Circulating tumor cells: A review of present methods and the need to identify heterogeneous phenotypes

Annals of Clinical and Laboratory Science

Volumn 43, Issue 3, 2013, Pages 295-304

  Millner, Lori M ^a   Linder, Mark W ^a   Valdes, Roland ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITHELIAL CELL ADHESION MOLECULE; LAPATINIB; TUMOR MARKER;

ARTICLE; BREAST CANCER; BREAST METASTASIS; CANCER DIAGNOSIS; CANCER LOCALIZATION; CANCER THERAPY; CELL DENSITY; CELL LINE; CELL SELECTION; CELL SEPARATION; CIRCULATING TUMOR CELL; CLINICAL EFFECTIVENESS; DRUG ACTIVITY; EARLY DIAGNOSIS; ENRICHMENT CULTURE; FLUORESCENCE; FLUORESCENCE IN SITU HYBRIDIZATION; HUMAN; METASTASIS; MICROFLUIDIC ANALYSIS; NUCLEIC ACID ANALYSIS; PHENOTYPE; PREDICTIVE VALUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TREATMENT OUTCOME;

CELL SEPARATION; HUMANS; NEOPLASMS; NEOPLASTIC CELLS, CIRCULATING; PHENOTYPE; TUMOR MARKERS, BIOLOGICAL;

EID: 84880973536     PISSN: 00917370     EISSN: 15508080     Source Type: Journal    
DOI: None     Document Type: Article

References (85)

1. Fidler, I. J. (2003) The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat Rev Cancer 3, 453-458
2. Chambers, A. F., Groom, A. C., and MacDonald, I. C. (2002) Dissemination and growth of cancer cells in metastatic sites. Nat Rev Cancer 2, 563-572
3. Yeatman, T. J., and Nicolson, G. L. (1993) Molecular basis of tumor progression: mechanisms of organ-specific tumor metastasis. Seminars in surgical oncology 9, 256-263
4. Naoe, M., Ogawa, Y., Morita, J., Omori, K., Takeshita, K., Shichijyo, T., Okumura, T., Igarashi, A., Yanaihara, A., Iwamoto, S., Fukagai, T., Miyazaki, A., and Yoshida, H. (2007) Detection of circulating urothelial cancer cells in the blood using the CellSearch System. Cancer 109, 1439-1445
5. Wolfrum, F., Vogel, I., Fandrich, F., and Kalthoff, H. (2005) Detection and clinical implications of minimal residual disease in gastro-intestinal cancer. Langenbeck's archives of surgery/Deutsche Gesellschaft fur Chirurgie 390, 430-441
6. Makarovskiy, A. N., Ackerley, W., 3rd, Wojcik, L., Halpert, G. K., Stein, B. S., Carreiro, M. P., and Hixson, D. C. (1997) Application of immunomagnetic beads in combination with RT-PCR for the detection of circulating prostate cancer cells. Journal of clinical laboratory analysis 11, 346-350
7. Allard, W. J., Matera, J., Miller, M. C., Repollet, M., Connelly, M. C., Rao, C., Tibbe, A. G., Uhr, J. W., and Terstappen, L. W. (2004) Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases. Clin Cancer Res 10, 6897-6904
8. Cristofanilli, M., Budd, G. T., Ellis, M. J., Stopeck, A., Matera, J., Miller, M. C., Reuben, J. M., Doyle, G. V., Allard, W. J., Terstappen, L. W., and Hayes, D. F. (2004) Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N Engl J Med 351, 781-791
9. Choy, A., and McCulloch, P. G. (1993) Detection and enumeration of circulating tumour cells in colorectal cancer. The British journal of surgery 80, 1490
10. Negin, B. P., and Cohen, S. J. (2010) Circulating tumor cells in colorectal cancer: past, present, and future challenges. Current treatment options in oncology 11, 1-13
11. Resel Folkersma, L., Olivier Gomez, C., San Jose Manso, L., Veganzones de Castro, S., Galante Romo, I., Vidaurreta Lazaro, M., de la Orden, G. V., Arroyo Fernandez, M., Diaz Rubio, E., Silmi Moyano, A., and Maestro de Las Casas, M. A. (2010) Immunomagnetic quantification of circulating tumoral cells in patients with prostate cancer: clinical and pathological correlation. Archivos espanoles de urologia 63, 23-31
12. Punnoose, E. A., Atwal, S. K., Spoerke, J. M., Savage, H., Pandita, A., Yeh, R. F., Pirzkall, A., Fine, B. M., Amler, L. C., Chen, D. S., and Lackner, M. R. (2010) Molecular biomarker analyses using circulating tumor cells. PLoS One 5, e12517
13. Millner, L. M., Linder, M. W., Valdes, R. Jr., (May 23-27, 2012) Advances in Cell Separation Technologies: Isolation of Circulating Tumor Cells. Association of Clinical Scientists, Mobile, Al.
14. Dupont Jensen, J., Laenkholm, A. V., Knoop, A., Ewertz, M., Bandaru, R., Liu, W., Hackl, W., Barrett, J. C., and Gardner, H. (2011) PIK3CA mutations may be discordant between primary and corresponding metastatic disease in breast cancer. Clin Cancer Res 17, 667-677
15. Pestrin, M., Bessi, S., Puglisi, F., Minisini, A. M., Masci, G., Battelli, N., Ravaioli, A., Gianni, L., Di Marsico, R., Tondini, C., Gori, S., Coombes, C. R., Stebbing, J., Biganzoli, L., Buyse, M., and Di Leo, A. (2012) Final results of a multicenter phase II clinical trial evaluating the activity of single-agent lapatinib in patients with HER2-negative metastatic breast cancer and HER2-positive circulating tumor cells. A proof-ofconcept study. Breast Cancer Res Treat
16. Paterlini-Brechot, P. (2011) Organ-specific markers in circulating tumor cell screening: an early indicator of metastasis-capable malignancy. Future Oncol 7, 849-871
17. Lara, J. F., Young, S. M., Velilla, R. E., Santoro, E. J., and Templeton, S. F. (2003) The relevance of occult axillary micrometastasis in ductal carcinoma in situ: a clinicopathologic study with long-term follow-up. Cancer 98, 2105-2113
18. Weaver, D. L. (2003) Occult "micrometastases" in ductal carcinoma in situ: investigative implications for sentinel lymph node biopsy. Cancer 98, 2083-2087
19. Lianidou, E. S., and Markou, A. (2011) Circulating tumor cells in breast cancer: detection systems, molecular characterization, and future challenges. Clinical chemistry 57, 1242-1255
20. Zhe, X., Cher, M. L., and Bonfil, R. D. (2011) Circulating tumor cells: finding the needle in the haystack. American journal of cancer research 1, 740-751
21. Mego, M., De Giorgi, U., Dawood, S., Wang, X., Valero, V., Andreopoulou, E., Handy, B., Ueno, N. T., Reuben, J. M., and Cristofanilli, M. (2011) Characterization of metastatic breast cancer patients with nondetectable circulating tumor cells. Int J Cancer 129, 417-423
22. Ross, A. A., Cooper, B. W., Lazarus, H. M., Mackay, W., Moss, T. J., Ciobanu, N., Tallman, M. S., Kennedy, M. J., Davidson, N. E., Sweet, D., and et al. (1993) Detection and viability of tumor cells in peripheral blood stem cell collections from breast cancer patients using immunocytochemical and clonogenic assay techniques. Blood 82, 2605-2610
23. Zieglschmid, V., Hollmann, C., and Bocher, O. (2005) Detection of disseminated tumor cells in peripheral blood. Critical reviews in clinical laboratory sciences 42, 155-196
24. Noble, P. B., and Cutts, J. H. (1967) Separation of blood leukocytes by Ficoll gradient. The Canadian veterinary journal. La revue veterinaire canadienne 8, 110-111
25. Rosenberg, R., Gertler, R., Friederichs, J., Fuehrer, K., Dahm, M., Phelps, R., Thorban, S., Nekarda, H., and Siewert, J. R. (2002) Comparison of two density gradient centrifugation systems for the enrichment of disseminated tumor cells in blood. Cytometry 49, 150-158
26. Carroll, S., and Al-Rubeai, M. (2005) ACSD labelling and magnetic cell separation: a rapid method of separating antibody secreting cells from non-secreting cells. Journal of immunological methods 296, 171-178
27. Talasaz, A. H., Powell, A. A., Huber, D. E., Berbee, J. G., Roh, K. H., Yu, W., Xiao, W., Davis, M. M., Pease, R. F., Mindrinos, M. N., Jeffrey, S. S., and Davis, R. W. (2009) Isolating highly enriched populations of circulating epithelial cells and other rare cells from blood using a magnetic sweeper device. Proceedings of the National Academy of Sciences of the United States of America 106, 3970-3975
28. Chalmers, J. J., Zborowski, M., Sun, L., and Moore, L. (1998) Flow through, immunomagnetic cell separation. Biotechnology progress 14, 141-148
29. Yellen, B. B., Erb, R. M., Son, H. S., Hewlin, R., Jr., Shang, H., and Lee, G. U. (2007) Traveling wave magnetophoresis for high resolution chip based separations. Lab Chip 7, 1681-1688
30. Pamme, N., and Manz, A. (2004) On-chip free-flow magnetophoresis: continuous flow separation of magnetic particles and agglomerates. Analytical chemistry 76, 7250-7256
31. Adams, J. D., Kim, U., and Soh, H. T. (2008) Multitarget magnetic activated cell sorter. Proceedings of the National Academy of Sciences of the United States of America 105, 18165-18170
32. Vona, G., Sabile, A., Louha, M., Sitruk, V., Romana, S., Schutze, K., Capron, F., Franco, D., Pazzagli, M., Vekemans, M., Lacour, B., Brechot, C., and Paterlini-Brechot, P. (2000) Isolation by size of epithelial tumor cells: a new method for the immunomorphological and molecular characterization of circulatingtumor cells. The American journal of pathology 156, 57-63
33. Mohamed, H., Murray, M., Turner, J. N., and Caggana, M. (2009) Isolation of tumor cells using size and deformation. Journal of chromatography. A 1216, 8289-8295
34. Tan, S. J., Yobas, L., Lee, G. Y., Ong, C. N., and Lim, C. T. (2009) Microdevice for the isolation and enumeration of cancer cells from blood. Biomedical microdevices 11, 883-892
35. Zheng, S., Lin, H., Liu, J. Q., Balic, M., Datar, R., Cote, R. J., and Tai, Y. C. (2007) Membrane microfilter device for selective capture, electrolysis and genomic analysis of human circulating tumor cells. Journal of chromatography. A 1162, 154-161
36. Marrinucci, D., Bethel, K., Bruce, R. H., Curry, D. N., Hsieh, B., Humphrey, M., Krivacic, R. T., Kroener, J., Kroener, L., Ladanyi, A., Lazarus, N. H., Nieva, J., and Kuhn, P. (2007) Case study of the morphologic variation of circulating tumor cells. Human pathology 38, 514-519
37. Tong, X., Xiong, Y., Zborowski, M., Farag, S. S., and Chalmers, J. J. (2007) A novel high throughput immunomagnetic cell sorting system for potential clinical scale depletion of T cells for allogeneic stem cell transplantation. Experimental hematology 35, 1613-1622
38. Tong, X., Yang, L., Lang, J. C., Zborowski, M., and Chalmers, J. J. (2007) Application of immunomagnetic cell enrichment in combination with RT-PCR for the detection of rare circulating head and neck tumor cells in human peripheral blood. Cytometry. Part B, Clinical cytometry 72, 310-323
39. Basu, S., Campbell, H. M., Dittel, B. N., and Ray, A. (2010) Purification of specific cell population by fluorescence activated cell sorting (FACS). J Vis Exp
40. Shapiro, H. M. (2003) Practical Flow Cytometry, John Wiley & Sons, Inc., Hoboken, N.J.
41. Mattanovich, D., and Borth, N. (2006) Applications of cell sorting in biotechnology. Microbial cell factories 5, 12
42. Arnold, L. W., and Lannigan, J. (2010) Practical issues in highspeed cell sorting. Current protocols in cytometry/editorial board, J. Paul Robinson, managing editor... [et al.] Chapter 1, Unit 1 24 21-30
43. Krivacic, R. T., Ladanyi, A., Curry, D. N., Hsieh, H. B., Kuhn, P., Bergsrud, D. E., Kepros, J. F., Barbera, T., Ho, M. Y., Chen, L. B., Lerner, R. A., and Bruce, R. H. (2004) A rare-cell detector for cancer. Proceedings of the National Academy of Sciences of the United States of America 101, 10501-10504
44. Hsieh, H. B., Marrinucci, D., Bethel, K., Curry, D. N., Humphrey, M., Krivacic, R. T., Kroener, J., Kroener, L., Ladanyi, A., Lazarus, N., Kuhn, P., Bruce, R. H., and Nieva, J. (2006) High speed detection of circulating tumor cells. Biosensors & bioelectronics 21, 1893-1899
45. Smith, B. M., Slade, M. J., English, J., Graham, H., Luchtenborg, M., Sinnett, H. D., Cross, N. C., and Coombes, R. C. (2000) 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 18, 1432-1439
46. de Cremoux, P., Extra, J. M., Denis, M. G., Pierga, J. Y., Bourstyn, E., Nos, C., Clough, K. B., Boudou, E., Martin, E. C., Muller, A., Pouillart, P., and Magdelenat, H. (2000) Detection of MUC1-expressing mammary carcinoma cells in the peripheral blood of breast cancer patients by real-time polymerase chain reaction. Clin Cancer Res 6, 3117-3122
47. Hardingham, J. E., Hewett, P. J., Sage, R. E., Finch, J. L., Nuttall, J. D., Kotasek, D., and Dobrovic, A. (2000) Molecular detection of blood-borne epithelial cells in colorectal cancer patients and in patients with benign bowel disease. Int J Cancer 89, 8-13
48. Wu, C. H., Lin, S. R., Yu, F. J., Wu, D. C., Pan, Y. S., Hsieh, J. S., Huang, S. Y., and Wang, J. Y. (2006) Development of a high-throughput membrane-array method for molecular diagnosis of circulating tumor cells in patients with gastric cancers. Int J Cancer 119, 373-379
49. Louha, M., Poussin, K., Ganne, N., Zylberberg, H., Nalpas, B., Nicolet, J., Capron, F., Soubrane, O., Vons, C., Pol, S., Beaugrand, M., Berthelot, P., Franco, D., Trinchet, J. C., Brechot, C., and Paterlini, P. (1997) Spontaneous and iatrogenic spreading of liver-derived cells into peripheral blood of patients with primary liver cancer. Hepatology 26, 998-1005
50. Kowalewska, M., Chechlinska, M., Markowicz, S., Kober, P., and Nowak, R. (2006) The relevance of RT-PCR detection of disseminated tumour cells is hampered by the expression of markers regarded as tumour-specific in activated lymphocytes. Eur J Cancer 42, 2671-2674
51. Feldman, B., Ebrahim, S. A., Hazan, S. L., Gyi, K., Johnson, M. P., Johnson, A., and Evans, M. I. (2000) Routine prenatal diagnosis of aneuploidy by FISH studies in high-risk pregnancies. American journal of medical genetics 90, 233-238
52. Evans, M. I., Sharp, M., Tepperberg, J., Kilpatrick, M. W., Tsipouras, P., and Tafas, T. (2006) Automated microscopy of amniotic fluid cells: detection of FISH signals using the FastFISH imaging system. Fetal diagnosis and therapy 21, 523-527
53. Kilpatrick, M. W., Tafas, T., Evans, M. I., Jackson, L. G., Antsaklis, A., Brambati, B., and Tsipouras, P. (2004) Automated detection of rare fetal cells in maternal blood: eliminating the false-positive XY signals in XX pregnancies. American journal of obstetrics and gynecology 190, 1571-1578; discussion 1578-1581
54. Ntouroupi, T. G., Ashraf, S. Q., McGregor, S. B., Turney, B. W., Seppo, A., Kim, Y., Wang, X., Kilpatrick, M. W., Tsipouras, P., Tafas, T., and Bodmer, W. F. (2008) Detection of circulating tumour cells in peripheral blood with an automated scanning fluorescence microscope. British journal of cancer 99, 789-795
55. Pethig, R., Menachery, A., Pells, S., and De Sousa, P. (2010) Dielectrophoresis: a review of applications for stem cell research. Journal of biomedicine & biotechnology 2010, 182581
56. Abonnenc, M., Borgatti, M., Romani, A., Altomare, L., Fabbri, E., Mancini, I., Medoro, G., Freida, D., Tartagni, M., Nastruzzi, C., Gambari, R., Baricordi, O., Rizzo, R., Guerrieri, R., and Manaresi, M. (2005) A Dielectrophoretic Microchip for Controlled Cell Targeting With Functionalized Microspheres. Nano Biotechnology 1
57. Fuchs, A. B., Romani, A., Freida, D., Medoro, G., Abonnenc, M., Altomare, L., Chartier, I., Guergour, D., Villiers, C., Marche, P. N., Tartagni, M., Guerrieri, R., Chatelain, F., and Manaresi, N. (2006) Electronic sorting and recovery of single live cells from microlitre sized samples. Lab Chip 6, 121-126
58. Borgatti, M., Altomare, L., Abonnec, M., Fabbri, E., Manaresi, N., Medoro, G., Romani, A., Tartagni, M., Nastruzzi, C., Di Croce, S., Tosi, A., Mancini, I., Guerrieri, R., and Gambari, R. (2005) Dielectrophoresis-based 'Lab-on-a-chip' devices for programmable binding of microspheres to target cells. International journal of oncology 27, 1559-1566 Circulating Tumor Cells 303
59. Cristofanilli, M., Broglio, K. R., Guarneri, V., Jackson, S., Fritsche, H. A., Islam, R., Dawood, S., Reuben, J. M., Kau, S. W., Lara, J. M., Krishnamurthy, S., Ueno, N. T., Hortobagyi, G. N., and Valero, V. (2007) Circulating tumor cells in metastatic breast cancer: biologic staging beyond tumor burden. Clinical breast cancer 7, 471-479
60. Dawood, S., Broglio, K., Valero, V., Reuben, J., Handy, B., Islam, R., Jackson, S., Hortobagyi, G. N., Fritsche, H., and Cristofanilli, M. (2008) Circulating tumor cells in metastatic breast cancer: from prognostic stratification to modification of the staging system? Cancer 113, 2422-2430
61. Swaby, R. F., and Cristofanilli, M. (2011) Circulating tumor cells in breast cancer: a tool whose time has come of age. BMC medicine 9, 43
62. Racila, E., Euhus, D., Weiss, A. J., Rao, C., McConnell, J., Terstappen, L. W., and Uhr, J. W. (1998) Detection and characterization of carcinoma cells in the blood. Proceedings of the National Academy of Sciences of the United States of America 95, 4589-4594
63. Riethdorf, S., Fritsche, H., Muller, V., Rau, T., Schindlbeck, C., Rack, B., Janni, W., Coith, C., Beck, K., Janicke, F., Jackson, S., Gornet, T., Cristofanilli, M., and Pantel, K. (2007) Detection of circulating tumor cells in peripheral blood of patients with metastatic breast cancer: a validation study of the CellSearch system. Clin Cancer Res 13, 920-928
64. Farace, F., Massard, C., Vimond, N., Drusch, F., Jacques, N., Billiot, F., Laplanche, A., Chauchereau, A., Lacroix, L., Planchard, D., Le Moulec, S., Andre, F., Fizazi, K., Soria, J. C., and Vielh, P. (2011) A direct comparison of CellSearch and ISET for circulating tumour-cell detection in patients with metastatic carcinomas. British journal of cancer
65. Paterlini-Brechot, P., and Benali, N. L. (2007) Circulating tumor cells (CTC) detection: clinical impact and future directions. Cancer Lett 253, 180-204
66. Andreopoulou, E., Yang, L. Y., Rangel, K. M., Reuben, J. M., Hsu, L., Krishnamurthy, S., Valero, V., Fritsche, H. A., and Cristofanilli, M. (2011) Comparison of assay methods for detection of circulating tumor cells (CTCs) in metastatic breast cancer (MBC): AdnaGen AdnaTest BreastCancer Select/Detect versus Veridex CellSearch system. Int J Cancer
67. Nagrath, S., Sequist, L. V., Maheswaran, S., Bell, D. W., Irimia, D., Ulkus, L., Smith, M. R., Kwak, E. L., Digumarthy, S., Muzikansky, A., Ryan, P., Balis, U. J., Tompkins, R. G., Haber, D. A., and Toner, M. (2007) Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature 450, 1235-1239
68. Stott, S. L., Hsu, C. H., Tsukrov, D. I., Yu, M., Miyamoto, D. T., Waltman, B. A., Rothenberg, S. M., Shah, A. M., Smas, M. E., Korir, G. K., Floyd, F. P., Jr., Gilman, A. J., Lord, J. B., Winokur, D., Springer, S., Irimia, D., Nagrath, S., Sequist, L. V., Lee, R. J., Isselbacher, K. J., Maheswaran, S., Haber, D. A., and Toner, M. (2010) Isolation of circulating tumor cells using a microvortex-generating herringbone-chip. Proceedings of the National Academy of Sciences of the United States of America 107, 18392-18397
69. Alix-Panabieres, C., Vendrell, J. P., Pelle, O., Rebillard, X., Riethdorf, S., Muller, V., Fabbro, M., and Pantel, K. (2007) Detection and characterization of putative metastatic precursor cells in cancer patients. Clinical chemistry 53, 537-539
70. Alix-Panabieres, C., Brouillet, J. P., Fabbro, M., Yssel, H., Rousset, T., Maudelonde, T., Choquet-Kastylevsky, G., and Vendrell, J. P. (2005) Characterization and enumeration of cells secreting tumor markers in the peripheral blood of breast cancer patients. Journal of immunological methods 299, 177-188
71. Alix-Panabieres, C., Muller, V., and Pantel, K. (2007) Current status in human breast cancer micrometastasis. Current opinion in oncology 19, 558-563
72. Deng, G., Herrler, M., Burgess, D., Manna, E., Krag, D., and Burke, J. F. (2008) 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 10, R69
73. Tse, J. C., and Kalluri, R. (2007) Mechanisms of metastasis: epithelial-to-mesenchymal transition and contribution of tumor microenvironment. Journal of cellular biochemistry 101, 816-829
74. Thompson, E. W., Newgreen, D. F., and Tarin, D. (2005) Carcinoma invasion and metastasis: a role for epithelial-mesenchymal transition? Cancer research 65, 5991-5995; discussion 5995
75. Frederick, B. A., Helfrich, B. A., Coldren, C. D., Zheng, D., Chan, D., Bunn, P. A., Jr., and Raben, D. (2007) Epithelial to mesenchymal transition predicts gefitinib resistance in cell lines of head and neck squamous cell carcinoma and non-small cell lung carcinoma. Molecular cancer therapeutics 6, 1683-1691
76. Powell, A. A., Talasaz, A. H., Zhang, H., Coram, M. A., Reddy, A., Deng, G., Telli, M. L., Advani, R. H., Carlson, R. W., Mollick, J. A., Sheth, S., Kurian, A. W., Ford, J. M., Stockdale, F. E., Quake, S. R., Pease, R. F., Mindrinos, M. N., Bhanot, G., Dairkee, S. H., Davis, R. W., and Jeffrey, S. S. (2012) Single cell profiling of circulating tumor cells: transcriptional heterogeneity and diversity from breast cancer cell lines. PLoS One 7, e33788
77. Balic, M., Dandachi, N., Hofmann, G., Samonigg, H., Loibner, H., Obwaller, A., van der Kooi, A., Tibbe, A. G., Doyle, G. V., Terstappen, L. W., and Bauernhofer, T. (2005) Comparison of two methods for enumerating circulating tumor cells in carcinoma patients. Cytometry. Part B, Clinical cytometry 68, 25-30
78. Becker, S., Becker-Pergola, G., Banys, M., Krawczyk, N., Wallwiener, D., Solomayer, E., Schuetz, C., and Fehm, T. (2009) Evaluation of a RT-PCR based routine screening tool for the detection of disseminated epithelial cells in the bone marrow of breast cancer patients. Breast Cancer Res Treat 117, 227-233
79. Ibrahim, S. F., and van den Engh, G. (2007) Flow cytometry and cell sorting. Advances in biochemical engineering/biotechnology 106, 19-39
80. Mollet, M., Godoy-Silva, R., Berdugo, C., and Chalmers, J. J. (2008) Computer simulations of the energy dissipation rate in a fluorescence-activated cell sorter: Implications to cells. Biotechnology and bioengineering 100, 260-272
81. Stahlberg, A., and Bengtsson, M. (2010) Single-cell gene expression profiling using reverse transcription quantitative realtime PCR. Methods 50, 282-288
82. Borgatti, M., Bianchi, N., Mancini, I., Feriotto, G., and Gambari, R. (2008) New trends in non-invasive prenatal diagnosis: applications of dielectrophoresis-based Lab-on-a-chip platforms to the identification and manipulation of rare cells. International journal of molecular medicine 21, 3-12
83. Mulhall, H. J., Labeed, F. H., Kazmi, B., Costea, D. E., Hughes, M. P., and Lewis, M. P. (2011) Cancer, pre-cancer and normal oral cells distinguished by dielectrophoresis. Analytical and bioanalytical chemistry
84. de Bono, J. S., Scher, H. I., Montgomery, R. B., Parker, C., Miller, M. C., Tissing, H., Doyle, G. V., Terstappen, L. W., Pienta, K. J., and Raghavan, D. (2008) Circulating tumor cells predict survival benefit from treatment in metastatic castration- resistant prostate cancer. Clin Cancer Res 14, 6302-6309
85. Naoe, M., Ogawa, Y., Takeshita, K., Iwamoto, S., and Miyazaki, A. (2008) Use of the CellSearch Circulating Tumor Cell Test for monitoring urothelial cancer: two case reports of metastatic urothelial cancer. South Med J 101, 439-441