Enumeration and molecular characterization of circulating tumor cells as an innovative tool for companion diagnostics in breast cancer

References

• Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science. 2011 Mar 25;331(6024):815–828.
   Web of Science ®Google Scholar
• Ashworth TR. A case of cancer in which cells similar to those in the tumours were seen in the blood after death. Aust Med J. 1869;14:146.
   Google Scholar
• Nadel E. Prefatory remarks for symposium issue of acta cytologica. Acta Cytol. 1965;9:346–350.
   PubMed Web of Science ®Google Scholar
• Coons AH, Kaplan MH. Localization of antigen in tissue cells: II. Improvements in a method for the detection of antigen by means of fluorescent antibody. J Exp Med. 1950;91(1):1–13.
   PubMed Web of Science ®Google Scholar
• Siegel R, Ma J, Zou Z, et al. Cancer statistics, 2014. CA-a cancer j clinicians. 2014;64(1):9–29.
   PubMed Web of Science ®Google Scholar
• Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin. 2018 Jan;68(1):7–30.
   PubMed Web of Science ®Google Scholar
• Clare SE, Sener SF, Wilkens W, et al. Prognostic significance of occult lymph node metastases in node-negative breast cancer. Ann Surg Oncol. 1997;4(6):447–451.
   PubMed Web of Science ®Google Scholar
• Braun S, Pantel K, Müller P, et al. Cytokeratin-positive cells in the bone marrow and survival of patients with stage I, II, or III breast cancer. N Engl J Med. 2000;342(8):525–533.
   PubMed Web of Science ®Google Scholar
• Weiss L. Metastasis of cancer: a conceptual history from antiquity to the 1990s. Cancer Metastasis Rev. 2000;19(3-4):I-xi, 193-383..
   PubMedGoogle Scholar
• Cristofanilli M, Budd GT, Ellis MJ, et al. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N Engl J Med. 2004 Aug 19;351(8):781–791..
   PubMed Web of Science ®Google Scholar
• Cohen SJ, Punt CJ, Iannotti N, et al. Relationship of circulating tumor cells to tumor response, progression-free survival, and overall survival in patients with metastatic colorectal cancer. J Clin Oncol. 2008 Jul 1;26(19):3213–3221.
   PubMed Web of Science ®Google Scholar
• Moreno JG, O’Hara SM, Gross S, et al. Changes in circulating carcinoma cells in patients with metastatic prostate cancer correlate with disease status. Urology. 2001 Sep;58(3):386–392.
   PubMed Web of Science ®Google Scholar
• de Bono JS, Scher HI, Montgomery RB, et al. Circulating tumor cells predict survival benefit from treatment in metastatic castration-resistant prostate cancer. Clin Cancer Res. 2008 Oct 1;14(19):6302–6309.
   PubMed Web of Science ®Google Scholar
• Allard WJ, Matera J, Miller MC, et al. Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases. Clin Cancer Res. 2004 Oct 15;10(20):6897–6904.
   PubMed Web of Science ®Google Scholar
• Mostert B, Kraan J, Bolt-de Vries J, et al. Detection of circulating tumor cells in breast cancer may improve through enrichment with anti-CD146. Breast Cancer Res Treat. 2011 May;127(1):33–41.
   PubMed Web of Science ®Google Scholar
• Mani SA, Guo W, Liao M-J, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008;133(4):704–715.
   PubMed Web of Science ®Google Scholar
• Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest. 2009;119(6):1420–1428.
   PubMed Web of Science ®Google Scholar
• Yu M, Bardia A, Wittner BS, et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science. 2013 Feb 1;339(6119):580–584.
   PubMed Web of Science ®Google Scholar
• Vona G, Sabile A, Louha M, et al. Isolation by size of epithelial tumor cells: a new method for the immunomorphological and molecular characterization of circulating tumor cells. Am J Pathol. 2000;156(1):57–63.
   PubMed Web of Science ®Google Scholar
• Fehm T, Hoffmann O, Aktas B, et al. Detection and characterization of circulating tumor cells in blood of primary breast cancer patients by RT-PCR and comparison to status of bone marrow disseminated cells. Breast Cancer Res. 2009;11(4):R59.
   PubMed Web of Science ®Google Scholar
• Fehm T, Müller V, Aktas B, et al. HER2 status of circulating tumor cells in patients with metastatic breast cancer: a prospective, multicenter trial. Breast Cancer Res Treat. 2010 Nov;124(2):403–412.
   PubMed Web of Science ®Google Scholar
• Van der Auwera I, Peeters D, Benoy I, et al. Circulating tumour cell detection: a direct comparison between the cellsearch system, the adnaTest and CK-19/mammaglobin RT–PCR in patients with metastatic breast cancer. Br J Cancer. 2010;102(2):276–284.
   PubMed Web of Science ®Google Scholar
• Nagrath S, Sequist LV, Maheswaran S, et al. Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature. 2007 Dec 20;450(7173):1235–1239.
   PubMed Web of Science ®Google Scholar
• Stott SL, Hsu CH, Tsukrov DI, et al. Isolation of circulating tumor cells using a microvortex-generating herringbone-chip. Proc Natl Acad Sci U S A. 2010 Oct 26;107(43):18392–18397.
   PubMed Web of Science ®Google Scholar
• Yoon HJ, Kim TH, Zhang Z, et al. Sensitive capture of circulating tumour cells by functionalized graphene oxide nanosheets. Nat Nanotechnol. 2013;8(10):735.
   PubMed Web of Science ®Google Scholar
• Talasaz AH, Powell AA, Huber DE, et al. Isolating highly enriched populations of circulating epithelial cells and other rare cells from blood using a magnetic sweeper device. Proc Nat Acad Sci. 2009;106(10):3970–3975.
   PubMed Web of Science ®Google Scholar
• Alix-Panabières C, Pantel K. Circulating tumor cells: liquid biopsy of cancer. Clin Chem. 2013;59(1):110–118.
   PubMed Web of Science ®Google Scholar
• Zheng S, Lin H, Liu JQ, et al. Membrane microfilter device for selective capture, electrolysis and genomic analysis of human circulating tumor cells. J Chromatogr A. 2007 Aug 31;1162(2):154–161.
   PubMed Web of Science ®Google Scholar
• Xenidis N, Ignatiadis M, Apostolaki S, et al. Cytokeratin-19 mRNA-positive circulating tumor cells after adjuvant chemotherapy in patients with early breast cancer. J Clin Oncol. 2009;27(13):2177–2184.
   PubMed Web of Science ®Google Scholar
• Stathopoulou A, Vlachonikolis I, Mavroudis D, et al. Molecular detection of cytokeratin-19–positive cells in the peripheral blood of patients with operable breast cancer: evaluation of their prognostic significance. J Clin Oncol. 2002;20(16):3404–3412.
   PubMed Web of Science ®Google Scholar
• Ignatiadis M, Xenidis N, Perraki M, et al. Different prognostic value of cytokeratin-19 mrna–positive circulating tumor cells according to estrogen receptor and HER2 status in early-stage breast cancer. J Clin Oncol. 2007;25(33):5194–5202.
   PubMed Web of Science ®Google Scholar
• Payne R, Wang F, Su N, et al. Viable circulating tumour cell detection using multiplex RNA in situ hybridisation predicts progression-free survival in metastatic breast cancer patients. Br J Cancer. 2012;106(11):1790–1797.
   PubMed Web of Science ®Google Scholar
• Pachmann K, Clement JH, Schneider C-P, et al. Standardized quantification of circulating peripheral tumor cells from lung and breast cancer. Clin Chem Lab Med. 2005;43(6):617–627.
   PubMed Web of Science ®Google Scholar
• Deng G, Herrler M, Burgess D, et al. Enrichment with anti-cytokeratin alone or combined with anti-EpCAM antibodies significantly increases the sensitivity for circulating tumor cell detection in metastatic breast cancer patients. Breast Cancer Res. 2008;10(4):R69.
   PubMed Web of Science ®Google Scholar
• Zhao M, Schiro PG, Kuo JS, et al. An automated high-throughput counting method for screening circulating tumor cells in peripheral blood. Anal Chem. 2013;85(4):2465–2471.
   PubMed Web of Science ®Google Scholar
• Hvichia GE, Parveen Z, Wagner C, et al. A novel microfluidic platform for size and deformability based separation and the subsequent molecular characterization of viable circulating tumor cells. Int J Cancer. 2016 Jun 15;138(12):2894–2904.
   PubMed Web of Science ®Google Scholar
• Hayes DF, Cristofanilli M, Budd GT, et al. Circulating tumor cells at each follow-up time point during therapy of metastatic breast cancer patients predict progression-free and overall survival. Clin Cancer Res. 2006 Jul 15;12(14 Pt 1):4218–4224.
   PubMed Web of Science ®Google Scholar
• Bidard F-C, Peeters DJ, Fehm T, et al. Clinical validity of circulating tumour cells in patients with metastatic breast cancer: a pooled analysis of individual patient data. Lancet Oncol. 2014;15(4):406–414.
   PubMed Web of Science ®Google Scholar
• Nolé F, Munzone E, Zorzino L, et al. Variation of circulating tumor cell levels during treatment of metastatic breast cancer: prognostic and therapeutic implications. Ann Oncol. 2008;19(5):891–897.
   PubMed Web of Science ®Google Scholar
• Budd GT, Cristofanilli M, Ellis MJ, et al. Circulating tumor cells versus imaging–predicting overall survival in metastatic breast cancer. Clin Cancer Res. 2006 Nov 1;12(21):6403–6409.
   PubMed Web of Science ®Google Scholar
• Smith BM, Slade MJ, English J, et al. Response of circulating tumor cells to systemic therapy in patients with metastatic breast cancer: comparison of quantitative polymerase chain reaction and immunocytochemical techniques. J Clin Oncol. 2000;18(7):1432–1439.
   PubMed Web of Science ®Google Scholar
• Cristofanilli M, Hayes DF, Budd GT, et al. Circulating tumor cells: a novel prognostic factor for newly diagnosed metastatic breast cancer. J Clin Oncol. 2005 Mar 1;23(7):1420–1430.
   PubMed Web of Science ®Google Scholar
• Andreopoulou E, Yang LY, Rangel KM, et al. Comparison of assay methods for detection of circulating tumor cells in metastatic breast cancer: adnaGen AdnaTest BreastCancer Select/Detect versus Veridex CellSearch system. Int J Cancer. 2012 Apr 1;130(7):1590–1597.
   PubMed Web of Science ®Google Scholar
• Smerage JB, Barlow WE, Hortobagyi GN, et al. Circulating tumor cells and response to chemotherapy in metastatic breast cancer: SWOG S0500. J Clin Oncol. 2014 Nov 1;32(31):3483–3489.
   PubMed Web of Science ®Google Scholar
• Sparano JA, Henry NL. Surveillance after treatment of localized breast cancer: time for reappraisal? J Natl Cancer Inst. 2019 Apr 1;111(4):339–341.
   PubMedGoogle Scholar
• Cabel L, Proudhon C, Gortais H, et al. Circulating tumor cells: clinical validity and utility. Int J Clin Oncol. 2017 Jun;22(3):421–430.
   PubMed Web of Science ®Google Scholar
• McInnes LM, Jacobson N, Redfern A, et al. Clinical implications of circulating tumor cells of breast cancer patients: role of epithelial-mesenchymal plasticity. Front Oncol. 2015;5:42.
   PubMed Web of Science ®Google Scholar
• Giordano A, Egleston BL, Hajage D, et al. Establishment and validation of circulating tumor cell-based prognostic nomograms in first-line metastatic breast cancer patients. Clin Cancer Res. 2013 Mar 15;19(6):1596–1602.
   PubMed Web of Science ®Google Scholar
• Giuliano AE, Connolly JL, Edge SB, et al. Breast cancer—major changes in the American joint committee on cancer eighth edition cancer staging manual. CA Cancer J Clin. 2017;67(4):290–303.
   PubMed Web of Science ®Google Scholar
• Harris L, Fritsche H, Mennel R, et al. American society of clinical oncology 2007 update of recommendations for the use of tumor markers in breast cancer. J Clin Oncol. 2007;25(33):5287–5312.
   PubMed Web of Science ®Google Scholar
• Febbo PG, Ladanyi M, Aldape KD, et al. NCCN task force report: evaluating the clinical utility of tumor markers in oncology. J Natl Compr Canc Netw. 2011 Nov;9(Suppl 5):S1–32. quiz S33.
   PubMed Web of Science ®Google Scholar
• Theriault RL, Carlson RW, Allred C, et al. Breast cancer, version 3.2013: featured updates to the NCCN guidelines. J Natl Compr Canc Netw. 2013 Jul;11(7):753–760. quiz 761.
   PubMed Web of Science ®Google Scholar
• Rack B, Andergassen U, Janni W, et al. CTCs in primary breast cancer (I). Recent Results Cancer Res. 2012;195:179–185.
   PubMedGoogle Scholar
• Mikulova V, Čabiňaková M, Janatkova I, et al. Detection of circulating tumor cells during follow-up of patients with early breast cancer: clinical utility for monitoring of therapy efficacy. Scand J Clin Lab Invest. 2014;74(2):132–142.
   PubMed Web of Science ®Google Scholar
• Rack B, Andergassen U, Janni W, et al. CTCs in primary breast cancer (I). Minimal Residual Dis Circulating Tumor Cells in Breast Cancer: Springer. 2012; 179–185.
   Google Scholar
• Lucci A, Hall CS, Lodhi AK, et al. Circulating tumour cells in non-metastatic breast cancer: a prospective study. Lancet Oncol. 2012;13(7):688–695.
   PubMed Web of Science ®Google Scholar
• Rack B, Schindlbeck C, Jückstock J, et al. Circulating tumor cells predict survival in early average-to-high risk breast cancer patients. J Natl Cancer Inst. 2014;106(5):dju066.
   PubMedGoogle Scholar
• Serrano MJ, Rovira PS, Martínez-Zubiaurre I, et al. Dynamics of circulating tumor cells in early breast cancer under neoadjuvant therapy. Exp Ther Med. 2012;4(1):43–48.
   PubMed Web of Science ®Google Scholar
• Pierga J-Y, Bidard F-C, Mathiot C, et al. Circulating tumor cell detection predicts early metastatic relapse after neoadjuvant chemotherapy in large operable and locally advanced breast cancer in a phase II randomized trial. Clin Cancer Res off J Am Assoc Cancer Res. 2008;14(21):7004–7010.
   PubMed Web of Science ®Google Scholar
• Riethdorf S, Fritsche H, Muller V, et al. Detection of circulating tumor cells in peripheral blood of patients with metastatic breast cancer: a validation study of the cellsearch system. Clin Cancer Res. 2007 Feb 1;13(3):920–928.
   PubMed Web of Science ®Google Scholar
• Riethdorf S, Müller V, Zhang L, et al. Detection and HER2 expression of circulating tumor cells: prospective monitoring in breast cancer patients treated in the neoadjuvant GeparQuattro trial. Clin Cancer Res off J Am Assoc Cancer Res. 2010;16(9):2634–2645.
   PubMed Web of Science ®Google Scholar
• Somlo G, Lau SK, Frankel P, et al. Multiple biomarker expression on circulating tumor cells in comparison to tumor tissues from primary and metastatic sites in patients with locally advanced/inflammatory, and stage IV breast cancer, using a novel detection technology. Breast Cancer Res Treat. 2011;128(1):155–163.
   PubMed Web of Science ®Google Scholar
• Stebbing J, Payne R, Reise J, et al. The efficacy of lapatinib in metastatic breast cancer with HER2 non-amplified primary tumors and EGFR positive circulating tumor cells: a proof-of-concept study. PloS One. 2013;8(5):e62543–e62543.
   PubMed Web of Science ®Google Scholar
• Bidard FC, Fehm T, Ignatiadis M, et al. Clinical application of circulating tumor cells in breast cancer: overview of the current interventional trials. Cancer Metastasis Rev. 2013 Jun;32(1–2):179–188..
   PubMed Web of Science ®Google Scholar
• Schochter F, Friedl TWP, deGregorio A, et al. Are circulating tumor cells (CTCs) ready for clinical use in breast cancer? An overview of completed and ongoing trials using CTCs for clinical treatment decisions. Cells. 2019 Nov 8;8(11):1412.
   PubMed Web of Science ®Google Scholar
• Bidard F, Jacot W, Dureau S, et al. Abstract GS3-07: clinical utility of circulating tumor cell count as a tool to chose between first line hormone therapy and chemotherapy for ER+ HER2-metastatic breast cancer: results of the phase III STIC CTC trial. AACR. 2019;79(4 Supplement):GS3-07-GS3-07.
   Google Scholar
• Paoletti C, Miao J, Dolce EM, et al. Circulating tumor cell clusters in patients with metastatic breast cancer: a SWOG S0500 translational medicine study. Clin Cancer Res off J Am Assoc Cancer Res. 2019;25(20):6089–6097.
   PubMed Web of Science ®Google Scholar
• Epstein FH, Schnipper LE. Clinical implications of tumor-cell heterogeneity. N Engl J Med. 1986 May 29;314(22):1423–1431.
   PubMed Web of Science ®Google Scholar
• Hayes DF, Paoletti C. Circulating tumour cells: insights into tumour heterogeneity. J Intern Med. 2013 Aug;274(2):137–143.
   PubMed Web of Science ®Google Scholar
• Schrijver WA, Suijkerbuijk KP, Van Gils CH, et al. Receptor conversion in distant breast cancer metastases: a systematic review and meta-analysis. JNCI. 2018;110(6):568–580.
   PubMedGoogle Scholar
• Yamanouchi K, Kuba S, Eguchi S. Hormone receptor, human epidermal growth factor receptor-2, and Ki-67 status in primary breast cancer and corresponding recurrences or synchronous axillary lymph node metastases. Surg Today. 2019 Jul;50(7):657-663.
   PubMed Web of Science ®Google Scholar
• Aceto N, Bardia A, Miyamoto DT, et al. Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis. Cell. 2014 Aug 28;158(5):1110–1122.
   PubMed Web of Science ®Google Scholar
• Hayes DF, Smerage JB. Circulating tumor cells. Prog Mol Biol Transl Sci. 2010;95:95–112.
   PubMed Web of Science ®Google Scholar
• Wang C, Mu Z, Ye Z, et al. Prognostic value of HER2 status on circulating tumor cells in advanced-stage breast cancer patients with HER2-negative tumors. Breast Cancer Res Treat. 2020 Jun;181(3):679–689.
   PubMed Web of Science ®Google Scholar
• Le Du F, Fujii T, Kida K, et al. EpCAM-independent isolation of circulating tumor cells with epithelial-to-mesenchymal transition and cancer stem cell phenotypes using apostream(R) in patients with breast cancer treated with primary systemic therapy. PLoS One. 2020;15(3):e0229903.
   PubMed Web of Science ®Google Scholar
• Flores L, Kindelberger D, Ligon A, et al. Improving the yield of circulating tumour cells facilitates molecular characterisation and recognition of discordant HER2 amplification in breast cancer. Br J Cancer. 2010;102(10):1495–1502.
   PubMed Web of Science ®Google Scholar
• Cristofanilli M, Pierga JY, Reuben J, et al. The clinical use of circulating tumor cells (CTCs) enumeration for staging of metastatic breast cancer (MBC): international expert consensus paper. Crit Rev Oncol Hematol. 2019 Feb;134:39–45.
   PubMed Web of Science ®Google Scholar