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

Acta Oncologica

Volumn 56, Issue 1, 2017, Pages 7-16

  Spindler, Karen Lise G ^a  

^a AARHUS UNIVERSITY HOSPITAL   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CARCINOEMBRYONIC ANTIGEN; DNA; NUCLEIC ACID; TUMOR MARKER;

ANALYTIC METHOD; CLINICAL FEATURE; DIAGNOSTIC VALUE; GENE MUTATION; HUMAN; METASTATIC COLORECTAL CANCER; PHASE 2 CLINICAL TRIAL (TOPIC); PLASMA; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVIEW; SERUM; STANDARD; BLOOD; COLORECTAL TUMOR; DNA MUTATIONAL ANALYSIS; GENETICS; MUTATION; PATHOLOGY; PROCEDURES; PROGNOSIS; SECONDARY; TUMOR EMBOLISM;

BIOMARKERS, TUMOR; COLORECTAL NEOPLASMS; DNA MUTATIONAL ANALYSIS; DNA, NEOPLASM; HUMANS; MUTATION; NEOPLASTIC CELLS, CIRCULATING; PROGNOSIS;

EID: 85006990389     PISSN: 0284186X     EISSN: 1651226X     Source Type: Journal    
DOI: 10.1080/0284186X.2016.1253861     Document Type: Review

References (95)

1. 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.
2. 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.
3. 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.
4. 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.
5. 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.
6. Heitzer E, Ulz P, Geigl JB., Circulating tumor DNA as a liquid biopsy for cancer. Clin Chem. 2015;61:112–123.
7. 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.
8. Mandel P., METAIS P Les acides nucléiques du plasma sanguin chez l'homme. C R Seances Soc Biol Fil. 1948;142:241–243.
9. 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.
10. 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.
11. 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.
12. 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.
13. Stroun M, Maurice P, Vasioukhin V, et al. The origin and mechanism of circulating DNA. Ann NY Acad Sci. 2000;906:161–168.
14. 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.
15. 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.
16. 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.
17. De Mattos-Arruda L, Olmos D, Tabernero J., Prognostic and predictive roles for circulating biomarkers in gastrointestinal cancer. Future Oncol. 2011;7:1385–1397.
18. 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.
19. 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.
20. 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.
21. Fleischhacker M, Schmidt B., Cell-free DNA resuscitated for tumor testing. Nat Med. 2008;14:914–915.
22. 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.
23. 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.
24. El Messaoudi S, Rolet F, Mouliere F, et al. Circulating cell free DNA:Preanalytical considerations. Clin Chim Acta. 2013;424:222–30.
25. 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.
26. 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.
27. 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.
28. 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.
29. 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.
30. 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.
31. Bronkhorst AJ, Aucamp J, Pretorius PJ., Cell-free DNA:preanalytical variables. Clin Chim Acta. 2015;450:243–253.
32. 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.
33. 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.
34. 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.
35. 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.
36. 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.
37. 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.
38. 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.
39. 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.
40. 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.
41. 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.
42. 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.
43. 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.
44. 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.
45. 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.
46. 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.
47. 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.
48. 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.
49. 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.
50. Lui YY1, Dennis YM., Circulating DNA in plasma and serum:biology, preanalytical issues and diagnostic applications. Clin Chem Lab Med. 2002;40:962–968.
51. 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.
52. Zonta E, Nizard P, Taly V., Assessment of DNA integrity, applications for cancer research. Adv Clin Chem. 2015;70:197–246.
53. 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.
54. 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.
55. 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.
56. 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.
57. 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.
58. 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.
59. 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.
60. 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.
61. 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.
62. 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.
63. 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.
64. Perkins G, Yap TA, et al. Multi-purpose utility of circulating plasma DNA testing in patients with advanced cancers. PLoS One. 2012;7:e47020.
65. 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.
66. 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.
67. 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.
68. 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.
69. 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.
70. 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.
71. 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.
72. 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.
73. 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.
74. 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.
75. 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.
76. 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.
77. Dawson SJ, Rosenfeld N, Caldas C., Circulating tumor DNA to monitor metastatic breast cancer. N Engl J Med. 2013;369:93–94.
78. 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.
79. 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.
80. 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.
81. Diehl F, Schmidt K, Choti MA., Circulating mutant DNA to assess tumor dynamics. Nat Med. 2008;14:985–990.
82. 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.
83. 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.
84. 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.
85. 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.
86. 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.
87. Rogosnitzky M, Danks R., Validation of blood testing for K-ras mutations in colorectal and pancreatic cancer. Anticancer Res. 2010;30:2943–2947.
88. 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.
89. 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.
90. 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.
91. 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.
92. 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.
93. 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.
94. 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.
95. 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.