisetsky DS. The role of macrophages in the in vitro generation of extracellular DNA from apoptotic and necrotic cells. Immunology. 2005;115:55–62.
   PubMed Web of Science ®Google Scholar
• Board RE, Williams VS, Knight L, et al. Isolation and extraction of circulating tumor DNA from patients with small cell lung cancer. Ann N Y Acad Sci. 2008;1137:98–107.
   PubMed Web of Science ®Google Scholar
• Vallee A, Marcq M, Bizieux A, et al. Plasma is a better source of tumor-derived circulating cell-free DNA than serum for the detection of EGFR alterations in lung tumor patients. Lung Cancer. 2013;82:373–374.
   PubMed Web of Science ®Google Scholar
• Gonzalez-Cao M, Mayo-de-Las-Casas C, Molina-Vila MA, et al. BRAF mutation analysis in circulating free tumor DNA of melanoma patients treated with BRAF inhibitors. Melanoma Res. 2015;25:486–495.
   PubMed Web of Science ®Google Scholar
• Malapelle U, Mayo de-Las-Casas C, Rocco D, et al. Development of a gene panel for next-generation sequencing of clinically relevant mutations in cell-free DNA from cancer patients. Br J Cancer. 2017;116:802–810.
   PubMed Web of Science ®Google Scholar
• Mayo-de-las-Casas C, Jordana-Ariza N, Garzón-Ibañez M, et al. Large scale, prospective screening of EGFR mutations in the blood of advanced NSCLC patients to guide treatment decisions. Ann Oncol. 2017. Published on line July 2017. DOI:10.1093/annonc/mdx288.
   PubMed Web of Science ®Google Scholar
• Santarpia M, Karachaliou N, Gonzalez-Cao M, et al. Feasibility of cell-free circulating tumor DNA testing for lung cancer. Biomark Med. 2016;10:417–430.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Zhang X, Gureasko J, Shen K, et al. An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor. Cell. 2006;125:1137–1149.
   PubMed Web of Science ®Google Scholar
• Soh J, Okumura N, Lockwood WW, et al. Oncogene mutations, copy number gains and mutant allele specific imbalance (MASI) frequently occur together in tumor cells. PLoS One. 2009;4:e7464.
   PubMed Web of Science ®Google Scholar
• 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;97:339–346.
   PubMed Web of Science ®Google Scholar
• 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;16:141–151.
   PubMed Web of Science ®Google Scholar
• Bethune G, Bethune D, Ridgway N, et al. Epidermal growth factor receptor (EGFR) in lung cancer: an overview and update. J Thorac Dis. 2010;2:48–51.
   PubMedGoogle Scholar
• Lovly CM, Iyengar P, Gainor JF. Managing resistance to EFGR- and ALK-targeted therapies. Am Soc Clin Oncol Educ Book. 2017;37:607–618.
   PubMedGoogle Scholar
• Sacher AG, Paweletz C, Dahlberg SE, et al. Prospective validation of rapid plasma genotyping for the detection of EGFR and KRAS mutations in advanced lung cancer. JAMA Oncol. 2016;2:1014–1022.
   PubMed Web of Science ®Google Scholar
• Karachaliou N, Mayo-De Las Casas C, Queralt C, et al. Association of EGFR L858R mutation in circulating free DNA with survival in the EURTAC trial. JAMA Oncol. 2015;1:149–157.
   PubMed Web of Science ®Google Scholar
• Rosell R, Moran T, Queralt C, et al. Screening for epidermal growth factor receptor mutations in lung cancer. N Engl J Med. 2009;361:958–967.
   PubMed Web of Science ®Google Scholar
• De Las Casas CM, Gonzalez-Cao M, Ramirez SV, et al. Usefulness of circulating free DNA for monitoring epidermal growth factor receptor mutations in advanced non-small cell lung cancer patients: a case report. Transl Lung Cancer Res. 2016;5:532–537.
   PubMed Web of Science ®Google Scholar
• European Medicines Agency, Summary of Product Characteristics for Iressa, Annex 1 [cited 2014 April 23]. Available from: http://www.ema.europa.eu/docs/en_GB/document_library/EPAR_-_Product_Information/human/001016/WC500036358.pdf.
   Google Scholar
• Janku F, Kurzrock R. Bringing blood-based molecular testing to the clinic. Clin Cancer Res. 2016;22:5400–5402.
   PubMed Web of Science ®Google Scholar
• Federal Drug Administration. List of Cleared or Approved Companion Diagnostic Devices [cited 2017 Oct 19]. Available from: http://www.fda.gov/MedicalDevices/ProductsandMedicalProcedures/InVitroDiagnostics/ucm301431.htm.
   Google Scholar
• Ai B, Liu H, Huang Y, et al. Circulating cell-free DNA as a prognostic and predictive biomarker in non-small cell lung cancer. Oncotarget. 2016;7:44583.
   PubMed Web of Science ®Google Scholar
• 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;120:3896–3901.
   PubMed Web of Science ®Google Scholar
• Marchetti A, Palma JF, Felicioni L, et al. Early prediction of response to tyrosine kinase inhibitors by quantification of EGFR mutations in plasma of NSCLC patients. J Thorac Oncol. 2015;10:1437–1443.
   PubMed Web of Science ®Google Scholar
• Bordi P, Del Re M, Danesi R, et al. Circulating DNA in diagnosis and monitoring EGFR gene mutations in advanced non-small cell lung cancer. Transl Lung Cancer Res. 2015;4:584–597.
   PubMed Web of Science ®Google Scholar
• 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;20:1698–1705.
   PubMed Web of Science ®Google Scholar
• Ahn M-J, 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;33:8078.
   Google Scholar
• Garzon M, Villatoro S, Teixido C, et al. KRAS mutations in the circulating free DNA (cfDNA) of non-small cell lung cancer (NSCLC) patients. Transl Lung Cancer Res. 2016;5:511–516.
   PubMed Web of Science ®Google Scholar
• Dong ZY, Zhong WZ, Zhang XC, et al. Potential predictive value of TP53 and KRAS mutation status for response to PD-1 blockade immunotherapy in lung adenocarcinoma. Clin Cancer Res. 2017;23:3012–3024.
   PubMed Web of Science ®Google Scholar
• Pan W, Yang Y, Zhu H, et al. KRAS mutation is a weak, but valid predictor for poor prognosis and treatment outcomes in NSCLC: a meta-analysis of 41 studies. Oncotarget. 2016;7:8373–8388.
   PubMed Web of Science ®Google Scholar
• Molina-Vila MA, Bertran-Alamillo J, Gasco A, et al. Nondisruptive p53 mutations are associated with shorter survival in patients with advanced non-small cell lung cancer. Clin Cancer Res. 2014;20:4647–4659.
   PubMed Web of Science ®Google Scholar
• Rosell R, Karachaliou N. Large-scale screening for somatic mutations in lung cancer. Lancet. 2016;387:1354–1356.
   PubMed Web of Science ®Google Scholar
• Yang Y, Shen X, Li R, et al. The detection and significance of EGFR and BRAF in cell-free DNA of peripheral blood in NSCLC. Oncotarget. 2017;8:49773.
   PubMed Web of Science ®Google Scholar
• Planchard D, Besse B, Groen HJ, et al. Dabrafenib plus trametinib in patients with previously treated BRAF(V600E)-mutant metastatic non-small cell lung cancer: an open-label, multicentre phase 2 trial. Lancet Oncol. 2016;17:984–993.
   PubMed Web of Science ®Google Scholar
• Fang M, Xu C, Wu J, et al. A comparison of consistency of detecting BRAF gene mutations in peripheral blood and tumor tissue of nonsmall-cell lung cancer patients. J Cancer Res Ther. 2014;10(Suppl):C150–154.
   PubMed Web of Science ®Google Scholar
• Morgensztern D, Campo MJ, Dahlberg SE, et al. Molecularly targeted therapies in non-small-cell lung cancer annual update 2014. J Thorac Oncol. 2015;10:S1–63.
   PubMed Web of Science ®Google Scholar
• Mohammed AA, El-Tanni H, Alsakkaf MA, et al. Genomic aberrations in non- small cell lung cancer and their impact on treatment outcome. J Cancer Res Ther. 2017;13:9–15.
   PubMed Web of Science ®Google Scholar
• Korpanty GJ, Graham DM, Vincent MD, et al. Biomarkers that currently affect clinical practice in lung cancer: EGFR, ALK, MET, ROS-1, and KRAS. Front Oncol. 2014;4:204.
   PubMedGoogle Scholar
• Reguart N, Teixido C, Gimenez-Capitan A, et al. Identification of ALK, ROS1, and RET fusions by a multiplexed mRNA-based assay in formalin-fixed, paraffin-embedded samples from advanced non-small-cell lung cancer patients. Clin Chem. 2017;63:751–760.
   PubMed Web of Science ®Google Scholar
• Nilsson RJ, Karachaliou N, Berenguer J, et al. Rearranged EML4-ALK fusion transcripts sequester in circulating blood platelets and enable blood-based crizotinib response monitoring in non-small-cell lung cancer. Oncotarget. 2016;7:1066–1075.
   PubMed Web of Science ®Google Scholar
• Aguado C, Gimenez-Capitan A, Karachaliou N, et al. Fusion gene and splice variant analyses in liquid biopsies of lung cancer patients. Transl Lung Cancer Res. 2016;5:525–531.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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;19:2240–2247.
   PubMed Web of Science ®Google Scholar
• Janne PA, Yang JC, Kim DW, et al. AZD9291 in EGFR inhibitor-resistant non-small-cell lung cancer. N Engl J Med. 2015;372:1689–1699.
   PubMed Web of Science ®Google Scholar
• Sequist LV, Soria JC, Goldman JW, et al. Rociletinib in EGFR-mutated non-small-cell lung cancer. N Engl J Med. 2015;372:1700–1709.
   PubMed Web of Science ®Google Scholar
• Engelman JA, Zejnullahu K, Gale CM, et al. PF00299804, an irreversible pan-ERBB inhibitor, is effective in lung cancer models with EGFR and ERBB2 mutations that are resistant to gefitinib. Cancer Res. 2007;67:11924–11932.
   PubMed Web of Science ®Google Scholar
• Fan W, Tang Z, Yin L, et al. MET-independent lung cancer cells evading EGFR kinase inhibitors are therapeutically susceptible to BH3 mimetic agents. Cancer Res. 2011;71:4494–4505.
   PubMed Web of Science ®Google Scholar
• Morgillo F, Della Corte CM, Fasano M, et al. Mechanisms of resistance to EGFR-targeted drugs: lung cancer. ESMO Open. 2016;1:e000060.
   PubMed Web of Science ®Google Scholar
• Lee JY, Qing X, Xiumin W, et al. Longitudinal monitoring of EGFR mutations in plasma predicts outcomes of NSCLC patients treated with EGFR TKIs: Korean Lung Cancer Consortium (KLCC-12-02). Oncotarget. 2016;7:6984–6993.
   PubMed Web of Science ®Google Scholar
• Sundaresan TK, Sequist LV, Heymach JV, et al. Detection of T790M, the acquired resistance EGFR mutation, by tumor biopsy versus noninvasive blood-based analyses. Clin Cancer Res. 2016;22:1103–1110.
   PubMed Web of Science ®Google Scholar
• Karlovich C, Goldman JW, Sun JM, et al. Assessment of EGFR mutation status in matched plasma and tumor tissue of NSCLC patients from a phase I study of rociletinib (CO-1686). Clin Cancer Res. 2016;22:2386–2395.
   PubMed Web of Science ®Google Scholar
• 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;21:560–562.
   PubMed Web of Science ®Google Scholar
• Chic N, Mayo-de-Las-Casas C, Reguart N. Successful treatment with gefitinib in advanced non-small cell lung cancer after acquired resistance to osimertinib. J Thorac Oncol. 2017;12:e78–e80.
   PubMedGoogle Scholar
• Yu HA, Tian SK, Drilon AE, et al. Acquired resistance of EGFR-mutant lung cancer to a T790M-specific EGFR Inhibitor: emergence of a third mutation (C797S) in the EGFR tyrosine kinase domain. JAMA Oncol. 2015;1:982–984.
   PubMed Web of Science ®Google Scholar
• Wang Z, Yang JJ, Huang J, et al. Brief report: lung adenocarcinoma harboring EGFR T790M and in trans C797S responds to combination therapy of first and third generation EGFR-TKIs and shifts allelic configuration at resistance. J Thorac Oncol. 2017;12(11):1723–1727.
   Web of Science ®Google Scholar
• Isozaki H, Takigawa N, Kiura K. Mechanisms of Acquired Resistance to ALK inhibitors and the rationale for treating ALK-positive lung cancer. Cancers (Basel). 2015;7:763–783.
   PubMed Web of Science ®Google Scholar
• Shaw AT, Friboulet L, Leshchiner I, et al. Resensitization to crizotinib by the lorlatinib ALK resistance mutation L1198F. N Engl J Med. 2016;374:54–61.
   PubMed Web of Science ®Google Scholar
• Doebele RC, Pilling AB, Aisner DL, et al. Mechanisms of resistance to crizotinib in patients with ALK gene rearranged non-small cell lung cancer. Clin Cancer Res. 2012;18:1472–1482.
   PubMed Web of Science ®Google Scholar
• Bordi P, Tiseo M, Rofi E, et al. Detection of ALK and KRAS mutations in circulating tumor DNA of patients with advanced ALK-positive NSCLC with disease progression during crizotinib treatment. Clin Lung Cancer. 2017;18(6):692–697.
   Web of Science ®Google Scholar
• Crowley E, Di Nicolantonio F, Loupakis F, et al. Liquid biopsy: monitoring cancer-genetics in the blood. Nat Rev Clin Oncol. 2013;10:472–484.
   PubMed Web of Science ®Google Scholar
• Volik S, Alcaide M, Morin RD, et al. Cell-free DNA (cfDNA): clinical significance and utility in cancer shaped by emerging technologies. Mol Cancer Res. 2016;14:898–908.
   PubMed Web of Science ®Google Scholar
• 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;4:136ra168.
   Web of Science ®Google Scholar
• 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;9:1345–1353.
   PubMed Web of Science ®Google Scholar
• 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;12:3915–3921.
   PubMed Web of Science ®Google Scholar
• 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;21:3196–3203.
   PubMed Web of Science ®Google Scholar
• 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;7:115–121.
   PubMed Web of Science ®Google Scholar
• Rosell R, Molina MA, Serrano MJ. EGFR mutations in circulating tumour DNA. Lancet Oncol. 2012;13:971–973.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Nordgard O, Oltedal S, Janssen EA, et al. Comparison of a PNA clamp PCR and an ARMS/Scorpion PCR assay for the detection of K-RAS mutations. Diagn Mol Pathol. 2012;21:9–13.
   PubMedGoogle Scholar
• Thress KS, Brant R, Carr TH, et al. EGFR mutation detection in ctDNA from NSCLC patient plasma: a cross-platform comparison of leading technologies to support the clinical development of AZD9291. Lung Cancer. 2015;90:509–515.
   PubMed Web of Science ®Google Scholar
• Oxnard GR, Thress KS, Alden RS, et al. Association between plasma genotyping and outcomes of treatment with osimertinib (AZD9291) in advanced non-small-cell lung cancer. J Clin Oncol. 2016;34:3375–3382.
   PubMed Web of Science ®Google Scholar
• Yang M, Topaloglu U, Petty WJ, et al. Circulating mutational portrait of cancer: manifestation of aggressive clonal events in both early and late stages. J Hematol Oncol. 2017;10:100.
   PubMed Web of Science ®Google Scholar