Methodological, biological and clinical aspects of circulating free DNA in metastatic colorectal cancer

References

• Ferlay J, Soerjomataram I, Ervik M, et al. GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC Cancer Base No. 11. Lyon, France: International Agency for Research on Cancer, 2013.
   Google Scholar
• Arnold M, Sierra MS, Laversanne M, et al. Global patterns and trends in colorectal cancer incidence and mortality. Gut. Forthcoming 2016. doi: 10.1136/gutjnl-2015-310912.
   Web of Science ®Google Scholar
• Chibaudel B, Tournigand C, Bonnetain F, et al. Therapeutic strategy in unresectable metastatic colorectal cancer: an updated review. Ther Adv Med Oncol. 2015;7:153–169.
   PubMed Web of Science ®Google Scholar
• Van Cutsem E, Cervantes A, Nordlinger B, ESMO Guidelines Working Group, et al. Metastatic colorectal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2014;25 (Suppl 3):iii1–iii9.
   PubMed Web of Science ®Google Scholar
• Russo M, Siravegna G, Blaszkowsky LS, et al. Tumor heterogeneity and lesion-specific response to targeted therapy in colorectal cancer. Cancer Discov. 2016;6:147–153.
   PubMed Web of Science ®Google Scholar
• Heitzer E, Ulz P, Geigl JB. Circulating tumor DNA as a liquid biopsy for cancer. Clin Chem. 2015;61:112–123.
   PubMed Web of Science ®Google Scholar
• Leon SA, Shapiro B, Sklaroff DM, et al. Free DNA in the serum of cancer patients and the effect of therapy. Cancer Res. 1977;37:646–650.
   PubMed Web of Science ®Google Scholar
• Mandel P. METAIS P Les acides nucléiques du plasma sanguin chez l'homme. C R Seances Soc Biol Fil. 1948;142:241–243.
   PubMedGoogle Scholar
• Galeazzi M, Morozzi G, Piccini M, et al. Dosage and characterization of circulating DNA: present usage and possible applications in systemic autoimmune disorders. Autoimmun Rev. 2003;2:50–55.
   PubMed Web of Science ®Google Scholar
• Li CN, Hsu HL, Wu TL, et al. Cell-free DNA is released from tumor cells upon cell death: a study of tissue cultures of tumor cell lines. J Clin Lab Anal. 2003;17:103–107.
   PubMed Web of Science ®Google Scholar
• Jahr S, Hentze H, Englisch S, et al. DNA fragments in the blood plasma of cancer patients: quantitations and evidence for their origin from apoptotic and necrotic cells. Cancer Res. 2001;61:1659–1665.
   PubMed Web of Science ®Google Scholar
• Thierry AR, Mouliere F, Gongora C, et al. Origin and quantification of circulating DNA in mice with human colorectal cancer xenografts. Nucleic Acids Res. 2010;38:6159–6175.
   PubMed Web of Science ®Google Scholar
• Stroun M, Maurice P, Vasioukhin V, et al. The origin and mechanism of circulating DNA. Ann NY Acad Sci. 2000;906:161–168.
   PubMed Web of Science ®Google Scholar
• Gormally E, Caboux E, Vineis P, et al. Circulating free DNA in plasma or serum as biomarker of carcinogenesis: practical aspects and biological significance. Mutat Res. 2007;635:105–117.
   PubMed Web of Science ®Google Scholar
• El-Gayar D, El-Abd N, Hassan N, et al. Increased free circulation DNA integrity Index as a serum biomarker in patients with colorectal carcinoma. Asian Pac J Cancer Prev. 2016;17:939–944.
   PubMedGoogle Scholar
• van der Vaart M, Pretorius PJ. Is the role of circulating DNA as a biomarker of cancer being prematurely overrated? Clin Biochem. 2010;43:26–36.
   PubMed Web of Science ®Google Scholar
• De Mattos-Arruda L, Olmos D, Tabernero J. Prognostic and predictive roles for circulating biomarkers in gastrointestinal cancer. Future Oncol. 2011;7:1385–1397.
   PubMed Web of Science ®Google Scholar
• Jung K, Fleischhacker M, Rabien A. Cell-free DNA in the blood as a solid tumor biomarker-a critical appraisal of the literature. Clin Chim Acta. 2010;411:1611–1624.
   PubMed Web of Science ®Google Scholar
• Swarup V, Rajeswari MR. Circulating (cell-free) nucleic acids: a promising, non-invasive tool for early detection of several human diseases. FEBS Lett. 2007;581:795–799.
   PubMed Web of Science ®Google Scholar
• Hao TS, Shi W, Shen XJ, et al. Circulating cell-free DNA in serum as a biomarker for diagnosis and prognostic prediction of colorectal cancer. Br J Cancer. 2014;111:1482–1489.
   PubMed Web of Science ®Google Scholar
• Fleischhacker M, Schmidt B. Cell-free DNA resuscitated for tumor testing. Nat Med. 2008;14:914–915.
   PubMed Web of Science ®Google Scholar
• Aung KL, Board RE, Ellison G, et al. Current status and future potential of somatic mutation testing from circulating free DNA in patients with solid tumours. Hugo J. 2010;4:11–21.
   PubMedGoogle Scholar
• Lim SH, Becker TM, Chua W, et al. Circulating tumour cells and circulating free nucleic acid as prognostic and predictive biomarkers in colorectal cancer. Cancer Lett. 2014;346:24–33.
   PubMed Web of Science ®Google Scholar
• El Messaoudi S, Rolet F, Mouliere F, et al. Circulating cell free DNA: Preanalytical considerations. Clin Chim Acta. 2013;424: 222–30.
   PubMed Web of Science ®Google Scholar
• Barra GB, Santa Rita TH, Vasques Jde A, et al. EDTA-mediated inhibition of DNases protects circulating cell-free DNA from ex vivo degradation in blood samples. Clin Biochem. 2015;48:976–81.
   PubMed Web of Science ®Google Scholar
• Malentacchi F, Pizzamiglio S, Verderio P, et al. Influence of storage conditions and extraction methods on the quantity and quality of circulating cell-free DNA (ccfDNA): the SPIDIA-DNAplas External Quality Assessment experience. Clin Chem Lab Med. 2015;53:1935–1942.
   PubMed Web of Science ®Google Scholar
• Devonshire AS, Whale AS, Gutteridge A, et al. Towards standardisation of cell-free DNA measurement in plasma: controls for extraction efficiency, fragment size bias and quantification. Anal Bioanal Chem. 2014;406:6499–6512.
   PubMed Web of Science ®Google Scholar
• Fleischhacker M, Schmidt B, Weickmann S, et al. Methods for isolation of cell-free plasma DNA strongly affect DNA yield. Clin Chim Acta. 2011;412:2085–2058.
   PubMed Web of Science ®Google Scholar
• Pallisgaard N, Spindler KL, Andersen RF, et al. Controls to validate plasma samples for cell free DNA quantification. Clin Chim Acta. 2015;446:141–146.
   PubMed Web of Science ®Google Scholar
• Benesova L, Belsanova B, Suchanek S, et al. Mutation-based detection and monitoring of cell-free tumor DNA in peripheral blood of cancer patients. Anal Biochem. 2013;433:227–234.
   PubMed Web of Science ®Google Scholar
• Bronkhorst AJ, Aucamp J, Pretorius PJ. Cell-free DNA: preanalytical variables. Clin Chim Acta. 2015;450:243–253.
   PubMed Web of Science ®Google Scholar
• Spindler KL, Pallisgaard N, Vogelius I, et al. Quantitative cell free DNA, KRAS and BRAF mutations in plasma from patients with metastatic colorectal cancer during treatment with cetuximab and irinotecan. Clin Cancer Res. 2012;18:1177–1185.
   PubMed Web of Science ®Google Scholar
• Spindler KL, Pallisgaard N, Appelt A, et al. Clinical utility of KRAS status in circulating plasma DNA compared to archival tumor tissue from patients with metastatic colorectal cancer treated with anti-EGFR therapy. Eur J Cancer. 2015;51:2678–2685.
   PubMed Web of Science ®Google Scholar
• Taly V, Pekin D, Benhaim L, et al. Multiplex picodroplet digital PCR to detect KRAS mutations in circulating DNA from the plasma of colorectal cancer patients. Clin Chem. 2013;59:1722–1731.
   PubMed Web of Science ®Google Scholar
• Day E, Dear PH, McCaughan F. Digital PCR strategies in the development and analysis of molecular biomarkers for personalized medicine. Methods. 2013;59:101–107.
   PubMed Web of Science ®Google Scholar
• Pekin D, Skhiri Y, Baret JC, et al. Quantitative and sensitive detection of rare mutations using droplet-based microfluidics. Lab Chip. 2011;11:2156–2166.
   PubMed Web of Science ®Google Scholar
• Andersen RF, Spindler KL, Brandslund I, et al. Improved sensitivity of circulating tumor DNA measurement using short PCR amplicons. Clin Chim Acta. 2015;439:97–101.
   PubMed Web of Science ®Google Scholar
• Diehl F, Li M, He Y, et al. BEAMing: single-molecule PCR on microparticles in water-in-oil emulsions. Nat Methods. 2006;3:551–559.
   PubMed Web of Science ®Google Scholar
• Diaz LA, Jr, Williams RT, Wu J, et al. The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers. Nature. 2012;486:537–540.
   PubMed Web of Science ®Google Scholar
• Misale S, Yaeger R, Hobor S, et al. Emergence of KRAS mutations and acquired resistance to anti-EGFR therapy in colorectal cancer. Nature. 2012;486:532–536.
   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;6:224ra24.
   PubMed Web of Science ®Google Scholar
• Narayan A, Carriero NJ, Gettinger SN, et al. Ultrasensitive measurement of hotspot mutations in tumor DNA in blood using error-suppressed multiplexed deep sequencing. Cancer Res. 2012;72:3492–3498.
   PubMed Web of Science ®Google Scholar
• Lebofsky R, Decraene C, Bernard V, et al. Circulating tumor DNA as a non-invasive substitute to metastasis biopsy for tumor genotyping and personalized medicine in a prospective trial across all tumor types. Mol Oncol 2015;9:783–790.
   PubMed Web of Science ®Google Scholar
• Frenel JS, Carreira S, Goodall J, et al. Serial next-generation sequencing of circulating cell-free dna evaluating tumor clone response to molecularly targeted drug administration. Clin Cancer Res. 2015;21:4586–4596.
   PubMed Web of Science ®Google Scholar
• Tabernero J, Lenz H-J, Siena S, et al. Analysis of circulating DNA and protein biomarkers to predict the clinical activity of regorafenib and assess prognosis in patients with metastatic colorectal cancer: a retrospective, exploratory analysis of the CORRECT trial. Lancet Onc. 2015;16:937–948.
   PubMed Web of Science ®Google Scholar
• Su YH, Wang M, Brenner DE, et al. Detection of mutated K-ras DNA in urine, plasma, and serum of patients with colorectal carcinoma or adenomatous polyps. Ann NY Acad Sci. 2008;1137:197–206.
   PubMed 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 USA. 2005;102:16368–16373.
   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;13:139–42.
   Web of Science ®Google Scholar
• Snyder MW, Kircher M, Hill AJ, et al. Cell-free DNA comprises an in vivo nucleosome footprint that informs its tissues-of-origin. Cell. 2016;164:57–68.
   PubMed Web of Science ®Google Scholar
• Lui YY1, Dennis YM. Circulating DNA in plasma and serum: biology, preanalytical issues and diagnostic applications. Clin Chem Lab Med. 2002;40:962–968.
   PubMed Web of Science ®Google Scholar
• Bronkhorst AJ, Wentzel JF, Aucamp J, et al. Characterization of the cell-free DNA released by cultured cancer cells. Biochim Biophys Acta. 2016;863:157–165.
   Web of Science ®Google Scholar
• Zonta E, Nizard P, Taly V. Assessment of DNA integrity, applications for cancer research. Adv Clin Chem. 2015;70:197–246.
   PubMed Web of Science ®Google Scholar
• Anker P, Mulcahy H, Chen XQ, et al. Review detection of circulating tumour DNA in the blood (plasma/serum) of cancer patients. Cancer Metastasis Rev. 1999;18:65–73.
   PubMed Web of Science ®Google Scholar
• Spindler KL, Sorensen M, Pallisgaard N, et al. Phase II trial of temsirolimus alone and in combination with irinotecan for KRAS mutant metastatic colorectal cancer: outcome and results of KRAS mutational analysis in plasma. Acta Oncol. 2013;52:963–970.
   PubMed Web of Science ®Google Scholar
• Spindler KL, Pallisgaard N, Andersen R, et al. Pemetrexed and gemcitabine for chemotherapy refractory colorectal cancer: results of a phase II and translational research study. J Cancer Ther. 2013;4:44–50.
   Google Scholar
• Spindler KL, Pallisgaard N, Andersen RF, et al. Gemcitabine and capecitabine for heavily pre-treated metastatic colorectal cancer: a phase II and translational research study. Anticancer Res. 2014;34:845–850.
   PubMed Web of Science ®Google Scholar
• Spindler KL, Appelt A, Pallisgaard N, et al. Cell-free DNA in healthy individuals, noncancerous disease and strong prognostic value in colorectal cancer. Int J Cancer. 2014;135:2984–2991.
   PubMed Web of Science ®Google Scholar
• Hansen TF, Andersen RF, Pallisgaard N, et al. A three weekly schedule of irinotecan and panitumumab as third-line treatment for patients with wild type KRAS metastatic colorectal cancer: Results from. A phase II trial. Colorec Cancer. 2014;3:135–145.
   Google Scholar
• Spindler KL, Pallisgaard N, Appelt A, et al. 3KRAS-mutated plasma DNA as predictor of outcome from irinotecan monotherapy in metastatic colorectal cancer. Br J Cancer. 2013;109:3067–3072.
   PubMed Web of Science ®Google Scholar
• Wong AL, Lim JS, Sinha A, et al. Tumour pharmacodynamics and circulating cell free DNA in patients with refractory colorectal carcinoma treated with regorafenib. J Transl Med. 2015;13:57.
   PubMed Web of Science ®Google Scholar
• Sefrioui D, Sarfan-Vasseur N, Beaussire L, et al. Clinical value of chip based digital-PCR platform for the detection of circulating DNA in metastatic colorectal cancer. Digest Liver Dis. 2015; 47:884–890.
   Web of Science ®Google Scholar
• Spindler KL, Pallisgaard N, Andersen RF, et al. Circulating free DNA as biomarker and source for mutation detection in metastatic colorectal cancer. PLoS One. 2015;10:e0108247.
   PubMed Web of Science ®Google Scholar
• da Silva Filho BF, Gurgel AP, Neto MÁ, et al. Circulating cell-free DNA in serum as a biomarker of colorectal cancer. J Clin Pathol. 2013;66:775–778.
   PubMed Web of Science ®Google Scholar
• Perkins G, Yap TA, et al. Multi-purpose utility of circulating plasma DNA testing in patients with advanced cancers. PLoS One. 2012;7:e47020.
   PubMed Web of Science ®Google Scholar
• Qi J, Qian C, Shi W, et al. Alu-based cell-free DNA: a potential complementary biomarker for diagnosis of colorectal cancer. Clin Biochem. 2013;46:64–9.
   PubMed Web of Science ®Google Scholar
• Mead R, Duku M, Bhandari P, et al. Circulating tumour markers can define patients with normal colons, benign polyps, and cancers. Br J Cancer. 2011;105:239–245.
   PubMed Web of Science ®Google Scholar
• Czeiger D, Shaked G, Eini H, et al. Measurement of circulating cell-freeDNA levesl by a new simple flouroscent test in patients with primary colorectal cancer. Am J Clin Pathol. 2011;135:264–270.
   PubMed Web of Science ®Google Scholar
• Danese E, Montagnana M, Minicozzi AM, et al. Real-time polymerase chain reaction quantification of free DNA in serum of patients with polyps and colorectal cancers. Clin Chem Lab Med. 2010;48:1665–8.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Boni L, Cassinotti E, Canziani M, et al. Free circulating DNA as possible tumour marker in colorectal cancer. Surg Oncol. 2007;16 (Suppl 1):S29–S31.
   PubMed Web of Science ®Google Scholar
• Flamini E, Mercatali L, Nanni O, et al. Free DNA and carcinoembryonic antigen serum levels: an important combination for diagnosis of colorectal cancer. Clin Cancer Res. 2006;12:6985–6988.
   PubMed Web of Science ®Google Scholar
• Shapiro B, Chakrabarty M, Cohn EM, et al. Determination of circulating DNA levels in patients with benign or malignant gastrointestinal disease. Cancer. 1983;51:2116–2120.
   PubMed Web of Science ®Google Scholar
• Guadalajara H, Domínguez-Berzosa C, García-Arranz M, et al. The concentration of deoxyribonucleic acid in plasma from 73 patients with colorectal cancer and apparent clinical correlations. Cancer Detect Prev. 2008;32:39–44.
   PubMedGoogle Scholar
• Eisenhauer EA, Therasse P, Bogaerts J. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer. 2009;45:228–47.
   PubMed Web of Science ®Google Scholar
• Aprile G, Fontanella C, Bonotto M, et al. Timing and extent of response in colorectal cancer: critical review of current data and implication for future trials. Oncotarget. 2015;6:28716–28730.
   PubMed Web of Science ®Google Scholar
• Mouliere F, Thierry AR. The importance of examining the proportion of circulating DNA originating from tumor, microenvironment and normal cells in colorectal cancer patients. Expert Opin Biol Ther. 2012;12 (Suppl 1):S209–S215.
   PubMed Web of Science ®Google Scholar
• Dawson SJ, Rosenfeld N, Caldas C. Circulating tumor DNA to monitor metastatic breast cancer. N Engl J Med. 2013;369:93–94.
   PubMed Web of Science ®Google Scholar
• Morelli MP, Overman MJ, Dasari A. Characterizing the patterns of clonal selection in circulating tumor DNA from patients with colorectal cancer refractory to anti-EGFR treatment. Ann Oncol. 2015;26:731–736.
   PubMed Web of Science ®Google Scholar
• Nygaard AD, Holdgaard PC, Spindler KL, et al. The correlation between cell-free DNA and tumour burden was estimated by PET/CT in patients with advanced NSCLC. Br J Cancer. 2014;110:363–368.
   PubMed Web of Science ®Google Scholar
• Ryan BM, Lefort F, McManus R, et al. A prospective study of circulating mutant KRAS2 in the serum of patients with colorectal neoplasia: strong prognostic indicator in postoperative follow up. Gut. 2003;52:101–108.
   PubMed Web of Science ®Google Scholar
• Diehl F, Schmidt K, Choti MA. Circulating mutant DNA to assess tumor dynamics. Nat Med. 2008;14:985–990.
   PubMed Web of Science ®Google Scholar
• Tie J, Kinde I, Wang Y, et al. Circulating tumor DNA as an early marker of therapeutic response in patients with metastatic colorectal cancer. Ann Oncol. 2015;26:1715–1722.
   PubMed Web of Science ®Google Scholar
• Siravegna G, Mussolin B, Buscarino M, et al. A.Clonal evolution and resistance to EGFR blockade in the blood of colorectal cancer patients. Nat Med. 2015;21:795–801.
   PubMed Web of Science ®Google Scholar
• Li G, Wang Z, Xu J, et al. The prognostic value of lactate dehydrogenase levels in colorectal cancer: a meta-analysis. BMC Cancer. 2016;16:249.
   PubMed Web of Science ®Google Scholar
• Spindler KL, Boysen A, Pallisgaard N, et al. A systematic review and meta-analysis of the prognostic value of total cell-free DNA quantification in metastatic colorectal cancer. The European Society of Medical Oncology Congress 2016; ESMO; 2016; Copenhagen.
   Google Scholar
• Qiu LX, Mao C, Zhang J, et al. Predictive and prognostic value of KRAS mutations in metastatic colorectal cancer patients treated with cetuximab: a meta-analysis of 22 studies. Eur J Cancer. 2010;46:2781–2787.
   PubMed Web of Science ®Google Scholar
• Rogosnitzky M, Danks R. Validation of blood testing for K-ras mutations in colorectal and pancreatic cancer. Anticancer Res. 2010;30:2943–2947.
   PubMed Web of Science ®Google Scholar
• Thierry AR, Mouliere F, El Messaoudi S, et al. Clinical validation of the detection of KRAS and BRAF mutations from circulating tumor DNA. Nat Med. 2014;20:430–435.
   PubMed Web of Science ®Google Scholar
• Yen LC, Yeh YS, Chen CW, et al. Detection of KRAS oncogene in peripheral blood as a predictor of the response to cetuximab plus chemotherapy in patients with metastatic colorectal cancer. Clin Cancer Res. 2009;15:4508–4513.
   PubMed Web of Science ®Google Scholar
• Xu JM, Liu XJ, Ge FJ, et al. KRAS mutations in tumor tissue and plasma by different assays predict survival of patients with metastatic colorectal cancer. J Exp Clin Cancer Res. 2014;33:104.
   PubMed Web of Science ®Google Scholar
• Shethah R, Morgan J. Comparison of KRAS mutation assessment in tumor DNA and circulating free DNA in plasma and serum samples. Clin Med Insights Pathol. 2012;5:15–22.
   PubMedGoogle Scholar
• Janku F, Angenendt F, Apostolia M, et al. Actionable mutations in plasma cell-free DNA in patients with advanced cancers referred for experimental targeted therapies. Oncotarget. 2015;6:12809–12821.
   PubMed Web of Science ®Google Scholar
• Kidess E, Heirich K, Wiggin M, et al. Mutation profiling of tumor DNA from plasma and tumor tissue of colorectal cancer patients with a novel, high-sensitivity multiplexed mutation detection platform. Oncotarget. 2015;6:2549–2561.
   PubMed Web of Science ®Google Scholar
• Spindler KL, Pallisgaard N, Andersen RF, et al. Changes in mutational status during third-line treatment for metastatic colorectal cancer–results of consecutive measurement of cell free DNA, KRAS and BRAF in the plasma. Int J Cancer. 2014;135:2215–2222.
   PubMed Web of Science ®Google Scholar
• Mohan S, Heitzer E, Ulz P, et al. Changes in colorectal carcinoma genomes under anti-EGFR therapy identified by whole-genome plasma DNA sequencing. PLoS Genet. 2014;10:e1004271.
   PubMed Web of Science ®Google Scholar