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Classifying circulating tumor cells to monitor cancer progression

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Pages 153-165 | Received 26 Oct 2016, Accepted 19 Dec 2016, Published online: 29 Dec 2016

References

  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin. 2015;65(1):5–29.
  • Bellassai N, Spoto G. Biosensors for liquid biopsy: circulating nucleic acids to diagnose and treat cancer. Anal Bioanal Chem. 2016;408:7255–7264.
  • Matikas A, Syrigos KN, Agelaki S. Circulating biomarkers in non-small-cell lung cancer: current status and future challenges. Clin Lung Cancer. 2016;17:507–516.
  • Gerlinger M, Rowan AJ, Horswell S, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med. 2012;366(10):883–892.
  • Lianidou ES, Mavroudis D, Georgoulias V. Clinical challenges in the molecular characterization of circulating tumour cells in breast cancer. Br J Cancer. 2013;108(12):2426–2432.
  • Crowley E, Di Nicolantonio F, Loupakis F, et al. Liquid biopsy: monitoring cancer-genetics in the blood. Nat Rev Clin Oncol. 2013;10(8):472–484.
  • Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100(1):57–70.
  • Caceres G, Puskas JA, Magliocco AM. Circulating tumor cells: a window into tumor development and therapeutic effectiveness. Cancer Control. 2015;22(2):167–176.
  • 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;14(19):6302–6309.
  • Cristofanilli M, Budd GT, Ellis MJ, et al. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N Engl J Med. 2004;351(8):781–791.
  • 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;23(7):1420–1430.
  • Krebs MG, Sloane R, Priest L, et al. Evaluation and prognostic significance of circulating tumor cells in patients with non-small-cell lung cancer. J Clin Oncol. 2011;29(12):1556–1563.
  • Barbazán J, Muinelo-Romay L, Vieito M, et al. A multimarker panel for circulating tumor cells detection predicts patient outcome and therapy response in metastatic colorectal cancer. Int J Cancer. 2014;135(11):2633–2643.
  • Hiltermann TJ, Pore MM, van den Berg A, et al. Circulating tumor cells in small-cell lung cancer: a predictive and prognostic factor. Ann Oncol. 2012;23(11):2937–2942.
  • Muthukkaruppan VR, Kubai L, Auerbach R. Tumor-induced neovascularization in the mouse eye. J Natl Cancer Inst. 1982;69(3):699–708.
  • Morgan CD. Observations on cancer: its pathology, and its relations to the organism and to other morbid growths. Lancet. 1874;103(2636):325–329.
  • Ashworth T. A case of cancer in which cells similar to those in the tumors were seen in the blood after death. Aust Med J. 1869;14:146–147.
  • Tsai W-S, Chen J-S, Shao H-J, et al. Circulating tumor cell count correlates with colorectal neoplasm progression and is a prognostic marker for distant metastasis in non-metastatic patients. Sci Rep. 2016;6:24517.
  • Alix-Panabieres C, Pantel K. Clinical applications of circulating tumor cells and circulating tumor DNA as liquid biopsy. Cancer Discov. 2016;6(5):479–491.
  • Alix-Panabieres C, Pantel K. Challenges in circulating tumour cell research. Nat Rev Cancer. 2014;14(9):623–631.
  • Kasimir-Bauer, S., Hoffmann O, Wallwiener D, et al. Expression of stem cell and epithelial-mesenchymal transition markers in primary breast cancer patients with circulating tumor cells. Breast Cancer Res. 2012;14(1):R15.
  • Méhes G, Witt A, Kubista E, et al. Circulating breast cancer cells are frequently apoptotic. Am J Pathol. 2001;159(1):17–20.
  • Hanna N. Inhibition of experimental tumor metastasis by selective activation of natural killer cells. Cancer Res. 1982;42(4):1337–1342.
  • Klein CA. Parallel progression of primary tumours and metastases. Nat Rev Cancer. 2009;9(4):302–312.
  • Bulfoni M, Turetta M, Del Ben F, et al. Dissecting the heterogeneity of circulating tumor cells in metastatic breast cancer: going far beyond the needle in the haystack. Int J Mol Sci. 2016;17(10):1775.
  • Thiery JP. Epithelial-mesenchymal transitions in development and pathologies. Curr Opin Cell Biol. 2003;15(6):740–746.
  • Tibbe AG, Miller MC, Terstappen LW. Statistical considerations for enumeration of circulating tumor cells. Cytometry A. 2007;71(3):154–162.
  • Broersen LH, van Pelt GW, Tollenaar RAEM, et al. Clinical application of circulating tumor cells in breast cancer. Cell Oncol (Dordr). 2014;37(1):9–15.
  • Lianidou ES, Markou A. Circulating tumor cells in breast cancer: detection systems, molecular characterization, and future challenges. Clin Chem. 2011;57(9):1242–1255.
  • Miller MC, Doyle GV, Terstappen LW. Significance of circulating tumor cells detected by the cellsearch system in patients with metastatic breast colorectal and prostate cancer. J Oncol. 2010;2010:1–8.
  • Went PT, Lugli A, Meier S, et al. Frequent EpCam protein expression in human carcinomas. Hum Pathol. 2004;35(1):122–128.
  • Barriere, G., Fici P, Gallerani G, et al. Circulating tumor cells and epithelial, mesenchymal and stemness markers: characterization of cell subpopulations. Ann Transl Med. 2014;2(11):109.
  • Tan SJ, Lakshmi RL, Chen P, et al. Versatile label free biochip for the detection of circulating tumor cells from peripheral blood in cancer patients. Biosens Bioelectron. 2010;26(4):1701–1705.
  • Lianidou ES, Markou A. Circulating tumor cells as emerging tumor biomarkers in breast cancer. Clin Chem Lab Med. 2011;49(10):1579–1590.
  • Sieuwerts AM, Mostert B, Bolt-De Vries J, et al. mRNA and microRNA expression profiles in circulating tumor cells and primary tumors of metastatic breast cancer patients. Clin Cancer Res. 2011;17(11):3600–3618.
  • Hofman P, Popper HH. Pathologists and liquid biopsies: to be or not to be? Virchows Arch. 2016;469(6):601–609.
  • Xenidis N, Perraki M, Kafousi M, et al. Predictive and prognostic value of peripheral blood cytokeratin-19 mRNA-positive cells detected by real-time polymerase chain reaction in node-negative breast cancer patients. J Clin Oncol. 2006;24(23):3756–3762.
  • 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.
  • Ramirez JM, Fehm T, Orsini M, et al. Prognostic relevance of viable circulating tumor cells detected by EPISPOT in metastatic breast cancer patients. Clin Chem. 2014;60(1):214–221.
  • 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;12(14 Pt 1):4218–4224.
  • 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.
  • 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;32(31):3483–3489.
  • Bidard FC, Pierga JY. Clinical utility of circulating tumor cells in metastatic breast cancer. J Clin Oncol. 2015;33(14):1622.
  • Bidard FC, Proudhon C, Pierga JY. Circulating tumor cells in breast cancer. Mol Oncol. 2016;10(3):418–430.
  • Alunni-Fabbroni M, Müller V, Fehm T, et al. Monitoring in metastatic breast cancer: is imaging outdated in the era of circulating tumor cells? Breast Care (Basel). 2014;9(1):16–21.
  • Androulakis N, Agelaki S, Perraki M, et al. Clinical relevance of circulating CK-19mRNA-positive tumour cells before front-line treatment in patients with metastatic breast cancer. Br J Cancer. 2012;106(12):1917–1925.
  • Reinholz MM, Kitzmann KA, Tenner K, et al. Cytokeratin-19 and mammaglobin gene expression in circulating tumor cells from metastatic breast cancer patients enrolled in North Central Cancer Treatment Group trials, N0234/336/436/437. Clin Cancer Res. 2011;17(22):7183–7193.
  • Georgoulias V, Apostolaki S, Bozionelou V, et al. Effect of front-line chemotherapy on circulating CK-19 mRNA-positive cells in patients with metastatic breast cancer. Cancer Chemother Pharmacol. 2014;74(6):1217–1225.
  • Pierga JY, 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. 2008;14(21):7004–7010.
  • 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;32(1–2):179–188.
  • 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.
  • Stathopoulou A, Gizi A, Perraki M, et al. Real-time quantification of CK-19 mRNA-positive cells in peripheral blood of breast cancer patients using the lightcycler system. Clin Cancer Res. 2003;9(14):5145–5151.
  • Stathopoulou A, Ntoulia M, Perraki M, et al. A highly specific real-time RT-PCR method for the quantitative determination of CK-19 mRNA positive cells in peripheral blood of patients with operable breast cancer. Int J Cancer. 2006;119(7):1654–1659.
  • Xenidis N, Markos V, Apostolaki S, et al. Clinical relevance of circulating CK-19 mRNA-positive cells detected during the adjuvant tamoxifen treatment in patients with early breast cancer. Ann Oncol. 2007;18(10):1623–1631.
  • 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.
  • Saloustros, E., Perraki M, Apostolaki S, et al. Cytokeratin-19 mRNA-positive circulating tumor cells during follow-up of patients with operable breast cancer: prognostic relevance for late relapse. Breast Cancer Res. 2011;13(3):R60.
  • Xenidis N, Perraki M, Apostolaki S, et al. Differential effect of adjuvant taxane-based and taxane-free chemotherapy regimens on the CK-19 mRNA-positive circulating tumour cells in patients with early breast cancer. Br J Cancer. 2013;108(3):549–556.
  • 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):1–11.
  • 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.
  • Bozionellou V, Mavroudis D, Perraki M, et al. Trastuzumab administration can effectively target chemotherapy-resistant cytokeratin-19 messenger RNA-positive tumor cells in the peripheral blood and bone marrow of patients with breast cancer. Clin Cancer Res. 2004;10(24):8185–8194.
  • Agelaki S, Kalykaki A, Markomanolaki H, et al. Efficacy of lapatinib in therapy-resistant HER2-positive circulating tumor cells in metastatic breast cancer. PLoS One. 2015;10(6):e0123683.
  • Georgoulias V, Bozionelou V, Agelaki S, et al. Trastuzumab decreases the incidence of clinical relapses in patients with early breast cancer presenting chemotherapy-resistant CK-19mRNA-positive circulating tumor cells: results of a randomized phase II study. Ann Oncol. 2012;23(7):1744–1750.
  • Schneck H, Blassl C, Meier-Stiegen F, et al. Analysing the mutational status of PIK3CA in circulating tumor cells from metastatic breast cancer patients. Mol Oncol. 2013;7(5):976–986.
  • Goodman, O.B., Jr., Fink LM, Symanowski JT, et al. Circulating tumor cells in patients with castration-resistant prostate cancer baseline values and correlation with prognostic factors. Cancer Epidemiol Biomarkers Prev. 2009;18(6):1904–1913.
  • Olmos D, Arkenau H-T, Ang JE, et al. Circulating tumour cell (CTC) counts as intermediate end points in castration-resistant prostate cancer (CRPC): a single-centre experience. Ann Oncol. 2009;20(1):27–33.
  • Thalgott M, Rack B, Maurer T, et al. Detection of circulating tumor cells in different stages of prostate cancer. J Cancer Res Clin Oncol. 2013;139(5):755–763.
  • Coumans FA, Doggen CJM, Attard G, et al. All circulating EpCAM+CK+CD45- objects predict overall survival in castration-resistant prostate cancer. Ann Oncol. 2010;21(9):1851–1857.
  • Scher HI, Jia X, De Bono JS, et al. Circulating tumour cells as prognostic markers in progressive, castration-resistant prostate cancer: a reanalysis of IMMC38 trial data. Lancet Oncol. 2009;10(3):233–239.
  • Scher HI, Heller G, Molina A, et al. Circulating tumor cell biomarker panel as an individual-level surrogate for survival in metastatic castration-resistant prostate cancer. J Clin Oncol. 2015;33(12):1348–1355.
  • Lorente D, Olmos D, Mateo J, et al. Decline in circulating tumor cell count and treatment outcome in advanced prostate cancer. Eur Urol. 2016;70:985–992.
  • Antonarakis ES, Lu C, Wang H, et al. AR-V7 and resistance to enzalutamide and abiraterone in prostate cancer. N Engl J Med. 2014;371(11):1028–1038.
  • Crespo M, van Dalum G, Ferraldeschi R, et al. Androgen receptor expression in circulating tumour cells from castration-resistant prostate cancer patients treated with novel endocrine agents. Br J Cancer. 2015;112(7):1166–1174.
  • Antonarakis ES, Lu C, Luber B, et al. Androgen receptor splice variant 7 and efficacy of Taxane chemotherapy in patients with metastatic castration-resistant prostate cancer. JAMA Oncol. 2015;1(5):582–591.
  • Scher HI, Lu D, Schreiber NA, et al. Association of AR-V7 on circulating tumor cells as a treatment-specific biomarker with outcomes and survival in castration-resistant prostate cancer. JAMA Oncol. 2016;2:1441.
  • Thalgott, M., Rack B, Eiber M, et al. Categorical versus continuous circulating tumor cell enumeration as early surrogate marker for therapy response and prognosis during docetaxel therapy in metastatic prostate cancer patients. BMC Cancer. 2015;15:458.
  • Onstenk W, Sieuwerts AM, Kraan J, et al. Efficacy of cabazitaxel in castration-resistant prostate cancer is independent of the presence of AR-V7 in circulating tumor cells. Eur Urol. 2015;68(6):939–945.
  • Thadani-Mulero M, Portella L, Sun S, et al. Androgen receptor splice variants determine taxane sensitivity in prostate cancer. Cancer Res. 2014;74(8):2270–2282.
  • Cohen SJ, Punt CJA, 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;26(19):3213–3221.
  • Sastre J, Maestro ML, Puente J, et al. Circulating tumor cells in colorectal cancer: correlation with clinical and pathological variables. Ann Oncol. 2008;19(5):935–938.
  • Jiao LR, Apostolopoulos C, Jacob J, et al. Unique localization of circulating tumor cells in patients with hepatic metastases. J Clin Oncol. 2009;27(36):6160–6165.
  • Lalmahomed ZS, Mostert B, Onstenk W, et al. Prognostic value of circulating tumour cells for early recurrence after resection of colorectal liver metastases. Br J Cancer. 2015;112(3):556–561.
  • Musella V, Pietrantonio F, Di Buduo E, et al. Circulating tumor cells as a longitudinal biomarker in patients with advanced chemorefractory, RAS-BRAF wild-type colorectal cancer receiving cetuximab or panitumumab. Int J Cancer. 2015;137(6):1467–1474.
  • Abdallah EA, Fanelli MF, Buim MEC, et al. Thymidylate synthase expression in circulating tumor cells: a new tool to predict 5-fluorouracil resistance in metastatic colorectal cancer patients. Int J Cancer. 2015;137(6):1397–1405.
  • Satelli A, Brownlee Z, Mitra A, et al. Circulating tumor cell enumeration with a combination of epithelial cell adhesion molecule- and cell-surface vimentin-based methods for monitoring breast cancer therapeutic response. Clin Chem. 2015;61(1):259–266.
  • Bork U, Rahbari NN, Schölch S, et al. Circulating tumour cells and outcome in non-metastatic colorectal cancer: a prospective study. Br J Cancer. 2015;112(8):1306–1313.
  • Iinuma H, Watanabe T, Mimori K, et al. Clinical significance of circulating tumor cells, including cancer stem-like cells, in peripheral blood for recurrence and prognosis in patients with Dukes’ stage B and C colorectal cancer. J Clin Oncol. 2011;29(12):1547–1555.
  • Vardakis N, Messaritakis I, Papadaki C, et al. Prognostic significance of the detection of peripheral blood CEACAM5mRNA-positive cells by real-time polymerase chain reaction in operable colorectal cancer. Clin Cancer Res. 2011;17(1):165–173.
  • Lu CY, Uen Y-H, Tsai H-L, et al. Molecular detection of persistent postoperative circulating tumour cells in stages II and III colon cancer patients via multiple blood sampling: prognostic significance of detection for early relapse. Br J Cancer. 2011;104(7):1178–1184.
  • Bessa X, Piñol V, Castellví-Bel S, et al. Prognostic value of postoperative detection of blood circulating tumor cells in patients with colorectal cancer operated on for cure. Ann Surg. 2003;237(3):368–375.
  • Fabbri F, Carloni S, Zoli W, et al. Detection and recovery of circulating colon cancer cells using a dielectrophoresis-based device: KRAS mutation status in pure CTCs. Cancer Lett. 2013;335(1):225–231.
  • Kalikaki A, Politaki H, Souglakos J, et al. KRAS genotypic changes of circulating tumor cells during treatment of patients with metastatic colorectal cancer. PLoS One. 2014;9(8):e104902.
  • Manzoni M, Comolli G, Torchio M, et al. Circulating endothelial cells and their subpopulations: role as predictive biomarkers in antiangiogenic therapy for colorectal cancer. Clin Colorectal Cancer. 2015;14(1):11–17.
  • Muinelo-Romay L, Vieito M, Abalo A, et al. Evaluation of circulating tumor cells and related events as prognostic factors and surrogate biomarkers in advanced NSCLC patients receiving first-line systemic treatment. Cancers (Basel). 2014;6(1):153–165.
  • Krebs MG, Hou J-M, Sloane R, et al. Analysis of circulating tumor cells in patients with non-small cell lung cancer using epithelial marker-dependent and -independent approaches. J Thorac Oncol. 2012;7(2):306–315.
  • Hofman V, Bonnetaud C, Ilie MI, et al. Preoperative circulating tumor cell detection using the isolation by size of epithelial tumor cell method for patients with lung cancer is a new prognostic biomarker. Clin Cancer Res. 2011;17(4):827–835.
  • Gorges TM, Penkalla N, Schalk T, et al. Enumeration and molecular characterization of tumor cells in lung cancer patients using a novel in vivo device for capturing circulating tumor cells. Clin Cancer Res. 2016;22(9):2197–2206.
  • Hirose T, Murata Y, Oki Y, et al. Relationship of circulating tumor cells to the effectiveness of cytotoxic chemotherapy in patients with metastatic non-small-cell lung cancer. Oncol Res. 2012;20(2–3):131–137.
  • Pailler E, Adam J, Barthélémy A, et al. Detection of circulating tumor cells harboring a unique ALK rearrangement in ALK-positive non-small-cell lung cancer. J Clin Oncol. 2013;31(18):2273–2281.
  • Nicolazzo C, Raimondi C, Mancini M, et al. Monitoring PD-L1 positive circulating tumor cells in non-small cell lung cancer patients treated with the PD-1 inhibitor Nivolumab. Sci Rep. 2016;6:31726.
  • Ilie M, Hofman V, Long-Mira E, et al. “Sentinel” circulating tumor cells allow early diagnosis of lung cancer in patients with chronic obstructive pulmonary disease. PLoS One. 2014;9(10):e111597.

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