Ultra-fast, label-free isolation of circulating tumor cells from blood using spiral microfluidics (original) (raw)

• Jemal, A. et al. Global cancer statistics. CA Cancer J. Clin. 61, 69–90 (2011).
  Google Scholar
• Esmaeilsabzali, H., Beischlag, T.V., Cox, M.E., Parameswaran, A.M. & Park, E.J. Detection and isolation of circulating tumor cells: principles and methods. Biotechnol. Adv. 31, 1063–1084 (2013).
  Article CAS Google Scholar
• Gupta, G.P. & Massagué, J. Cancer metastasis: building a framework. Cell 127, 679–695 (2006).
  Article CAS Google Scholar
• van de Stolpe, A., Pantel, K., Sleijfer, S., Terstappen, L.W. & den Toonder, J.M. Circulating tumor cell isolation and diagnostics: toward routine clinical use. Cancer Res. 71, 5955–5960 (2011).
  Article CAS Google Scholar
• Ashworth, T. A case of cancer in which cells similar to those in the tumours were seen in the blood after death. Australian Med. J. 14, 146–149 (1869).
  Google Scholar
• Wittekind, C. & Neid, M. Cancer invasion and metastasis. Oncology 69, 14–16 (2005).
  Article Google Scholar
• Racila, E. et al. Detection and characterization of carcinoma cells in the blood. Proc. Natl. Acad. Sci. 95, 4589–4594 (1998).
  Article CAS Google Scholar
• Adalsteinsson, V.A. & Love, J.C. Toward engineered processes for sequencing-based analysis of single circulating tumor cells. Curr. Opin. Chem. Eng. 4, 97–104 (2014).
  Article Google Scholar
• Majid, E.W. & Lim, C.T. Microfluidic Platforms for Human Disease Cell Mechanics Studies (Springer, 2013).
• Lara, O., Tong, X., Zborowski, M. & Chalmers, J.J. Enrichment of rare cancer cells through depletion of normal cells using density and flow-through, immunomagnetic cell separation. Exp. Hematol. 32, 891–904 (2004).
  Article Google Scholar
• De Giorgi, V. et al. Application of a filtration-and isolation-by-size technique for the detection of circulating tumor cells in cutaneous melanoma. J. Invest. Dermatol. 130, 2440–2447 (2010).
  Article CAS Google Scholar
• Warkiani, M.E. et al. Isoporous micro/nanoengineered membranes. ACS Nano 7, 1882–1904 (2013).
  Article CAS Google Scholar
• Matas, J.-P., Morris, J.F. & Guazzelli, E. Inertial migration of rigid spherical particles in Poiseuille flow. J. Fluid Mech. 515, 171–195 (2004).
  Article Google Scholar
• Whitesides, G.M. The origins and the future of microfluidics. Nature 442, 368–373 (2006).
  Article CAS Google Scholar
• Schwartz, M. Molecular characterization of CTCs. Genet. Eng. Biotechnol. News 33, 36–37 (2013).
  Article Google Scholar
• Nagrath, S. et al. Isolation of rare circulating tumor cells in cancer patients by microchip technology. Nature 450, 1235–1239 (2007).
  Article CAS Google Scholar
• Gleghorn, J.P. et al. Capture of circulating tumor cells from whole blood of prostate cancer patients using geometrically enhanced differential immunocapture (GEDI) and a prostate-specific antibody. Lab Chip 10, 27–29 (2010).
  Article CAS Google Scholar
• Chen, W. et al. Nanoroughened surfaces for efficient capture of circulating tumor cells without using capture antibodies. ACS Nano 7, 566–575 (2012).
  Article Google Scholar
• Wang, S. et al. Highly efficient capture of circulating tumor cells by using nanostructured silicon substrates with integrated chaotic micromixers. Angew. Chem. Int. Ed. Engl. 50, 3084–3088 (2011).
  Article CAS Google Scholar
• Allan, A.L. & Keeney, M. Circulating tumor cell analysis: technical and statistical considerations for application to the clinic. J. Oncol. 2010, 426218 (2010).
  Article Google Scholar
• Thiery, J.P. & Lim, C.T. Tumor dissemination: an EMT affair. Cancer Cell 23, 272–273 (2013).
  Article CAS Google Scholar
• Prang, N. et al. Cellular and complement-dependent cytotoxicity of EpCAM-specific monoclonal antibody MT201 against breast cancer cell lines. Br. J. cancer 92, 342–349 (2005).
  Article CAS Google Scholar
• Maheswaran, S. et al. Detection of mutations in EGFR in circulating lung-cancer cells. N. Engl. J. Med. 359, 366–377 (2008).
  Article CAS Google Scholar
• Riethdorf, S. 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. 16, 2634–2645 (2010).
  Article CAS Google Scholar
• Lacroix, M. Significance, detection and markers of disseminated breast cancer cells. Endocr. Relat. Cancer 13, 1033–1067 (2006).
  Article CAS Google Scholar
• Kemmner, W. Currently used markers for CTC isolation-advantages, limitations and impact on cancer prognosis. J. Clin. Exp. Pathol. 1, 102 (2011).
  Google Scholar
• Pecot, C.V. et al. A novel platform for detection of CK+ and CK CTCs. Cancer Discov. 1, 580–586 (2011).
  Article CAS Google Scholar
• Sieuwerts, A.M. et al. Anti-epithelial cell adhesion molecule antibodies and the detection of circulating normal-like breast tumor cells. J. Natl. Cancer Inst. 101, 61–66 (2009).
  Article CAS Google Scholar
• Fehm, T. et al. Methods for isolating circulating epithelial cells and criteria for their classification as carcinoma cells. Cytotherapy 7, 171–185 (2005).
  Article CAS Google Scholar
• Pachmann, K. et al. Standardized quantification of circulating peripheral tumor cells from lung and breast cancer. Clin. Chem. Lab. Med. 43, 617–627 (2005).
  Article CAS Google Scholar
• Tkaczuk, K.H.R. et al. The significance of circulating epithelial cells in breast cancer patients by a novel negative selection method. Breast Cancer Res. Treat. 111, 355–364 (2008).
  Article Google Scholar
• Alix-Panabières, C. et al. Detection of circulating prostate-specific antigen–secreting cells in prostate cancer patients. Clin. Chem. 51, 1538–1541 (2005).
  Article Google Scholar
• Ozkumur, E. et al. Inertial focusing for tumor antigen–dependent and–independent sorting of rare circulating tumor cells. Sci. Transl. Med. 5, 179ra47 (2013).
  Article Google Scholar
• Yang, L. et al. Optimization of an enrichment process for circulating tumor cells from the blood of head and neck cancer patients through depletion of normal cells. Biotechnol. Bioeng. 102, 521–534 (2009).
  Article CAS Google Scholar
• Munz, M. et al. Side-by-side analysis of five clinically tested anti-EpCAM monoclonal antibodies. Cancer Cell Int. 10, 44 (2010).
  Article Google Scholar
• Chaudhuri, P.K., Ebrahimi Warkiani, E., Jing, T., Kenry & Lim, C.T. Microfluidics for research and applications in oncology. Analyst http://dx.doi.org/10.1039/C5AN00382B (2015).
• Hyun, K.A., Kwon, K., Han, H., Kim, S.I. & Jung, H.I. Microfluidic flow fractionation device for label-free isolation of circulating tumor cells (CTCs) from breast cancer patients. Biosens. Bioelectron. 40, 206–212 (2013).
  Article CAS Google Scholar
• Tan, S.J. et al. Versatile label free biochip for the detection of circulating tumor cells from peripheral blood in cancer patients. Biosens. Bioelectron. 26, 1701–1705 (2010).
  Article CAS Google Scholar
• Warkiani, M.E. et al. Slanted spiral microfluidics for the ultra-fast, label-free isolation of circulating tumor cells. Lab Chip 14, 128–137 (2014).
  Article CAS Google Scholar
• Gertler, R. et al. Detection of circulating tumor cells in blood using an optimized density gradient centrifugation. Recent Results Cancer Res. 162, 149–155 (2003).
  Article Google Scholar
• Hur, S.C., Henderson-MacLennan, N.K., McCabe, E.R. & Di Carlo, D. Deformability-based cell classification and enrichment using inertial microfluidics. Lab Chip 11, 912–920 (2011).
  Article CAS Google Scholar
• Moon, H.S. et al. Continuous separation of breast cancer cells from blood samples using multi-orifice flow fractionation (MOFF) and dielectrophoresis (DEP). Lab Chip 11, 1118–1125 (2011).
  Article CAS Google Scholar
• Huang, S.B. et al. High-purity and label-free isolation of circulating tumor cells (CTCs) in a microfluidic platform by using optically-induced-dielectrophoretic (ODEP) force. Lab Chip 13, 1371–1383 (2013).
  Article CAS Google Scholar
• Cima, I. et al. Label-free isolation of circulating tumor cells in microfluidic devices: current research and perspectives. Biomicrofluidics 7, 011810 (2013).
  Article Google Scholar
• Gao, D. et al. Organoid cultures derived from patients with advanced prostate cancer. Cell 159, 176–187 (2014).
  Article CAS Google Scholar
• Sollier, E. et al. Size-selective collection of circulating tumor cells using Vortex technology. Lab Chip 14, 63–77 (2014).
  Article CAS Google Scholar
• Karabacak, N.M. et al. Microfluidic, marker-free isolation of circulating tumor cells from blood samples. Nat. Protoc. 9, 694–710 (2014).
  Article CAS Google Scholar
• Hou, H. et al. Isolation and retrieval of circulating tumor cells using centrifugal forces. Sci. Rep. 3, 1259 (2013).
  Article Google Scholar
• Warkiani, M.E. et al. An ultra-high-throughput spiral microfluidic biochip for the enrichment of circulating tumor cells. Analyst 139, 3245–3255 (2014).
  Article CAS Google Scholar
• Khoo, B.L. et al. Clinical validation of an ultra-high-throughput spiral microfluidics for the detection and enrichment of viable circulating tumor cells. PLoS ONE 9, e99409 (2014).
  Article Google Scholar
• Segre, G. Radial particle displacements in Poiseuille flow of suspensions. Nature 189, 209–210 (1961).
  Article Google Scholar
• Segre, G. & Silberberg, A. Behaviour of macroscopic rigid spheres in Poiseuille flow Part 2. Experimental results and interpretation. J. Fluid Mech. 14, 136–157 (1962).
  Article Google Scholar
• Karnis, A., Goldsmith, H. & Mason, S. The flow of suspensions through tubes: V. Inertial effects. Can. J. Chem. Eng. 44, 181–193 (1966).
  Article CAS Google Scholar
• Tachibana, M. On the behaviour of a sphere in the laminar tube flows. Rheol. Acta 12, 58–69 (1973).
  Article Google Scholar
• Choi, Y.-S., Seo, K.-W. & Lee, S.-J. Lateral and cross-lateral focusing of spherical particles in a square microchannel. Lab Chip 11, 460–465 (2011).
  Article CAS Google Scholar
• Di Carlo, D., Irimia, D., Tompkins, R.G. & Toner, M. Continuous inertial focusing, ordering, and separation of particles in microchannels. Proc. Natl. Acad. Sci. 104, 18892–18897 (2007).
  Article CAS Google Scholar
• Bhagat, A.A.S., Kuntaegowdanahalli, S.S. & Papautsky, I. Continuous particle separation in spiral microchannels using dean flows and differential migration. Lab Chip 8, 1906–1914 (2008).
  Article CAS Google Scholar
• Dean, W. Fluid motion in a curved channel. Proc. R. Soci. Lond. 121, 402–420 (1928).
  Article Google Scholar
• Di Carlo, D. Inertial microfluidics. Lab Chip 9, 3038–3046 (2009).
  Article CAS Google Scholar
• Hayes, D.F. & Smerage, J.B. Circulating tumor cells. Prog. Mol. Biol. Transl. Sci. 95, 95–112 (2009).
  Article Google Scholar
• Kuntaegowdanahalli, S.S., Bhagat, A.A.S., Kumar, G. & Papautsky, I. Inertial microfluidics for continuous particle separation in spiral microchannels. Lab Chip 9, 2973–2980 (2009).
  Article CAS Google Scholar
• Khoo, B. et al. Ultra-high throughput enrichment of viable circulating tumor cells. in The 15th International Conference on Biomedical Engineering (ICBME 2013, 4th 43, 1–4 (Springer).
• Cristofanilli, M. et al. Circulating tumor cells: a novel prognostic factor for newly diagnosed metastatic breast cancer. J. Clin. Oncol. 23, 1420–1430 (2005).
  Article Google Scholar
• Smerage, J. & Hayes, D. The measurement and therapeutic implications of circulating tumour cells in breast cancer. Br. J. Cancer 94, 8–12 (2006).
  Article CAS Google Scholar
• Yu, M. et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science 339, 580–584 (2013).
  Article CAS Google Scholar
• Payne, R. 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 106, 1790–1797 (2012).
  Article CAS Google Scholar
• Yu, M. et al. Ex vivo culture of circulating breast tumor cells for individualized testing of drug susceptibility. Science 345, 216–220 (2014).
  Article CAS Google Scholar
• Zhang, L. et al. The identification and characterization of breast cancer CTCs competent for brain metastasis. Sci. Transl. Med. 5, 180ra148 (2013).
  Article Google Scholar
• Khoo, B.L. et al. Short-term expansion of breast circulating cancer cells predicts response to anti-cancer therapy. Oncotarget 6, 15578–15593 (2015).
  Article Google Scholar
• Dittrich, P.S. & Manz, A. Lab-on-a-chip: microfluidics in drug discovery. Nat. Rev. Drug Discov. 5, 210–218 (2006).
  Article CAS Google Scholar
• Wu, T.-L. et al. Cell-free DNA: measurement in various carcinomas and establishment of normal reference range. Clin. Chim. Acta 321, 77–87 (2002).
  Article CAS Google Scholar
• Aceto, N. et al. Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis. Cell 158, 1110–1122 (2014).
  Article CAS Google Scholar
• Borgen, E. et al. Standardization of the immunocytochemical detection of cancer cells in BM and blood: I. establishment of objective criteria for the evaluation of immunostained cells. Cytotherapy 1, 377–388 (1999).
  Article CAS Google Scholar
• Al-Hajj, M., Wicha, M.S., Benito-Hernandez, A., Morrison, S.J. & Clarke, M.F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. USA 100, 3983–3988 (2003).
  Article CAS Google Scholar
• Li, X. et al. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J. Natl. Cancer Inst. 100, 672–679 (2008).
  Article CAS Google Scholar
• Friedl, P. & Gilmour, D. Collective cell migration in morphogenesis, regeneration and cancer. Nat. Rev. Mol. Cell Biol. 10, 445–457 (2009).
  Article CAS Google Scholar